Skip to main content

Main menu

  • HOME
  • CONTENT
    • Early Release
    • Featured
    • Current Issue
    • Issue Archive
    • Collections
    • Podcast
  • ALERTS
  • FOR AUTHORS
    • Information for Authors
    • Fees
    • Journal Clubs
    • eLetters
    • Submit
  • EDITORIAL BOARD
  • ABOUT
    • Overview
    • Advertise
    • For the Media
    • Rights and Permissions
    • Privacy Policy
    • Feedback
  • SUBSCRIBE

User menu

  • Log out
  • Log in
  • My Cart

Search

  • Advanced search
Journal of Neuroscience
  • Log out
  • Log in
  • My Cart
Journal of Neuroscience

Advanced Search

Submit a Manuscript
  • HOME
  • CONTENT
    • Early Release
    • Featured
    • Current Issue
    • Issue Archive
    • Collections
    • Podcast
  • ALERTS
  • FOR AUTHORS
    • Information for Authors
    • Fees
    • Journal Clubs
    • eLetters
    • Submit
  • EDITORIAL BOARD
  • ABOUT
    • Overview
    • Advertise
    • For the Media
    • Rights and Permissions
    • Privacy Policy
    • Feedback
  • SUBSCRIBE
PreviousNext
Viewpoints

Activity Shapes Neural Circuit Form and Function: A Historical Perspective

Yuan Pan and Michelle Monje
Journal of Neuroscience 29 January 2020, 40 (5) 944-954; DOI: https://doi.org/10.1523/JNEUROSCI.0740-19.2019
Yuan Pan
Department of Neurology and Neurological Sciences, Stanford University, Stanford, California 94305
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Michelle Monje
Department of Neurology and Neurological Sciences, Stanford University, Stanford, California 94305
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Michelle Monje
  • Article
  • Figures & Data
  • Info & Metrics
  • eLetters
  • PDF
Loading

Abstract

The brilliant and often prescient hypotheses of Ramon y Cajal have proven foundational for modern neuroscience, but his statement that “In adult centers the nerve paths are something fixed, ended, immutable … ” is an exception that did not stand the test of empirical study. Mechanisms of cellular and circuit-level plasticity continue to shape and reshape many regions of the adult nervous system long after the neurodevelopmental period. Initially focused on neurons alone, the field has followed a meteoric trajectory in understanding of activity-regulated neurodevelopment and ongoing neuroplasticity with an arc toward appreciating neuron–glial interactions and the role that each neural cell type plays in shaping adaptable neural circuity. In this review, as part of a celebration of the 50th anniversary of Society for Neuroscience, we provide a historical perspective, following this arc of inquiry from neuronal to neuron–glial mechanisms by which activity and experience modulate circuit structure and function. The scope of this consideration is broad, and it will not be possible to cover the wealth of knowledge about all aspects of activity-dependent circuit development and plasticity in depth.

Introduction

Neuronal activity, the electrical activity of neurons, governs neural circuit formation during prenatal/perinatal neurodevelopment and neural circuit function/plasticity during adulthood (LoTurco et al., 1995; Leclerc et al., 2001; Luk et al., 2003; Deisseroth et al., 2004; Luk and Sadikot, 2004; Tozuka et al., 2005; Song et al., 2013; Paez-Gonzalez et al., 2014). Establishment of synaptic connectivity begins as a diffuse process that is refined in an activity-dependent manner during development (for review, see Shatz, 1990; Katz and Shatz, 1996). Ongoing adaptive changes to dynamic circuit function are then mediated throughout life by plasticity in the strength and number of individual synapses, the establishment and elimination of synaptic connections, and alterations to spike timing. Over the past several decades of research, it has become increasingly clear that mechanisms of neuronal connectivity and circuit function require the cooperative activities of neurons together with each class of glial cells: astrocytes, oligodendrocytes, and microglia. Herein, we review the role of neuronal activity in neural circuit assembly and function throughout neurodevelopment and adulthood, with additional focus on roles of glial cells in this process.

Principles of activity-dependent circuit development

Spontaneous neuronal activity in early neurodevelopment

The critical role of neuronal activity in neurodevelopment was first appreciated in the beautifully patterned visual system, with highly ordered synaptic connections. The initial neuron migration, differentiation, and synaptic connections of the visual system are guided by molecular cues. These processes lead to excessive neuronal arborization and synaptic connections that are refined by spontaneous and then visually evoked activity-dependent mechanisms. Herein, we define activity-dependent as the dependence on neuronal activity. Retinal ganglion cells (RGCs) from the retina project to the lateral geniculate nucleus (LGN) in the visual thalamus, and from LGN to layer 4 of the primary visual cortex (Fig. 1). Many early studies of spontaneous neuronal activity focused on segregation of axonal projections from the eyes, a process that is initiated before birth when visual experience-dependent neuronal activity is absent. During the prenatal period, the input from two eyes is segregated into distinct layers in the LGN by remodeling the axon branches and synaptic connections of RGCs (Sretavan and Shatz, 1984, 1986; Campbell and Shatz, 1992). Similarly, in the visual cortex, neurons that respond preferentially to one eye are segregated from neurons that respond preferentially to the other eye in structures called ocular dominance columns, a phenomenon discovered by Hubel and Wiesel (1969) around the time of the first Society for Neuroscience (SfN) conference. Contemporaneously, Hubel and Wiesel (1969) reported another organized visual cortex structure, orientation columns that respond to a specific line orientation. Both eye segregation and the formation of orientation columns happen before vision-induced neuronal activity is possible (Horton and Hocking, 1996b), indicating the existence of experience-independent mechanisms for early circuit assembly.

Figure 1.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 1.

Illustration of segregation of projections from the eye. The retinal input from two eyes (blue represents left; red represents right) is segregated into distinct layers in the LGN by remodeling the axon branches and synaptic connections of RGCs. In the layer IVc of the primary visual cortex (V1), LGN neurons that respond preferentially to one eye segregate from neurons that respond preferentially to the other eye in structures called ocular dominance columns. Illustration by Sigrid Knemeyer.

Even before eye opening, when photoreceptors cannot transmit information about incoming light, RGCs (the output neurons of the retina) exhibit spontaneous activity that drives neurodevelopment (Galli and Maffei, 1988; Maffei and Galli-Resta, 1990; Meister et al., 1991; Wong et al., 1993). Spontaneous activity is the firing of action potentials without external stimuli and was first recorded in retinal neurons in rat fetuses by Galli and Maffei (1988). Discovery of retinal spontaneous activity was not surprising because its presence in the embryonic retina has long been suspected. In 1990, retinal waves, the synchronized spontaneous activity of neighboring RGCs, were recorded by the same group (Maffei and Galli-Resta, 1990). Retinal waves occur in gap junction-coupled clusters formed by immature retinal neurons that exhibit synchronized membrane depolarization and consequent intracellular calcium waves (Wong et al., 1995; Feller et al., 1996; Pearson et al., 2004).

Spontaneous neuronal activity is required for development of appropriate connectivity. In prenatal cats, infusion of tetrodotoxin (TTX) (a neurotoxin that blocks voltage-gated sodium channels and prevents action potentials) into RGC axons prevents normal arborization and segregation of RGC terminal synapses in the LGN (Shatz and Stryker, 1988; Sretavan et al., 1988). Spontaneous activity similarly shapes development of the visual cortex. Infusion of TTX into the thalamocortical visual pathway before eye opening results in abnormal thalamic axon arborization in the visual cortex of cats (Herrmann and Shatz, 1995), and inhibiting early spontaneous retinal activity leads to abnormal development of ocular dominance columns in visual cortex of ferrets (Huberman et al., 2006).

In the 1950s–1960s, Hubel and Wiesel (1959, 1962) also described the receptive fields of single cells in the visual cortex. Consistent with the findings that most visual pathway circuits are established before visual experience, the receptive fields of cortical cells responding to patterned light are similar in kittens with no prior experience and those in adult experienced cats (Hubel and Wiesel, 1963), as is the selectivity for stimulus orientation in kitten visual cortex (Sherk and Stryker, 1976), underscoring the role of spontaneous activity during early neurodevelopment.

Such spontaneous activity has been demonstrated in other developing brain regions, such as the auditory pathway (Moore and Kitzes, 1985; Kitzes et al., 1995; Russell and Moore, 1995), hippocampus (Ben-Ari et al., 1989; Garaschuk et al., 1998), cerebellum (Watt et al., 2009), and somatosensory cortex (Anton-Bolanos et al., 2019) in many mammalian species (Anderson et al., 1985; Yuste et al., 1992; Horton and Hocking, 1996a; Lamblin et al., 1999; Khazipov et al., 2001, 2004; Leinekugel et al., 2002; Moreno-Juan et al., 2017). In the auditory system, spontaneous activity of auditory neurons is present before the onset of hearing and may contribute to circuit development (for review, see Wang and Bergles, 2015). During this period, inner hair cells generate spontaneous periodic bursts of action potentials, and cochlear ablation/deafferentation results in abnormal synaptic connections in the developing auditory pathway (Moore and Kitzes, 1985; Kitzes et al., 1995; Russell and Moore, 1995). In the immature somatosensory cortex, a recent study demonstrates that spontaneous activity from prenatal thalamic neurons drives the development of functional columnar structures (Anton-Bolanos et al., 2019), furthering the concept that spontaneous neuronal activity is required for early neuronal circuit assembly throughout the CNS.

Experience-dependent neuronal activity in neurodevelopment

Spontaneous activity is critical for early neurodevelopment; however, it is not sufficient for mature circuit formation. Around the time of the first SfN meeting, seminal work began to reveal that experience is critical for circuit refinement (Wiesel and Hubel, 1963a,b). For example, visual experience is required for refinement of synaptic connections at thalamic axon terminals that form the ocular dominance columns in the visual cortex (Hubel et al., 1977; LeVay et al., 1980). Monocular deprivation or strabismus after eye opening leads to a stark increase in neuronal representation of the normal eye in the visual cortex (Hubel and Wiesel, 1965, 1970; Hubel et al., 1977). This shift in ocular dominance induced by monocular deprivation is prevented by intracortical infusion of TTX (Reiter et al., 1986).

Importantly, a critical period exists during which experience-dependent neuronal activity regulates visual system neurodevelopment (Wiesel and Hubel, 1963a,b; Hubel and Wiesel, 1970; Daw et al., 1992). For example, monocular deprivation in kittens during the critical period results in LGN atrophy and diminished cortical response to the deprived eye. However, no such changes are observed in kittens that underwent monocular deprivation outside of the critical period or in adult cats that underwent monocular deprivation, illustrating a critical period for visual experience-dependent development (Wiesel and Hubel, 1963a, b). Together, these studies demonstrated that experience-dependent neuronal activity modulates visual cortex development.

Astrocytes in circuit establishment during neurodevelopment

Understandably, studies of circuit establishment and function were initially focused on neurons. In the 1990s, attention was drawn to glia, which include astrocytes, microglia, and oligodendrocytes in the central nervous system (CNS). Originally thought of as “glue” and as interstitial cells simply playing a supporting role to neurons, glial cells are now understood to be indispensable for proper neurodevelopment and plasticity (the ability of neural cells and circuit function to change continuously) (Fig. 2). The focus was initially on astrocytes, star-shaped glial cells with extensive processes. In the 1980s–1990s, a role for glial cells in sensing neuronal activity was proposed based on the discoveries that glial cells express many neurotransmitter receptors (Pearce et al., 1988; Gallo and Bertolotto, 1990; Barres, 1991). In 1990, attention was drawn to the observation that neurotransmitters, such as glutamate, can elevate intracellular calcium concentration ([Ca2+]i) of astrocytes (Cornell-Bell et al., 1990; Cornell-Bell and Finkbeiner, 1991). Several groups later observed activity-induced [Ca2+]i elevation in astrocytes using hippocampal slice preparations (Dani et al., 1992; Porter and McCarthy, 1996; Pasti et al., 1997). Kriegler and Chiu (1993) and demonstrated an activity-dependent neuron–glia interaction during which activity of axons triggers [Ca2+]i elevation in nonsynaptically associated glial cells.

Figure 2.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 2.

Evolving view of circuit establishment and plasticity. A, Neural circuit establishment involves synaptogenesis between appropriate presynaptic (red) and postsynaptic (orange) neurons and subsequent refinement of synaptic connectivity. B, Astrocytes (green) promote synaptogenesis and modulate synaptic function. Microglia (purple) prune less active synapses, and oligodendrocytes, generated by OPCs (blue), ensheath axons to modulate spike timing and overall circuit dynamics. Together, the major classes of glia promote, support, and alter neural circuit function. Circuit activity influences each process. Illustration by Sigrid Knemeyer.

A massive wave of synaptogenesis occurs in early postnatal life, followed by a period of synapse elimination and circuit refinement, and the onset of this synaptogenic developmental period coincides with the early postnatal maturation of astrocytes (for review, see Chung et al., 2015). Advances in neuronal cell culture techniques enabled direct evaluations of the role astrocytes play in synaptogenesis. In RGC cultures (Meyer-Franke et al., 1995), RGC neurites establish contact with each other, but few synapses form. Addition of astrocytes or astrocyte-conditioned medium results in a massive increase in RGC synapse formation in vitro, indicating that astrocytes secrete synaptogenic factors required for appropriate connectivity (Mauch et al., 2001; Nägler et al., 2001; Ullian et al., 2001; Christopherson et al., 2005; for review, see Ullian et al., 2004). Subsequent work showed that astrocytes promote the formation of both excitatory and inhibitory synapses in various organisms (Elmariah et al., 2005; Colón-Ramos et al., 2007; Hughes et al., 2010; Muthukumar et al., 2014). Concordantly, glial ablation during synaptogenesis in Drosophila results in 50% reduction in synapse number (Muthukumar et al., 2014). Furthermore, a large number of astrocytic genes are regulated by synaptic activity (Hasel et al., 2017). For example, the activity of GABAergic neurons is required for increased expression of astrocytic GABA transporters during Drosophila synaptogenesis (Muthukumar et al., 2014). Astrocytes in turn mediate synaptogenesis via both secreted [e.g., hevin and secreted protein acidic and rich in cysteine (SPARC)] and membrane-bound factors (e.g., protocadherin and ephrin) (for review, see Eroglu, 2009; Risher and Eroglu, 2012). Despite these important findings, the role of neuronal activity in astrocyte-mediated circuit assembly remains to be determined.

Microglia and astrocytes in pruning synapses for circuit precision

As Hubel and Weisel demonstrated 50 years ago, circuits, once established, require refinement for precise connectivity. Elimination of extraneous synapses (synaptic pruning) is critical for proper circuit function. Synaptic pruning is regulated by neuronal activity and experience (for review, see Katz and Shatz, 1996; Hua and Smith, 2004). Microglia, brain resident immune cells, are major players in this activity-dependent synaptic pruning (for review, see Michell-Robinson et al., 2015; Schafer and Stevens, 2015; Salter and Stevens, 2017; Li and Barres, 2018). Microglia, which comprise 5%–15% of CNS cells, colonize the brain during early CNS development (Ginhoux et al., 2010). Microglia dynamically interact with synapses and prune immature/inappropriate synapses (Fig. 2) (for review, see Wake et al., 2013; Schafer and Stevens, 2015).

The role of microglia as a major player in synapse pruning was first identified in 2007, when Beth Stevens and Ben Barres revealed the microglial complement immune pathway as the molecular mediator of synapse elimination (for review, see Schafer and Stevens, 2010; Stephan et al., 2012). This area of research was primarily conducted in the visual system because of the beautifully organized eye-segregation process, which occurs during an active period for synaptic pruning. In the developing LGN, synaptic input (RGC axons) from both eyes initially forms overlapping synaptic fields, which are later pruned to eye-specific regions (Rakic, 1976; Hubel et al., 1977; LeVay et al., 1978; Chen and Regehr, 2000; Hooks and Chen, 2006; for review, see Huberman, 2007). Components of the classical complement immune pathway, such as C1q and its downstream effector C3, are expressed at synapses in developing, but not mature, LGN (Stevens et al., 2007; Schafer et al., 2012). During the developmental period in which active synaptic pruning occurs, microglia are the only cell type that expresses complement receptor 3 (CR3, CD11b) (Akiyama and McGeer, 1990), which mediates microglial engulfment of RGC axon terminals in the LGN (Schafer et al., 2012). Mice lacking C1q, C3, or CR3 exhibit similar phenotypes in which RGC axon terminals fail to form eye-specific regions in LGN, indicating defective synaptic pruning (Stevens et al., 2007; Schafer et al., 2012). Consistent with this, microglial engulfment of RGC presynaptic terminals is decreased and synaptic connectivity is compromised in CR3/C3 knockout (KO) mice (Schafer et al., 2012).

Microglia-mediated synaptic pruning is regulated by activity. In the visual system, reducing neuronal activity through light deprivation increases the number of microglia positioned at dendritic spines that eventually diminish in size. This implies a role for microglia in eliminating synapses that are less active (Tremblay et al., 2010). Consistent with the regulatory role of neuronal activity in microglia-mediated synaptic pruning, reintroducing dark-reared mice to light is sufficient to reverse the effect (Tremblay et al., 2010). Schafer et al. (2012, 2014) later established an in vivo engulfment assay and directly demonstrated the relationship between neuronal activity and microglial engulfment of synapses. During eye segregation in the LGN, silent (TTX-treated) RGC terminals are more likely to be engulfed by microglia, relative to normal (vehicle-treated) RGC terminals. In contrast, activated (forskolin-treated) RGC terminals are less likely to be eliminated by microglia (Schafer et al., 2012). Together, mounting evidence indicates that microglia are indispensable for proper synaptic pruning/refinement.

Like microglia, astrocytes participate in synaptic pruning by phagocytosis of unwanted synapses, in this case via the MERTK/MEGF10 pathway (Chung et al., 2013). Studies in the visual system demonstrate that astrocytes also regulate synaptic pruning indirectly by secreting transforming growth factor (TGF)-β, which stimulates neuronal expression of C1q and consequently triggers microglial phagocytosis (Rakic, 1976; Stevens et al., 2007; Schafer et al., 2012; Bialas and Stevens, 2013). Thus, synaptic pruning is mediated by an interplay among astrocytes, neurons, and microglia. Future studies are needed to determine whether and how neuronal activity contributes to astrocyte-mediated synaptic pruning.

Oligodendrocytes in developmental myelination

Neuronal activity also has profound effects on oligodendrocyte lineage cells, which form myelin and thus strongly influence the timing of action potential conduction and neural circuit dynamics, as well as providing metabolic support to axons (Saab et al., 2013). Myelinating oligodendrocytes are generated by oligodendrocyte precursor cells (OPCs), a unipotent stem cell population that self-renews to maintain a homeostatic precursor population density and generates new oligodendrocytes throughout life (Fig. 2) (Tripathi et al., 2017; Hill et al., 2018; Hughes et al., 2018).

Developmental myelination in the CNS begins perinatally and spans nearly three decades of human life (Yakovlev and Lecours, 1967; Lebel et al., 2012), allowing ample opportunity for experience to modulate developmental myelination. In the 1940s, formation of myelin with “ideal” geometric proportions was proposed to promote maximal action potential speed for a given axonal diameter (Huxley and Stampfli, 1949). At that time, it was unclear to what extent developmental myelination may be influenced by experience.

The idea that neurons may regulate the degree to which their axons are myelinated again emerged from early observations in the visual system. In the 1960s, Gyllensten and Malmfors (1963) discovered that dark rearing, which decreases retinal activity, delays myelination of RGC axons in the optic nerve; and conversely, premature eye opening results in accelerated myelination in the optic nerve (Tauber et al., 1980). It is now clear that, during development, axonal activity influences selection of axons for ensheathment in a manner dependent on vesicular release (Hines et al., 2015; Mensch et al., 2015). However, the idea that neuronal activity can influence myelination was brought into question by the observations that myelination can also proceed in an neuronal activity-independent manner, evidenced by myelination of fixed axons or inert nanofibers of appropriate diameter in vitro (Bullock and Rome, 1990; Lee et al., 2012) and of silenced optic nerve axons in vivo (Mayoral et al., 2018). These findings led to a two-phase model of myelination: intrinsic myelination occurs independent of activity, and adaptive myelination that is regulated by neuronal activity/experience (Bechler et al., 2015) This is discussed in more detail below.

Activity-dependent plasticity of form and function

Neuronal activity in synaptic plasticity and circuit function

In the adult brain, the number, shape, and strength of synapses change over time in response to neuronal activity (for review, see Katz and Shatz, 1996; Citri and Malenka, 2008; Ho et al., 2011). In general, this activity-dependent synaptic plasticity is hypothesized to be a central cellular correlate of learning and memory. The rules and mechanisms governing these changes are diverse and depend upon the type of synapse, type of presynaptic and postsynaptic cell, relative timing of spikes or depolarization in these cells, brain region, developmental stage, and recent activity history, among many other factors. Synaptic function can be modulated by vesicle release probability and quantal composition on the presynaptic side, and by trafficking of neurotransmitter receptors to and from the postsynaptic membrane (Malenka and Bear, 2004). For example, neuronal activity during experience, such as motor skill learning, sensory experience, and fear conditioning, can alter synaptic receptor composition and synapse numbers in behavior-relevant circuits (Trachtenberg et al., 2002; Holtmaat et al., 2006; De Roo et al., 2008; Xu et al., 2009; Yang et al., 2009; Lai et al., 2012). In addition, activity can change the morphology of postsynaptic dendritic spines, which can be associated with functional changes to the synapses (Van Harreveld and Fifkova, 1975; Engert and Bonhoeffer, 1999; Maletic-Savatic et al., 1999; Grutzendler et al., 2002; Trachtenberg et al., 2002). For example, repetitive activation of hippocampal CA1 pyramidal neurons may lead to sustained enlargement of originally small dendritic spines, and this spine enlargement can be associated with increased AMPA receptor (AMPAR)-mediated currents (Matsuzaki et al., 2004).

Two important forms of activity-dependent synaptic modification are long-term potentiation (LTP) the persistent enhancement of synaptic strength, and long-term depression (LTD), the persistent reduction of synaptic strength (for review, see Malenka and Bear, 2004). In 1949, Donald Hebb proposed a theory for synaptic plasticity (Hebb's rule), according to which the repeated successful activation of one neuron (B) by another (A) will increase the efficacy (i.e., the strength) of the synapse connecting A to B (Hebb, 1949). Hebb's rule was confirmed by the discovery of LTP in the late 1960s (Lømo, 1966; Bliss and Lømo, 1970; Bliss and Gardner-Medwin, 1973), around the time of the first SfN meeting, although not all plastic synapses follow this rule. In the early 1990s, a debate over whether LTP is presynaptic or postsynaptic spurred intense research into the underlying mechanisms of LTP. Although some synapse types express presynaptic LTP and others express postsynaptic LTP, one question in the debate was whether LTP at the hippocampal CA3/CA1 synapse is due to increased presynaptic neurotransmitter release probability or to increased/altered postsynaptic receptors. Addressing this controversy inspired development and application of new tools, such as 2-photon glutamate uncaging (Matsuzaki et al., 2004) and optical quantal analysis allowing for single-synapse resolution (Emptage et al., 2003; Enoki et al., 2009). These efforts resulted in profound new knowledge about synaptic biology, such as regulation of postsynaptic receptor trafficking by neuronal activity (for review, see Malenka and Nicoll, 1999; Malinow and Malenka, 2002; Bredt and Nicoll, 2003).

Many forms of LTP and LTD exist depending on the type of synapse, developmental stages, and postsynaptic receptors involved. Here, we summarize key steps in hippocampal CA3/CA1 LTP and LTD (for review in various forms and mechanisms of LTP and LDP, see Malinow and Malenka, 2002; Malenka and Bear, 2004). Hippocampal LTP consists of two main phases: early (E) and late (L) LTP. Generally speaking, E-LTP can be induced by high-frequency stimulation of a synapse, which triggers calcium influx through neuronal NMDA receptors (NMDARs) or L-type voltage-gated calcium channels (VGCCs) (Lynch et al., 1983; Malenka et al., 1988, 1992; Grover and Teyler, 1990). This rise in calcium levels within dendritic spines leads to persistent activation of Ca2+/calmodulin-dependent protein kinase II (CaMKII) and protein kinase C (PKC) which phosphorylate AMPARs to increase channel activity and/or postsynaptic trafficking (Barria et al., 1997; Benke et al., 1998; Deisseroth et al., 1998; Strack and Colbran, 1998; Lee et al., 2003). Unlike E-LTP, which is independent of protein synthesis, L-LTP involves transcriptional (Frey et al., 1996) and translational (Frey et al., 1988) changes (for review, see Abraham and Williams, 2003; Pittenger and Kandel, 2003; Lynch, 2004). Activation of the transcription factor cAMP response element-binding protein (CREB) is critical for the transcriptional changes (Dash et al., 1990; Bourtchuladze et al., 1994; Yin et al., 1994; Deisseroth et al., 1998). The MAPK/ERK and mTOR pathways are important in translational control during L-LTP (Casadio et al., 1999; Tang et al., 2002; Kelleher et al., 2004; Kovács et al., 2007).

In 1992, Bear and Malenka demonstrated that low-frequency stimulation induces LTD in hippocampal slices (Dudek and Bear, 1992; Mulkey and Malenka, 1992). As for LTP, this form of LTD involves NMDAR activation and increases in postsynaptic calcium concentration; however, the downstream pathways elicited are distinct. The lower-intensity stimulation that induces LTD leads to moderate calcium influx and downstream activation of the calcineurin/inhibitor-1/protein phosphatases cascade (Mulkey and Malenka, 1992; Mulkey et al., 1993, 1994), dephosphorylation of AMPARs (Lee et al., 1998, 2000, 2003) and endocytosis of AMPARs from the postsynaptic density (Lüthi et al., 1999; Beattie et al., 2000; Ehlers, 2000; Lin et al., 2000; Man et al., 2000; Lee et al., 2002; for review, see Carroll et al., 2001; Bredt and Nicoll, 2003).

A wealth of work over the past two decades has advanced our understanding of activity-dependent synaptic plasticity, LTP, LTD, and the roles of these processes in learning, memory, and neurological diseases. We suggest interested readers see excellent reviews on this important topic (Turrigiano, 1999; Lamprecht and LeDoux, 2004; Malenka and Bear, 2004; Sutton and Schuman, 2006; Blundon and Zakharenko, 2008; Bourne and Harris, 2008; Alberini, 2009; Makino and Malinow, 2009; Bagetta et al., 2010; Collingridge et al., 2010; Kasai et al., 2010; Caroni et al., 2012; Pozueta et al., 2013).

Astrocytes in modulating circuit function

Astrocytes modulate synaptic function, influencing both presynaptic and postsynaptic mechanisms (for review, see Allen and Eroglu, 2017). In 1998, Kang et al., demonstrated that the activity of hippocampal interneurons increases the [Ca2+]i in surrounding astrocytes, which in turn potentiates inhibitory transmission (Kang et al., 1998). The next year, Ventura and Harris (1999) described the fine structure of synapses and revealed their “tripartite” nature, specifically, that they are composed of not only a presynaptic axon and postsynaptic dendrite, but also a perisynaptic astrocyte process (PAP) (for review, see Araque et al., 1999). PAPs assist fast clearance of extracellular neurotransmitters and stabilize synaptic connections. PAPs are highly motile; and in response to neuronal activity, individual PAPs exhibit localized morphological changes (for review, see Theodosis et al., 2008), and altered neurotransmitter transporter expression (Genoud et al., 2006; Haber et al., 2006; Bernardinelli et al., 2014). For example, activation of synaptic terminals in situ enhances the motility of PAPs within synaptic regions (Hirrlinger et al., 2004). Consistent with this, neuronal activation that induces LTP leads to increased PAP motility (Bernardinelli et al., 2014). Similar increased PAP motility, as well as increased glutamate transporter expression and increased astrocytic coverage on synapses, was observed in the somatosensory cortex following whisker stimulation of adult mice (Genoud et al., 2006; Bernardinelli et al., 2014). These neuronal activity-dependent PAP changes often happen at a slow timescale (hours to days) and are mediated partly by astrocytic metabotropic glutamate receptors and intracellular calcium signaling (Porter and McCarthy, 1996; Pasti et al., 1997; Hirase et al., 2004; Wang et al., 2006; Bernardinelli et al., 2014). However, the downstream events mediating changes in PAP motility and protein expression, and how these changes affect activity-dependent circuit function require future investigation.

Myelin plasticity in circuit function

Neural circuit function requires not only precise connectivity but also regulation of signal timing and metabolic support for axons. Myelination can robustly influence neural circuit dynamics (for review, see Mount and Monje, 2017). The geometric properties of myelinated internodes, including sheath thickness and internode length, contribute to conduction velocity, together with the diameter of the axon itself. The “ideal” ratio of sheath thickness relative to axon diameter (g-ratio) may maximize conduction velocity, although it is important to note that, in terms of complex circuit function, faster is not necessarily better. Rather, subtle changes in spike arrival time can influence synchronicity of signals and spike timing-dependent synaptic plasticity (for review, see Bi and Poo, 2001). Relatively small variations in myelin profiles can exert large changes in conduction velocity, which may substantially influence circuit dynamics and thereby alter neural function (Pajevic et al., 2014; Steadman et al., 2019).

While some CNS structures, such as the optic nerve and spinal cord, exhibit complete myelination with close to the “ideal” g-ratio, the neocortex and subcortical projection fibers involved in associative cognitive function exhibit myelination patterns and profiles that are far from “ideal.” Cortical axons exhibit variable myelin profiles along the length of a given axon, with some axonal regions lacking internodes (Tomassy et al., 2014) and a significant proportion of corpus callosum axons are unmyelinated (Sturrock, 1980). The opportunity for “tuning” myelination over the lifespan exists, particularly in regions with available unmyelinated axonal territory, such as the neocortex and intercortical projections. Concordantly, oligodendrocytes (Tripathi et al., 2017; Hill et al., 2018; Hughes et al., 2018) and myelin (Yakovlev and Lecours, 1967) accumulate over the lifespan.

In the 1990s, Barres and Raff extended the idea that axonal activity may influence myelin beyond the developmental period and demonstrated that neuronal activity may influence OPC behavior in the adult optic nerve (Barres and Raff, 1993). Both transecting the optic nerve and intravitreal injection of TTX inhibited OPC proliferation, whereas TTX did not alter OPC proliferation in the absence of neurons (Barres and Raff, 1993). Consistent with this, later studies demonstrated that enhancing neuronal firing with α-scorpion toxin promotes optic nerve myelination (Demerens et al., 1996). It was discovered in 2000 that OPCs form “axon–glial” synapses with neurons (Bergles et al., 2000; Karadottir et al., 2005; Kougioumtzidou et al., 2017), and the influence of neuronal activity on oligodendrogenesis and myelination was shown in vitro (Stevens et al., 2002; Ishibashi et al., 2006; Wake et al., 2011, 2015).

Recently, advances in neuroscience techniques enabled in vivo studies of adaptive myelination with spatiotemporal resolution. Several recent studies demonstrated the direct role of neuronal activity in promoting myelination and modulating behavior in vivo. Optogenetic stimulation of cortical projection neurons in mouse premotor cortex results in circuit-specific increases in OPC proliferation, oligodendrogenesis, and changes in cortical projection axon myelination, both during the juvenile period and in adulthood (Gibson et al., 2014). This neuronal-activity-regulated myelination in the premotor circuit requires neuronal-activity-regulated brain-derived neurotrophic factor (BDNF) signaling to the Tropomyosin receptor kinase B (TrkB) on OPCs (Geraghty et al., 2019) and is associated with improved motor function that depends on new oligodendrocyte generation (Gibson et al., 2014). Similarly, chemogenetic stimulation of somatosensory cortical neurons results in circuit-specific increases in OPC proliferation, oligodendrogenesis, and myelination of the stimulated axons (Mitew et al., 2018). Using in vivo 2-photon imaging, Hughes et al. (2018) conducted a longitudinal study that tracked oligodendrocytes in the mouse somatosensory superficial cortex. Sensory enrichment (whisker stimulation) triggered a robust increase in new oligodendrocyte generation and new myelin sheath formation in somatosensory (barrel) cortex.

Further supporting an adaptive role for activity-dependent changes in myelin-forming cells, Richardson and colleagues demonstrated that new oligodendrocyte generation is also required for learning new motor skills in adulthood (McKenzie et al., 2014). Mice trained to run on a complex wheel exhibited increased oligodendrogenesis in the premotor circuit, and motor skill learning in this task was blocked by preventing new oligodendrogenesis through conditional, inducible KO of myelin regulatory factor (Myrf), which is required for oligodendrocyte maturation, in OPCs during adulthood (McKenzie et al., 2014). If the conditional KO was introduced after the skill was learned, oligodendrogenesis was no longer required for performing this task, indicating a role for oligodendrocytes in the learning process. Consistent with this principle that neuronal activity can influence ongoing plasticity of myelin, experience-dependent changes in myelin structure have been demonstrated in humans using diffusion tensor imaging. Individuals who trained in specific tasks, such as juggling (Scholz et al., 2009) and piano practicing (Bengtsson et al., 2005), exhibited myelin structure changes evident on diffusion tensor imaging in circuits relevant to hand-eye coordination and to motor function.

Myelin plasticity contributes to nonmotor cognitive function as well. Ongoing activity-regulated myelination is required for normal cognitive behavioral function in a test of attention and short-term memory in mice (Geraghty et al., 2019). Water-maze learning induces OPC proliferation, oligodendrogenesis, and de novo myelination in hippocampal-frontal circuitry, and oligodendrogenesis is required for spatial learning (Steadman et al., 2019). Importantly, spatial learning-induced oligodendrogenesis continues through the consolidation phase and is required for memory consolidation (Steadman et al., 2019). Concordantly, disruption of myelin plasticity contributes to cognitive impairment observed in a mouse model of chemotherapy-related cognitive impairment (Geraghty et al., 2019). The influence of experience on myelin structure and thus circuit dynamics may be bidirectional, with experiential deprivation in the form of social isolation leading to reduced myelin sheath thickness in the prefrontal cortex of both juvenile and adult mice; these myelin structural changes are associated with impairments in social function upon reintroduction to social interactions (Liu et al., 2012; Makinodan et al., 2012). Promoting oligodendrogenesis in socially isolated mice normalizes myelin and rescues social avoidance behavior (Liu et al., 2016). Collectively, adaptive myelination is emerging as a versatile process by which experience influences circuit dynamics and behavior.

In conclusion, our understanding of neuronal activity-regulated circuit establishment and plasticity has advanced tremendously in the past 50 years. Starting from an intense period of neuron-centric investigations, the field is marching into a new area of studying glial contributions to activity-dependent events. The entire neuroscience field has advanced exponentially with the development of neuromodulatory tools (e.g., optogenetics and chemogenetics), circuit mapping tools (e.g., transsynaptic viral mapping), and imaging techniques (e.g., 2-photon imaging, tissue clearing, and large-volume imaging). With the enormous leap in our knowledge about the CNS, much remains unknown. Mapping of neuron–neuron and neuron–glia (e.g., OPCs) communication will promote understanding of how the brain functions as a cellular society in health and diseases. The role of astrocytes in activity-dependent synaptic pruning and the role of microglia in synaptic plasticity remain to be fully explored. In addition, how glial cells affect activity-dependent neurodevelopment and plasticity in disease states is largely unknown. Adding another layer of complexity is the heterogeneity of each glial cell type. For example, different subtypes or states of astrocytes or microglia may perform diverse functions (Zhang and Barres, 2010; Liddelow and Barres, 2017; Hammond et al., 2019; Masuda et al., 2019; Spitzer et al., 2019). Recent advances in spatially resolved single-cell sequencing will aid in determining how glial heterogeneity contributes to neurodevelopment and circuit function. In addition, there is a pressing need for tools that allow simultaneous profiling of neural cell transcriptome and function. Aided by the tools of modern neuroscience, the cellular and molecular mechanisms underlying activity-dependent neurodevelopment and circuit function are coming to light. Yet much remains to be elucidated in the next 50 years.

Footnotes

  • This work was supported by National Institute of Neurological Disorders and Stroke R01NS092597, National Institutes of Health Director's Pioneer Award DP1NS111132, Department of Defense, Brantley's Project (supported by Ian's Friends Foundation), Maternal and Child Health Research Institute at Stanford, and Bio-X Institute at Stanford.

  • The authors declare no competing financial interests.

  • Correspondence should be addressed to Michelle Monje at mmonje{at}stanford.edu

References

  1. ↵
    1. Abraham WC,
    2. Williams JM
    (2003) Properties and mechanisms of LTP maintenance. Neuroscientist 9:463–474. doi:10.1177/1073858403259119 pmid:14678579
    OpenUrlCrossRefPubMed
  2. ↵
    1. Akiyama H,
    2. McGeer PL
    (1990) Brain microglia constitutively express beta-2 integrins. J Neuroimmunol 30:81–93. doi:10.1016/0165-5728(90)90055-R pmid:1977769
    OpenUrlCrossRefPubMed
  3. ↵
    1. Alberini CM
    (2009) Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 89:121–145. doi:10.1152/physrev.00017.2008 pmid:19126756
    OpenUrlCrossRefPubMed
  4. ↵
    1. Allen NJ,
    2. Eroglu C
    (2017) Cell biology of astrocyte-synapse interactions. Neuron 96:697–708. doi:10.1016/j.neuron.2017.09.056 pmid:29096081
    OpenUrlCrossRefPubMed
  5. ↵
    1. Anderson CM,
    2. Torres F,
    3. Faoro A
    (1985) The EEG of the early premature. Electroencephalogr Clin Neurophysiol 60:95–105. doi:10.1016/0013-4694(85)90015-X pmid:2578372
    OpenUrlCrossRefPubMed
  6. ↵
    1. Anton-Bolanos N,
    2. Sempere-Ferràndez A,
    3. Guillamón-Vivancos T,
    4. Martini FJ,
    5. Pérez-Saiz L,
    6. Gezelius H,
    7. Filipchuk A,
    8. Valdeolmillos M,
    9. López-Bendito G
    (2019) Prenatal activity from thalamic neurons governs the emergence of functional cortical maps in mice. Science 364:987–990. doi:10.1126/science.aav7617 pmid:31048552
    OpenUrlAbstract/FREE Full Text
  7. ↵
    1. Araque A,
    2. Parpura V,
    3. Sanzgiri RP,
    4. Haydon PG
    (1999) Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 22:208–215. doi:10.1016/S0166-2236(98)01349-6 pmid:10322493
    OpenUrlCrossRefPubMed
  8. ↵
    1. Bagetta V,
    2. Ghiglieri V,
    3. Sgobio C,
    4. Calabresi P,
    5. Picconi B
    (2010) Synaptic dysfunction in Parkinson's disease. Biochem Soc Trans 38:493–497. doi:10.1042/BST0380493 pmid:20298209
    OpenUrlAbstract/FREE Full Text
  9. ↵
    1. Barres BA
    (1991) New roles for glia. J Neurosci 11:3685–3694. doi:10.1523/JNEUROSCI.11-12-03685.1991 pmid:1720814
    OpenUrlFREE Full Text
  10. ↵
    1. Barres BA,
    2. Raff MC
    (1993) Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361:258–260. doi:10.1038/361258a0 pmid:8093806
    OpenUrlCrossRefPubMed
  11. ↵
    1. Barria A,
    2. Muller D,
    3. Derkach V,
    4. Griffith LC,
    5. Soderling TR
    (1997) Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science 276:2042–2045. doi:10.1126/science.276.5321.2042 pmid:9197267
    OpenUrlAbstract/FREE Full Text
  12. ↵
    1. Beattie EC,
    2. Carroll RC,
    3. Yu X,
    4. Morishita W,
    5. Yasuda H,
    6. von Zastrow M,
    7. Malenka RC
    (2000) Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat Neurosci 3:1291–1300. doi:10.1038/81823 pmid:11100150
    OpenUrlCrossRefPubMed
  13. ↵
    1. Bechler ME,
    2. Byrne L,
    3. Ffrench-Constant C
    (2015) CNS myelin sheath lengths are an intrinsic property of oligodendrocytes. Curr Biol 25:2411–2416. doi:10.1016/j.cub.2015.07.056 pmid:26320951
    OpenUrlCrossRefPubMed
  14. ↵
    1. Ben-Ari Y,
    2. Cherubini E,
    3. Corradetti R,
    4. Gaiarsa JL
    (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 416:303–325. doi:10.1113/jphysiol.1989.sp017762 pmid:2575165
    OpenUrlCrossRefPubMed
  15. ↵
    1. Bengtsson SL,
    2. Nagy Z,
    3. Skare S,
    4. Forsman L,
    5. Forssberg H,
    6. Ullén F
    (2005) Extensive piano practicing has regionally specific effects on white matter development. Nat Neurosci 8:1148–1150. doi:10.1038/nn1516 pmid:16116456
    OpenUrlCrossRefPubMed
  16. ↵
    1. Benke TA,
    2. Lüthi A,
    3. Isaac JT,
    4. Collingridge GL
    (1998) Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 393:793–797. doi:10.1038/31709 pmid:9655394
    OpenUrlCrossRefPubMed
  17. ↵
    1. Bergles DE,
    2. Roberts JD,
    3. Somogyi P,
    4. Jahr CE
    (2000) Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405:187–191. doi:10.1038/35012083 pmid:10821275
    OpenUrlCrossRefPubMed
  18. ↵
    1. Bernardinelli Y,
    2. Randall J,
    3. Janett E,
    4. Nikonenko I,
    5. König S,
    6. Jones EV,
    7. Flores CE,
    8. Murai KK,
    9. Bochet CG,
    10. Holtmaat A,
    11. Muller D
    (2014) Activity-dependent structural plasticity of perisynaptic astrocytic domains promotes excitatory synapse stability. Curr Biol 24:1679–1688. doi:10.1016/j.cub.2014.06.025 pmid:25042585
    OpenUrlCrossRefPubMed
  19. ↵
    1. Bi G,
    2. Poo M
    (2001) Synaptic modification by correlated activity: Hebb's postulate revisited. Annu Rev Neurosci 24:139–166. doi:10.1146/annurev.neuro.24.1.139 pmid:11283308
    OpenUrlCrossRefPubMed
  20. ↵
    1. Bialas AR,
    2. Stevens B
    (2013) TGF-beta signaling regulates neuronal C1q expression and developmental synaptic refinement. Nat Neurosci 16:1773–1782. doi:10.1038/nn.3560 pmid:24162655
    OpenUrlCrossRefPubMed
  21. ↵
    1. Bliss TV,
    2. Gardner-Medwin AR
    (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the unanaestetized rabbit following stimulation of the perforant path. J Physiol 232:357–374. doi:10.1113/jphysiol.1973.sp010274 pmid:4727085
    OpenUrlCrossRefPubMed
  22. ↵
    1. Bliss TV,
    2. Lømo T
    (1970) Plasticity in a monosynaptic cortical pathway. J Physiol 207:61P. pmid:5511138
    OpenUrlPubMed
  23. ↵
    1. Blundon JA,
    2. Zakharenko SS
    (2008) Dissecting the components of long-term potentiation. Neuroscientist 14:598–608. doi:10.1177/1073858408320643 pmid:18940785
    OpenUrlCrossRefPubMed
  24. ↵
    1. Bourne JN,
    2. Harris KM
    (2008) Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 31:47–67. doi:10.1146/annurev.neuro.31.060407.125646 pmid:18284372
    OpenUrlCrossRefPubMed
  25. ↵
    1. Bourtchuladze R,
    2. Frenguelli B,
    3. Blendy J,
    4. Cioffi D,
    5. Schutz G,
    6. Silva AJ
    (1994) Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79:59–68. doi:10.1016/0092-8674(94)90400-6 pmid:7923378
    OpenUrlCrossRefPubMed
  26. ↵
    1. Bredt DS,
    2. Nicoll RA
    (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40:361–379. doi:10.1016/S0896-6273(03)00640-8 pmid:14556714
    OpenUrlCrossRefPubMed
  27. ↵
    1. Bullock PN,
    2. Rome LH
    (1990) Glass micro-fibers: a model system for study of early events in myelination. J Neurosci Res 27:383–393. doi:10.1002/jnr.490270317 pmid:2097381
    OpenUrlCrossRefPubMed
  28. ↵
    1. Campbell G,
    2. Shatz CJ
    (1992) Synapses formed by identified retinogeniculate axons during the segregation of eye input. J Neurosci 12:1847–1858. doi:10.1523/JNEUROSCI.12-05-01847.1992 pmid:1578274
    OpenUrlAbstract/FREE Full Text
  29. ↵
    1. Caroni P,
    2. Donato F,
    3. Muller D
    (2012) Structural plasticity upon learning: regulation and functions. Nat Rev Neurosci 13:478–490. doi:10.1038/nrn3258 pmid:22714019
    OpenUrlCrossRefPubMed
  30. ↵
    1. Carroll RC,
    2. Beattie EC,
    3. von Zastrow M,
    4. Malenka RC
    (2001) Role of AMPA receptor endocytosis in synaptic plasticity. Nat Rev Neurosci 2:315–324. doi:10.1038/35072500 pmid:11331915
    OpenUrlCrossRefPubMed
  31. ↵
    1. Casadio A,
    2. Martin KC,
    3. Giustetto M,
    4. Zhu H,
    5. Chen M,
    6. Bartsch D,
    7. Bailey CH,
    8. Kandel ER
    (1999) A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 99:221–237. doi:10.1016/S0092-8674(00)81653-0 pmid:10535740
    OpenUrlCrossRefPubMed
  32. ↵
    1. Chen C,
    2. Regehr WG
    (2000) Developmental remodeling of the retinogeniculate synapse. Neuron 28:955–966. doi:10.1016/S0896-6273(00)00166-5 pmid:11163279
    OpenUrlCrossRefPubMed
  33. ↵
    1. Christopherson KS,
    2. Ullian EM,
    3. Stokes CC,
    4. Mullowney CE,
    5. Hell JW,
    6. Agah A,
    7. Lawler J,
    8. Mosher DF,
    9. Bornstein P,
    10. Barres BA
    (2005) Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120:421–433. doi:10.1016/j.cell.2004.12.020 pmid:15707899
    OpenUrlCrossRefPubMed
  34. ↵
    1. Chung WS,
    2. Clarke LE,
    3. Wang GX,
    4. Stafford BK,
    5. Sher A,
    6. Chakraborty C,
    7. Joung J,
    8. Foo LC,
    9. Thompson A,
    10. Chen C,
    11. Smith SJ,
    12. Barres BA
    (2013) Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways. Nature 504:394–400. doi:10.1038/nature12776 pmid:24270812
    OpenUrlCrossRefPubMed
  35. ↵
    1. Chung WS,
    2. Allen NJ,
    3. Eroglu C
    (2015) Astrocytes control synapse formation, function, and elimination. Cold Spring Harb Perspect Biol 7:a020370. doi:10.1101/cshperspect.a020370 pmid:25663667
    OpenUrlAbstract/FREE Full Text
  36. ↵
    1. Citri A,
    2. Malenka RC
    (2008) Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 33:18–41. doi:10.1038/sj.npp.1301559 pmid:17728696
    OpenUrlCrossRefPubMed
  37. ↵
    1. Collingridge GL,
    2. Peineau S,
    3. Howland JG,
    4. Wang YT
    (2010) Long-term depression in the CNS. Nat Rev Neurosci 11:459–473. doi:10.1038/nrn2867 pmid:20559335
    OpenUrlCrossRefPubMed
  38. ↵
    1. Colón-Ramos DA,
    2. Margeta MA,
    3. Shen K
    (2007) Glia promote local synaptogenesis through UNC-6 (netrin) signaling in C. elegans. Science 318:103–106. doi:10.1126/science.1143762 pmid:17916735
    OpenUrlAbstract/FREE Full Text
  39. ↵
    1. Cornell-Bell AH,
    2. Finkbeiner SM
    (1991) Ca2+ waves in astrocytes. Cell Calcium 12:185–204. doi:10.1016/0143-4160(91)90020-F pmid:1647876
    OpenUrlCrossRefPubMed
  40. ↵
    1. Cornell-Bell AH,
    2. Finkbeiner SM,
    3. Cooper MS,
    4. Smith SJ
    (1990) Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247:470–473. doi:10.1126/science.1967852 pmid:1967852
    OpenUrlAbstract/FREE Full Text
  41. ↵
    1. Dani JW,
    2. Chernjavsky A,
    3. Smith SJ
    (1992) Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron 8:429–440. doi:10.1016/0896-6273(92)90271-E pmid:1347996
    OpenUrlCrossRefPubMed
  42. ↵
    1. Dash PK,
    2. Hochner B,
    3. Kandel ER
    (1990) Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature 345:718–721. doi:10.1038/345718a0 pmid:2141668
    OpenUrlCrossRefPubMed
  43. ↵
    1. Daw NW,
    2. Fox K,
    3. Sato H,
    4. Czepita D
    (1992) Critical period for monocular deprivation in the cat visual cortex. J Neurophysiol 67:197–202. doi:10.1152/jn.1992.67.1.197 pmid:1552319
    OpenUrlCrossRefPubMed
  44. ↵
    1. Deisseroth K,
    2. Heist EK,
    3. Tsien RW
    (1998) Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons. Nature 392:198–202. doi:10.1038/32448 pmid:9515967
    OpenUrlCrossRefPubMed
  45. ↵
    1. Deisseroth K,
    2. Singla S,
    3. Toda H,
    4. Monje M,
    5. Palmer TD,
    6. Malenka RC
    (2004) Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42:535–552. doi:10.1016/S0896-6273(04)00266-1 pmid:15157417
    OpenUrlCrossRefPubMed
  46. ↵
    1. Demerens C,
    2. Stankoff B,
    3. Logak M,
    4. Anglade P,
    5. Allinquant B,
    6. Couraud F,
    7. Zalc B,
    8. Lubetzki C
    (1996) Induction of myelination in the central nervous system by electrical activity. Proc Natl Acad Sci U S A 93:9887–9892. doi:10.1073/pnas.93.18.9887 pmid:8790426
    OpenUrlAbstract/FREE Full Text
  47. ↵
    1. De Roo M,
    2. Klauser P,
    3. Muller D
    (2008) LTP promotes a selective long-term stabilization and clustering of dendritic spines. PLoS Biol 6:e219. doi:10.1371/journal.pbio.0060219 pmid:18788894
    OpenUrlCrossRefPubMed
  48. ↵
    1. Dudek SM,
    2. Bear MF
    (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-d-aspartate receptor blockade. Proc Natl Acad Sci U S A 89:4363–4367. doi:10.1073/pnas.89.10.4363 pmid:1350090
    OpenUrlAbstract/FREE Full Text
  49. ↵
    1. Ehlers MD
    (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28:511–525. doi:10.1016/S0896-6273(00)00129-X pmid:11144360
    OpenUrlCrossRefPubMed
  50. ↵
    1. Elmariah SB,
    2. Oh EJ,
    3. Hughes EG,
    4. Balice-Gordon RJ
    (2005) Astrocytes regulate inhibitory synapse formation via Trk-mediated modulation of postsynaptic GABAA receptors. J Neurosci 25:3638–3650. doi:10.1523/JNEUROSCI.3980-04.2005 pmid:15814795
    OpenUrlAbstract/FREE Full Text
  51. ↵
    1. Emptage NJ,
    2. Reid CA,
    3. Fine A,
    4. Bliss TV
    (2003) Optical quantal analysis reveals a presynaptic component of LTP at hippocampal Schaffer-associational synapses. Neuron 38:797–804. doi:10.1016/S0896-6273(03)00325-8 pmid:12797963
    OpenUrlCrossRefPubMed
  52. ↵
    1. Engert F,
    2. Bonhoeffer T
    (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399:66–70. doi:10.1038/19978 pmid:10331391
    OpenUrlCrossRefPubMed
  53. ↵
    1. Enoki R,
    2. Hu YL,
    3. Hamilton D,
    4. Fine A
    (2009) Expression of long-term plasticity at individual synapses in hippocampus is graded, bidirectional, and mainly presynaptic: optical quantal analysis. Neuron 62:242–253. doi:10.1016/j.neuron.2009.02.026 pmid:19409269
    OpenUrlCrossRefPubMed
  54. ↵
    1. Eroglu C
    (2009) The role of astrocyte-secreted matricellular proteins in central nervous system development and function. J Cell Commun Signal 3:167–176. doi:10.1007/s12079-009-0078-y pmid:19904629
    OpenUrlCrossRefPubMed
  55. ↵
    1. Feller MB,
    2. Wellis DP,
    3. Stellwagen D,
    4. Werblin FS,
    5. Shatz CJ
    (1996) Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science 272:1182–1187. doi:10.1126/science.272.5265.1182 pmid:8638165
    OpenUrlAbstract
  56. ↵
    1. Frey U,
    2. Krug M,
    3. Reymann KG,
    4. Matthies H
    (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452:57–65. doi:10.1016/0006-8993(88)90008-X pmid:3401749
    OpenUrlCrossRefPubMed
  57. ↵
    1. Frey U,
    2. Frey S,
    3. Schollmeier F,
    4. Krug M
    (1996) Influence of actinomycin D, a RNA synthesis inhibitor, on long-term potentiation in rat hippocampal neurons in vivo and in vitro. J Physiol 490:703–711. doi:10.1113/jphysiol.1996.sp021179 pmid:8683469
    OpenUrlCrossRefPubMed
  58. ↵
    1. Galli L,
    2. Maffei L
    (1988) Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. Science 242:90–91. doi:10.1126/science.3175637 pmid:3175637
    OpenUrlAbstract/FREE Full Text
  59. ↵
    1. Gallo V,
    2. Bertolotto A
    (1990) Extracellular matrix of cultured glial cells: selective expression of chondroitin 4-sulfate by type-2 astrocytes and their progenitors. Exp Cell Res 187:211–223. doi:10.1016/0014-4827(90)90084-N pmid:2108048
    OpenUrlCrossRefPubMed
  60. ↵
    1. Garaschuk O,
    2. Hanse E,
    3. Konnerth A
    (1998) Developmental profile and synaptic origin of early network oscillations in the CA1 region of rat neonatal hippocampus. J Physiol 507:219–236. doi:10.1111/j.1469-7793.1998.219bu.x pmid:9490842
    OpenUrlCrossRefPubMed
  61. ↵
    1. Genoud C,
    2. Quairiaux C,
    3. Steiner P,
    4. Hirling H,
    5. Welker E,
    6. Knott GW
    (2006) Plasticity of astrocytic coverage and glutamate transporter expression in adult mouse cortex. PLoS Biol 4:e343. doi:10.1371/journal.pbio.0040343 pmid:17048987
    OpenUrlCrossRefPubMed
  62. ↵
    1. Geraghty AC,
    2. Gibson EM,
    3. Ghanem RA,
    4. Greene JJ,
    5. Ocampo A,
    6. Goldstein AK,
    7. Ni L,
    8. Yang T,
    9. Marton RM,
    10. Pasca SP,
    11. Greenberg ME,
    12. Longo FM,
    13. Monje M
    (2019) Loss of adaptive myelination contributes to methotrexate chemotherapy-related cognitive impairment. Neuron 103:250–265.e8. doi:10.1016/j.neuron.2019.04.032 pmid:31122677
    OpenUrlCrossRefPubMed
  63. ↵
    1. Gibson EM,
    2. Purger D,
    3. Mount CW,
    4. Goldstein AK,
    5. Lin GL,
    6. Wood LS,
    7. Inema I,
    8. Miller SE,
    9. Bieri G,
    10. Zuchero JB,
    11. Barres BA,
    12. Woo PJ,
    13. Vogel H,
    14. Monje M
    (2014) Neuronal activity promotes oligodendrogenesis and adaptive myelination in the mammalian brain. Science 344:1252304. doi:10.1126/science.1252304 pmid:24727982
    OpenUrlAbstract/FREE Full Text
  64. ↵
    1. Ginhoux F,
    2. Greter M,
    3. Leboeuf M,
    4. Nandi S,
    5. See P,
    6. Gokhan S,
    7. Mehler MF,
    8. Conway SJ,
    9. Ng LG,
    10. Stanley ER,
    11. Samokhvalov IM,
    12. Merad M
    (2010) Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330:841–845. doi:10.1126/science.1194637 pmid:20966214
    OpenUrlAbstract/FREE Full Text
  65. ↵
    1. Grover LM,
    2. Teyler TJ
    (1990) Two components of long-term potentiation induced by different patterns of afferent activation. Nature 347:477–479. doi:10.1038/347477a0 pmid:1977084
    OpenUrlCrossRefPubMed
  66. ↵
    1. Grutzendler J,
    2. Kasthuri N,
    3. Gan WB
    (2002) Long-term dendritic spine stability in the adult cortex. Nature 420:812–816. doi:10.1038/nature01276 pmid:12490949
    OpenUrlCrossRefPubMed
  67. ↵
    1. Gyllensten L,
    2. Malmfors T
    (1963) Myelinization of the optic nerve and its dependence on visual function: a quantitative investigation in mice. J Embryol Exp Morphol 11:255–266. pmid:13963537
    OpenUrlAbstract/FREE Full Text
  68. ↵
    1. Haber M,
    2. Zhou L,
    3. Murai KK
    (2006) Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses. J Neurosci 26:8881–8891. doi:10.1523/JNEUROSCI.1302-06.2006 pmid:16943543
    OpenUrlAbstract/FREE Full Text
  69. ↵
    1. Hammond TR,
    2. Dufort C,
    3. Dissing-Olesen L,
    4. Giera S,
    5. Young A,
    6. Wysoker A,
    7. Walker AJ,
    8. Gergits F,
    9. Segel M,
    10. Nemesh J,
    11. Marsh SE,
    12. Saunders A,
    13. Macosko E,
    14. Ginhoux F,
    15. Chen J,
    16. Franklin RJM,
    17. Piao X,
    18. McCarroll SA,
    19. Stevens B
    (2019). Single-Cell RNA Sequencing of Microglia throughout the Mouse Lifespan and in the Injured Brain Reveals Complex Cell-State Changes. Immunity 50:253–271.e256.
    OpenUrlCrossRefPubMed
  70. ↵
    1. Hasel P,
    2. Dando O,
    3. Jiwaji Z,
    4. Baxter P,
    5. Todd AC,
    6. Heron S,
    7. Márkus NM,
    8. McQueen J,
    9. Hampton DW,
    10. Torvell M,
    11. Tiwari SS,
    12. McKay S,
    13. Eraso-Pichot A,
    14. Zorzano A,
    15. Masgrau R,
    16. Galea E,
    17. Chandran S,
    18. Wyllie DJ,
    19. Simpson TI,
    20. Hardingham GE
    (2017) Neurons and neuronal activity control gene expression in astrocytes to regulate their development and metabolism. Nat Commun 8:15132. doi:10.1038/ncomms15132 pmid:28462931
    OpenUrlCrossRefPubMed
  71. ↵
    1. Hebb DO
    (1949) The organization of behavior. New York: Wiley.
  72. ↵
    1. Herrmann K,
    2. Shatz CJ
    (1995) Blockade of action potential activity alters initial arborization of thalamic axons within cortical layer 4. Proc Natl Acad Sci U S A 92:11244–11248. doi:10.1073/pnas.92.24.11244 pmid:7479973
    OpenUrlAbstract/FREE Full Text
  73. ↵
    1. Hill RA,
    2. Li AM,
    3. Grutzendler J
    (2018) Lifelong cortical myelin plasticity and age-related degeneration in the live mammalian brain. Nat Neurosci 21:683–695. doi:10.1038/s41593-018-0120-6 pmid:29556031
    OpenUrlCrossRefPubMed
  74. ↵
    1. Hines JH,
    2. Ravanelli AM,
    3. Schwindt R,
    4. Scott EK,
    5. Appel B
    (2015) Neuronal activity biases axon selection for myelination in vivo. Nat Neurosci 18:683–689. doi:10.1038/nn.3992 pmid:25849987
    OpenUrlCrossRefPubMed
  75. ↵
    1. Hirase H,
    2. Qian L,
    3. Barthó P,
    4. Buzsáki G
    (2004) Calcium dynamics of cortical astrocytic networks in vivo. PLoS Biol 2:E96. doi:10.1371/journal.pbio.0020096 pmid:15094801
    OpenUrlCrossRefPubMed
  76. ↵
    1. Hirrlinger J,
    2. Hülsmann S,
    3. Kirchhoff F
    (2004) Astroglial processes show spontaneous motility at active synaptic terminals in situ. Eur J Neurosci 20:2235–2239. doi:10.1111/j.1460-9568.2004.03689.x pmid:15450103
    OpenUrlCrossRefPubMed
  77. ↵
    1. Ho VM,
    2. Lee JA,
    3. Martin KC
    (2011) The cell biology of synaptic plasticity. Science 334:623–628. doi:10.1126/science.1209236 pmid:22053042
    OpenUrlAbstract/FREE Full Text
  78. ↵
    1. Holtmaat A,
    2. Wilbrecht L,
    3. Knott GW,
    4. Welker E,
    5. Svoboda K
    (2006) Experience-dependent and cell-type-specific spine growth in the neocortex. Nature 441:979–983. doi:10.1038/nature04783 pmid:16791195
    OpenUrlCrossRefPubMed
  79. ↵
    1. Hooks BM,
    2. Chen C
    (2006) Distinct roles for spontaneous and visual activity in remodeling of the retinogeniculate synapse. Neuron 52:281–291. doi:10.1016/j.neuron.2006.07.007 pmid:17046691
    OpenUrlCrossRefPubMed
  80. ↵
    1. Horton JC,
    2. Hocking DR
    (1996a) Anatomical demonstration of ocular dominance columns in striate cortex of the squirrel monkey. J Neurosci 16:5510–5522. doi:10.1523/JNEUROSCI.16-17-05510.1996 pmid:8757263
    OpenUrlAbstract/FREE Full Text
  81. ↵
    1. Horton JC,
    2. Hocking DR
    (1996b) An adult-like pattern of ocular dominance columns in striate cortex of newborn monkeys prior to visual experience. J Neurosci 16:1791–1807. doi:10.1523/JNEUROSCI.16-05-01791.1996 pmid:8774447
    OpenUrlAbstract/FREE Full Text
  82. ↵
    1. Hua JY,
    2. Smith SJ
    (2004) Neural activity and the dynamics of central nervous system development. Nat Neurosci 7:327–332. doi:10.1038/nn1218 pmid:15048120
    OpenUrlCrossRefPubMed
  83. ↵
    1. Hubel DH,
    2. Wiesel TN
    (1959) Receptive fields of single neurones in the cat's striate cortex. J Physiol 148:574–591. doi:10.1113/jphysiol.1959.sp006308 pmid:14403679
    OpenUrlCrossRefPubMed
  84. ↵
    1. Hubel DH,
    2. Wiesel TN
    (1962) Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol 160:106–154. doi:10.1113/jphysiol.1962.sp006837 pmid:14449617
    OpenUrlCrossRefPubMed
  85. ↵
    1. Hubel DH,
    2. Wiesel TN
    (1963) Receptive fields of cells in striate cortex of very young, visually inexperienced kittens. J Neurophysiol 26:994–1002. doi:10.1152/jn.1963.26.6.994 pmid:14084171
    OpenUrlCrossRefPubMed
  86. ↵
    1. Hubel DH,
    2. Wiesel TN
    (1965) Binocular interaction in striate cortex of kittens reared with artificial squint. J Neurophysiol 28:1041–1059. doi:10.1152/jn.1965.28.6.1041 pmid:5883731
    OpenUrlCrossRefPubMed
  87. ↵
    1. Hubel DH,
    2. Wiesel TN
    (1969) Anatomical demonstration of columns in the monkey striate cortex. Nature 221:747–750. doi:10.1038/221747a0 pmid:4974881
    OpenUrlCrossRefPubMed
  88. ↵
    1. Hubel DH,
    2. Wiesel TN
    (1970) The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol 206:419–436. doi:10.1113/jphysiol.1970.sp009022 pmid:5498493
    OpenUrlCrossRefPubMed
  89. ↵
    1. Hubel DH,
    2. Wiesel TN,
    3. LeVay S
    (1977) Plasticity of ocular dominance columns in monkey striate cortex. Philos Trans R Soc Lond B Biol Sci 278:377–409. doi:10.1098/rstb.1977.0050 pmid:19791
    OpenUrlCrossRefPubMed
  90. ↵
    1. Huberman AD
    (2007) Mechanisms of eye-specific visual circuit development. Curr Opin Neurobiol 17:73–80. doi:10.1016/j.conb.2007.01.005 pmid:17254766
    OpenUrlCrossRefPubMed
  91. ↵
    1. Huberman AD,
    2. Speer CM,
    3. Chapman B
    (2006) Spontaneous retinal activity mediates development of ocular dominance columns and binocular receptive fields in V1. Neuron 52:247–254. doi:10.1016/j.neuron.2006.07.028 pmid:17046688
    OpenUrlCrossRefPubMed
  92. ↵
    1. Hughes EG,
    2. Elmariah SB,
    3. Balice-Gordon RJ
    (2010) Astrocyte secreted proteins selectively increase hippocampal GABAergic axon length, branching, and synaptogenesis. Mol Cell Neurosci 43:136–145. doi:10.1016/j.mcn.2009.10.004 pmid:19850128
    OpenUrlCrossRefPubMed
  93. ↵
    1. Hughes EG,
    2. Orthmann-Murphy JL,
    3. Langseth AJ,
    4. Bergles DE
    (2018) Myelin remodeling through experience-dependent oligodendrogenesis in the adult somatosensory cortex. Nat Neurosci 21:696–706. doi:10.1038/s41593-018-0121-5 pmid:29556025
    OpenUrlCrossRefPubMed
  94. ↵
    1. Huxley AF,
    2. Stampfli R
    (1949) Evidence for saltatory conduction in peripheral myelinated nerve fibres. J Physiol 108:315–339. doi:10.1113/jphysiol.1949.sp004335 pmid:16991863
    OpenUrlCrossRefPubMed
  95. ↵
    1. Ishibashi T,
    2. Dakin KA,
    3. Stevens B,
    4. Lee PR,
    5. Kozlov SV,
    6. Stewart CL,
    7. Fields RD
    (2006) Astrocytes promote myelination in response to electrical impulses. Neuron 49:823–832. doi:10.1016/j.neuron.2006.02.006 pmid:16543131
    OpenUrlCrossRefPubMed
  96. ↵
    1. Kang J,
    2. Jiang L,
    3. Goldman SA,
    4. Nedergaard M
    (1998) Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci 1:683–692. doi:10.1038/3684 pmid:10196584
    OpenUrlCrossRefPubMed
  97. ↵
    1. Karadottir R,
    2. Cavelier P,
    3. Bergersen L,
    4. Attwell D
    (2005) NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438:1162–1166.
    OpenUrlCrossRefPubMed
  98. ↵
    1. Kasai H,
    2. Hayama T,
    3. Ishikawa M,
    4. Watanabe S,
    5. Yagishita S,
    6. Noguchi J
    (2010) Learning rules and persistence of dendritic spines. Eur J Neurosci 32:241–249. doi:10.1111/j.1460-9568.2010.07344.x pmid:20646057
    OpenUrlCrossRefPubMed
  99. ↵
    1. Katz LC,
    2. Shatz CJ
    (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133–1138. doi:10.1126/science.274.5290.1133 pmid:8895456
    OpenUrlAbstract/FREE Full Text
  100. ↵
    1. Kelleher RJ 3rd.,
    2. Govindarajan A,
    3. Jung HY,
    4. Kang H,
    5. Tonegawa S
    (2004) Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116:467–479. doi:10.1016/S0092-8674(04)00115-1 pmid:15016380
    OpenUrlCrossRefPubMed
  101. ↵
    1. Khazipov R,
    2. Esclapez M,
    3. Caillard O,
    4. Bernard C,
    5. Khalilov I,
    6. Tyzio R,
    7. Hirsch J,
    8. Dzhala V,
    9. Berger B,
    10. Ben-Ari Y
    (2001) Early development of neuronal activity in the primate hippocampus in utero. J Neurosci 21:9770–9781. doi:10.1523/JNEUROSCI.21-24-09770.2001 pmid:11739585
    OpenUrlAbstract/FREE Full Text
  102. ↵
    1. Khazipov R,
    2. Sirota A,
    3. Leinekugel X,
    4. Holmes GL,
    5. Ben-Ari Y,
    6. Buzsáki G
    (2004) Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 432:758–761. doi:10.1038/nature03132 pmid:15592414
    OpenUrlCrossRefPubMed
  103. ↵
    1. Kitzes LM,
    2. Kageyama GH,
    3. Semple MN,
    4. Kil J
    (1995) Development of ectopic projections from the ventral cochlear nucleus to the superior olivary complex induced by neonatal ablation of the contralateral cochlea. J Comp Neurol 353:341–363. doi:10.1002/cne.903530303 pmid:7751435
    OpenUrlCrossRefPubMed
  104. ↵
    1. Kougioumtzidou E,
    2. Shimizu T,
    3. Hamilton NB,
    4. Tohyama K,
    5. Sprengel R,
    6. Monyer H,
    7. Attwell D,
    8. Richardson WD
    (2017) Signalling through AMPA receptors on oligodendrocyte precursors promotes myelination by enhancing oligodendrocyte survival. Elife 6:e28080. doi:10.7554/eLife.28080 pmid:28608780
    OpenUrlCrossRefPubMed
  105. ↵
    1. Kovács KA,
    2. Steullet P,
    3. Steinmann M,
    4. Do KQ,
    5. Magistretti PJ,
    6. Halfon O,
    7. Cardinaux JR
    (2007) TORC1 is a calcium- and cAMP-sensitive coincidence detector involved in hippocampal long-term synaptic plasticity. Proc Natl Acad Sci U S A 104:4700–4705. doi:10.1073/pnas.0607524104 pmid:17360587
    OpenUrlAbstract/FREE Full Text
  106. ↵
    1. Kriegler S,
    2. Chiu SY
    (1993) Calcium signaling of glial cells along mammalian axons. J Neurosci 13:4229–4245. doi:10.1523/JNEUROSCI.13-10-04229.1993 pmid:7692011
    OpenUrlAbstract/FREE Full Text
  107. ↵
    1. Lai CS,
    2. Franke TF,
    3. Gan WB
    (2012) Opposite effects of fear conditioning and extinction on dendritic spine remodelling. Nature 483:87–91. doi:10.1038/nature10792 pmid:22343895
    OpenUrlCrossRefPubMed
  108. ↵
    1. Lamblin MD,
    2. André M,
    3. Challamel MJ,
    4. Curzi-Dascalova L,
    5. d'Allest AM,
    6. De Giovanni E,
    7. Moussalli-Salefranque F,
    8. Navelet Y,
    9. Plouin P,
    10. Radvanyi-Bouvet MF,
    11. Samson-Dollfus D,
    12. Vecchierini-Blineau MF
    (1999) Electroencephalography of the premature and term newborn: maturational aspects and glossary. Neurophysiol Clin 29:123–219. doi:10.1016/S0987-7053(99)80051-3 pmid:10367287
    OpenUrlCrossRefPubMed
  109. ↵
    1. Lamprecht R,
    2. LeDoux J
    (2004) Structural plasticity and memory. Nat Rev Neurosci 5:45–54. doi:10.1038/nrn1301 pmid:14708003
    OpenUrlCrossRefPubMed
  110. ↵
    1. Lebel C,
    2. Gee M,
    3. Camicioli R,
    4. Wieler M,
    5. Martin W,
    6. Beaulieu C
    (2012) Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage 60:340–352. doi:10.1016/j.neuroimage.2011.11.094 pmid:22178809
    OpenUrlCrossRefPubMed
  111. ↵
    1. Leclerc C,
    2. Rizzo C,
    3. Daguzan C,
    4. Néant I,
    5. Batut J,
    6. Augé B,
    7. Moreau M
    (2001) Neural determination in Xenopus laevis embryos: control of early neural gene expression by calcium. J Soc Biol 195:327–337. doi:10.1051/jbio/2001195030327 pmid:11833471
    OpenUrlCrossRefPubMed
  112. ↵
    1. Lee HK,
    2. Kameyama K,
    3. Huganir RL,
    4. Bear MF
    (1998) NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus. Neuron 21:1151–1162. doi:10.1016/S0896-6273(00)80632-7 pmid:9856470
    OpenUrlCrossRefPubMed
  113. ↵
    1. Lee HK,
    2. Barbarosie M,
    3. Kameyama K,
    4. Bear MF,
    5. Huganir RL
    (2000) Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature 405:955–959. doi:10.1038/35016089 pmid:10879537
    OpenUrlCrossRefPubMed
  114. ↵
    1. Lee HK,
    2. Takamiya K,
    3. Han JS,
    4. Man H,
    5. Kim CH,
    6. Rumbaugh G,
    7. Yu S,
    8. Ding L,
    9. He C,
    10. Petralia RS,
    11. Wenthold RJ,
    12. Gallagher M,
    13. Huganir RL
    (2003) Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112:631–643. doi:10.1016/S0092-8674(03)00122-3 pmid:12628184
    OpenUrlCrossRefPubMed
  115. ↵
    1. Lee SH,
    2. Liu L,
    3. Wang YT,
    4. Sheng M
    (2002) Clathrin adaptor AP2 and NSF interact with overlapping sites of GluR2 and play distinct roles in AMPA receptor trafficking and hippocampal LTD. Neuron 36:661–674. doi:10.1016/S0896-6273(02)01024-3 pmid:12441055
    OpenUrlCrossRefPubMed
  116. ↵
    1. Lee S,
    2. Leach MK,
    3. Redmond SA,
    4. Chong SY,
    5. Mellon SH,
    6. Tuck SJ,
    7. Feng ZQ,
    8. Corey JM,
    9. Chan JR
    (2012) A culture system to study oligodendrocyte myelination processes using engineered nanofibers. Nat Methods 9:917–922. doi:10.1038/nmeth.2105 pmid:22796663
    OpenUrlCrossRefPubMed
  117. ↵
    1. Leinekugel X,
    2. Khazipov R,
    3. Cannon R,
    4. Hirase H,
    5. Ben-Ari Y,
    6. Buzsáki G
    (2002) Correlated bursts of activity in the neonatal hippocampus in vivo. Science 296:2049–2052. doi:10.1126/science.1071111 pmid:12065842
    OpenUrlAbstract/FREE Full Text
  118. ↵
    1. LeVay S,
    2. Stryker MP,
    3. Shatz CJ
    (1978) Ocular dominance columns and their development in layer IV of the cat's visual cortex: a quantitative study. J Comp Neurol 179:223–244. doi:10.1002/cne.901790113 pmid:8980725
    OpenUrlCrossRefPubMed
  119. ↵
    1. LeVay S,
    2. Wiesel TN,
    3. Hubel DH
    (1980) The development of ocular dominance columns in normal and visually deprived monkeys. J Comp Neurol 191:1–51. doi:10.1002/cne.901910102 pmid:6772696
    OpenUrlCrossRefPubMed
  120. ↵
    1. Li Q,
    2. Barres BA
    (2018) Microglia and macrophages in brain homeostasis and disease. Nat Rev Immunol 18:225–242. doi:10.1038/nri.2017.125 pmid:29151590
    OpenUrlCrossRefPubMed
  121. ↵
    1. Liddelow SA,
    2. Barres BA
    (2017) Reactive astrocytes: production, function, and therapeutic potential. Immunity 46:957–967. doi:10.1016/j.immuni.2017.06.006 pmid:28636962
    OpenUrlCrossRefPubMed
  122. ↵
    1. Lin JW,
    2. Ju W,
    3. Foster K,
    4. Lee SH,
    5. Ahmadian G,
    6. Wyszynski M,
    7. Wang YT,
    8. Sheng M
    (2000) Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization. Nat Neurosci 3:1282–1290. doi:10.1038/81814 pmid:11100149
    OpenUrlCrossRefPubMed
  123. ↵
    1. Liu J,
    2. Dietz K,
    3. DeLoyht JM,
    4. Pedre X,
    5. Kelkar D,
    6. Kaur J,
    7. Vialou V,
    8. Lobo MK,
    9. Dietz DM,
    10. Nestler EJ,
    11. Dupree J,
    12. Casaccia P
    (2012) Impaired adult myelination in the prefrontal cortex of socially isolated mice. Nat Neurosci 15:1621–1623. doi:10.1038/nn.3263 pmid:23143512
    OpenUrlCrossRefPubMed
  124. ↵
    1. Liu J,
    2. Dupree JL,
    3. Gacias M,
    4. Frawley R,
    5. Sikder T,
    6. Naik P,
    7. Casaccia P
    (2016) Clemastine enhances myelination in the prefrontal cortex and rescues behavioral changes in socially isolated mice. J Neurosci 36:957–962. doi:10.1523/JNEUROSCI.3608-15.2016 pmid:26791223
    OpenUrlAbstract/FREE Full Text
  125. ↵
    1. Lømo T
    (1966) Frequency potentiation of excitatory synaptic activity in the dentate area of the hippocampal formation. Acta Physiol Scand 68(Suppl. 277):128.
    OpenUrl
  126. ↵
    1. LoTurco JJ,
    2. Owens DF,
    3. Heath MJ,
    4. Davis MB,
    5. Kriegstein AR
    (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15:1287–1298. doi:10.1016/0896-6273(95)90008-X pmid:8845153
    OpenUrlCrossRefPubMed
  127. ↵
    1. Luk KC,
    2. Sadikot AF
    (2004) Glutamate and regulation of proliferation in the developing mammalian telencephalon. Dev Neurosci 26:218–228. doi:10.1159/000082139 pmid:15711062
    OpenUrlCrossRefPubMed
  128. ↵
    1. Luk KC,
    2. Kennedy TE,
    3. Sadikot AF
    (2003) Glutamate promotes proliferation of striatal neuronal progenitors by an NMDA receptor-mediated mechanism. J Neurosci 23:2239–2250. doi:10.1523/JNEUROSCI.23-06-02239.2003 pmid:12657683
    OpenUrlAbstract/FREE Full Text
  129. ↵
    1. Lüthi A,
    2. Chittajallu R,
    3. Duprat F,
    4. Palmer MJ,
    5. Benke TA,
    6. Kidd FL,
    7. Henley JM,
    8. Isaac JT,
    9. Collingridge GL
    (1999) Hippocampal LTD expression involves a pool of AMPARs regulated by the NSF-GluR2 interaction. Neuron 24:389–399. doi:10.1016/S0896-6273(00)80852-1 pmid:10571232
    OpenUrlCrossRefPubMed
  130. ↵
    1. Lynch G,
    2. Larson J,
    3. Kelso S,
    4. Barrionuevo G,
    5. Schottler F
    (1983) Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature 305:719–721. doi:10.1038/305719a0 pmid:6415483
    OpenUrlCrossRefPubMed
  131. ↵
    1. Lynch MA
    (2004) Long-term potentiation and memory. Physiol Rev 84:87–136. doi:10.1152/physrev.00014.2003 pmid:14715912
    OpenUrlCrossRefPubMed
  132. ↵
    1. Maffei L,
    2. Galli-Resta L
    (1990) Correlation in the discharges of neighboring rat retinal ganglion cells during prenatal life. Proc Natl Acad Sci U S A 87:2861–2864. doi:10.1073/pnas.87.7.2861 pmid:2320593
    OpenUrlAbstract/FREE Full Text
  133. ↵
    1. Makino H,
    2. Malinow R
    (2009) AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron 64:381–390. doi:10.1016/j.neuron.2009.08.035 pmid:19914186
    OpenUrlCrossRefPubMed
  134. ↵
    1. Makinodan M,
    2. Rosen KM,
    3. Ito S,
    4. Corfas G
    (2012) A critical period for social experience-dependent oligodendrocyte maturation and myelination. Science 337:1357–1360. doi:10.1126/science.1220845 pmid:22984073
    OpenUrlAbstract/FREE Full Text
  135. ↵
    1. Malenka RC,
    2. Bear MF
    (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5–21. doi:10.1016/j.neuron.2004.09.012 pmid:15450156
    OpenUrlCrossRefPubMed
  136. ↵
    1. Malenka RC,
    2. Nicoll RA
    (1999) Long-term potentiation: a decade of progress? Science 285:1870–1874. doi:10.1126/science.285.5435.1870 pmid:10489359
    OpenUrlAbstract/FREE Full Text
  137. ↵
    1. Malenka RC,
    2. Kauer JA,
    3. Zucker RS,
    4. Nicoll RA
    (1988) Postsynaptic calcium is sufficient for potentiation of hippocampal synaptic transmission. Science 242:81–84. doi:10.1126/science.2845577 pmid:2845577
    OpenUrlAbstract/FREE Full Text
  138. ↵
    1. Malenka RC,
    2. Lancaster B,
    3. Zucker RS
    (1992) Temporal limits on the rise in postsynaptic calcium required for the induction of long-term potentiation. Neuron 9:121–128. doi:10.1016/0896-6273(92)90227-5 pmid:1632966
    OpenUrlCrossRefPubMed
  139. ↵
    1. Maletic-Savatic M,
    2. Malinow R,
    3. Svoboda K
    (1999) Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283:1923–1927. doi:10.1126/science.283.5409.1923 pmid:10082466
    OpenUrlAbstract/FREE Full Text
  140. ↵
    1. Malinow R,
    2. Malenka RC
    (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103–126. doi:10.1146/annurev.neuro.25.112701.142758 pmid:12052905
    OpenUrlCrossRefPubMed
  141. ↵
    1. Man HY,
    2. Lin JW,
    3. Ju WH,
    4. Ahmadian G,
    5. Liu L,
    6. Becker LE,
    7. Sheng M,
    8. Wang YT
    (2000) Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron 25:649–662. doi:10.1016/S0896-6273(00)81067-3 pmid:10774732
    OpenUrlCrossRefPubMed
  142. ↵
    1. Masuda T,
    2. Sankowski R,
    3. Staszewski O,
    4. Böttcher C,
    5. Amann L,
    6. Sagar,
    7. Scheiwe C,
    8. Nessler S,
    9. Kunz P,
    10. van Loo G,
    11. Coenen VA,
    12. Reinacher PC,
    13. Michel A,
    14. Sure U,
    15. Gold R,
    16. Grün D,
    17. Priller J,
    18. Stadelmann C,
    19. Prinz M
    (2019) Spatial and temporal heterogeneity of mouse and human microglia at single-cell resolution. Nature 566:388–392. doi:10.1038/s41586-019-0924-x pmid:30760929
    OpenUrlCrossRefPubMed
  143. ↵
    1. Matsuzaki M,
    2. Honkura N,
    3. Ellis-Davies GC,
    4. Kasai H
    (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761–766. doi:10.1038/nature02617 pmid:15190253
    OpenUrlCrossRefPubMed
  144. ↵
    1. Mauch DH,
    2. Nägler K,
    3. Schumacher S,
    4. Göritz C,
    5. Müller EC,
    6. Otto A,
    7. Pfrieger FW
    (2001) CNS synaptogenesis promoted by glia-derived cholesterol. Science 294:1354–1357. doi:10.1126/science.294.5545.1354 pmid:11701931
    OpenUrlAbstract/FREE Full Text
  145. ↵
    1. Mayoral SR,
    2. Etxeberria A,
    3. Shen YA,
    4. Chan JR
    (2018) Initiation of CNS myelination in the optic nerve is dependent on axon caliber. Cell Rep 25:544–550.e43. doi:10.1016/j.celrep.2018.09.052 pmid:30332636
    OpenUrlCrossRefPubMed
  146. ↵
    1. McKenzie IA,
    2. Ohayon D,
    3. Li H,
    4. de Faria JP,
    5. Emery B,
    6. Tohyama K,
    7. Richardson WD
    (2014) Motor skill learning requires active central myelination. Science 346:318–322. doi:10.1126/science.1254960 pmid:25324381
    OpenUrlAbstract/FREE Full Text
  147. ↵
    1. Meister M,
    2. Wong RO,
    3. Baylor DA,
    4. Shatz CJ
    (1991) Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252:939–943. doi:10.1126/science.2035024 pmid:2035024
    OpenUrlAbstract/FREE Full Text
  148. ↵
    1. Mensch S,
    2. Baraban M,
    3. Almeida R,
    4. Czopka T,
    5. Ausborn J,
    6. El Manira A,
    7. Lyons DA
    (2015) Synaptic vesicle release regulates myelin sheath number of individual oligodendrocytes in vivo. Nat Neurosci 18:628–630. doi:10.1038/nn.3991 pmid:25849985
    OpenUrlCrossRefPubMed
  149. ↵
    1. Meyer-Franke A,
    2. Kaplan MR,
    3. Pfrieger FW,
    4. Barres BA
    (1995) Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron 15:805–819. doi:10.1016/0896-6273(95)90172-8 pmid:7576630
    OpenUrlCrossRefPubMed
  150. ↵
    1. Michell-Robinson MA,
    2. Touil H,
    3. Healy LM,
    4. Owen DR,
    5. Durafourt BA,
    6. Bar-Or A,
    7. Antel JP,
    8. Moore CS
    (2015) Roles of microglia in brain development, tissue maintenance and repair. Brain 138:1138–1159. doi:10.1093/brain/awv066 pmid:25823474
    OpenUrlCrossRefPubMed
  151. ↵
    1. Mitew S,
    2. Gobius I,
    3. Fenlon LR,
    4. McDougall SJ,
    5. Hawkes D,
    6. Xing YL,
    7. Bujalka H,
    8. Gundlach AL,
    9. Richards LJ,
    10. Kilpatrick TJ,
    11. Merson TD,
    12. Emery B
    (2018) Pharmacogenetic stimulation of neuronal activity increases myelination in an axon-specific manner. Nat Commun 9:306. doi:10.1038/s41467-017-02719-2 pmid:29358753
    OpenUrlCrossRefPubMed
  152. ↵
    1. Moore DR,
    2. Kitzes LM
    (1985) Projections from the cochlear nucleus to the inferior colliculus in normal and neonatally cochlea-ablated gerbils. J Comp Neurol 240:180–195. doi:10.1002/cne.902400208 pmid:4056109
    OpenUrlCrossRefPubMed
  153. ↵
    1. Moreno-Juan V,
    2. Filipchuk A,
    3. Antón-Bolaños N,
    4. Mezzera C,
    5. Gezelius H,
    6. Andrés B,
    7. Rodríguez-Malmierca L,
    8. Susín R,
    9. Schaad O,
    10. Iwasato T,
    11. Schüle R,
    12. Rutlin M,
    13. Nelson S,
    14. Ducret S,
    15. Valdeolmillos M,
    16. Rijli FM,
    17. López-Bendito G
    (2017) Prenatal thalamic waves regulate cortical area size prior to sensory processing. Nat Commun 8:14172. doi:10.1038/ncomms14172 pmid:28155854
    OpenUrlCrossRefPubMed
  154. ↵
    1. Mount CW,
    2. Monje M
    (2017) Wrapped to adapt: experience-dependent myelination. Neuron 95:743–756. doi:10.1016/j.neuron.2017.07.009 pmid:28817797
    OpenUrlCrossRefPubMed
  155. ↵
    1. Mulkey RM,
    2. Malenka RC
    (1992) Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9:967–975. doi:10.1016/0896-6273(92)90248-C pmid:1419003
    OpenUrlCrossRefPubMed
  156. ↵
    1. Mulkey RM,
    2. Herron CE,
    3. Malenka RC
    (1993) An essential role for protein phosphatases in hippocampal long-term depression. Science 261:1051–1055. doi:10.1126/science.8394601 pmid:8394601
    OpenUrlAbstract/FREE Full Text
  157. ↵
    1. Mulkey RM,
    2. Endo S,
    3. Shenolikar S,
    4. Malenka RC
    (1994) Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369:486–488. doi:10.1038/369486a0 pmid:7515479
    OpenUrlCrossRefPubMed
  158. ↵
    1. Muthukumar AK,
    2. Stork T,
    3. Freeman MR
    (2014) Activity-dependent regulation of astrocyte GAT levels during synaptogenesis. Nat Neurosci 17:1340–1350. doi:10.1038/nn.3791 pmid:25151265
    OpenUrlCrossRefPubMed
  159. ↵
    1. Nägler K,
    2. Mauch DH,
    3. Pfrieger FW
    (2001) Glia-derived signals induce synapse formation in neurones of the rat central nervous system. J Physiol 533:665–679. doi:10.1111/j.1469-7793.2001.00665.x pmid:11410625
    OpenUrlCrossRefPubMed
  160. ↵
    1. Paez-Gonzalez P,
    2. Asrican B,
    3. Rodriguez E,
    4. Kuo CT
    (2014) Identification of distinct ChAT(+) neurons and activity-dependent control of postnatal SVZ neurogenesis. Nat Neurosci 17:934–942. doi:10.1038/nn.3734 pmid:24880216
    OpenUrlCrossRefPubMed
  161. ↵
    1. Pajevic S,
    2. Basser PJ,
    3. Fields RD
    (2014) Role of myelin plasticity in oscillations and synchrony of neuronal activity. Neuroscience 276:135–147. doi:10.1016/j.neuroscience.2013.11.007 pmid:24291730
    OpenUrlCrossRefPubMed
  162. ↵
    1. Pasti L,
    2. Volterra A,
    3. Pozzan T,
    4. Carmignoto G
    (1997) Intracellular calcium oscillations in astrocytes: a highly plastic, bidirectional form of communication between neurons and astrocytes in situ. J Neurosci 17:7817–7830. doi:10.1523/JNEUROSCI.17-20-07817.1997 pmid:9315902
    OpenUrlAbstract/FREE Full Text
  163. ↵
    1. Pearce B,
    2. Morrow C,
    3. Murphy S
    (1988) Characteristics of phorbol ester- and agonist-induced down-regulation of astrocyte receptors coupled to inositol phospholipid metabolism. J Neurochem 50:936–944. doi:10.1111/j.1471-4159.1988.tb03002.x pmid:2828550
    OpenUrlCrossRefPubMed
  164. ↵
    1. Pearson RA,
    2. Catsicas M,
    3. Becker DL,
    4. Bayley P,
    5. Lüneborg NL,
    6. Mobbs P
    (2004) Ca(2+) signalling and gap junction coupling within and between pigment epithelium and neural retina in the developing chick. Eur J Neurosci 19:2435–2445. doi:10.1111/j.0953-816X.2004.03338.x pmid:15128397
    OpenUrlCrossRefPubMed
  165. ↵
    1. Pittenger C,
    2. Kandel ER
    (2003) In search of general mechanisms for long-lasting plasticity: Aplysia and the hippocampus. Philos Trans R Soc Lond B Biol Sci 358:757–763. doi:10.1098/rstb.2002.1247 pmid:12740123
    OpenUrlCrossRefPubMed
  166. ↵
    1. Porter JT,
    2. McCarthy KD
    (1996) Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J Neurosci 16:5073–5081. doi:10.1523/JNEUROSCI.16-16-05073.1996 pmid:8756437
    OpenUrlAbstract/FREE Full Text
  167. ↵
    1. Pozueta J,
    2. Lefort R,
    3. Shelanski ML
    (2013) Synaptic changes in Alzheimer's disease and its models. Neuroscience 251:51–65. doi:10.1016/j.neuroscience.2012.05.050 pmid:22687952
    OpenUrlCrossRefPubMed
  168. ↵
    1. Rakic P
    (1976) Prenatal genesis of connections subserving ocular dominance in the rhesus monkey. Nature 261:467–471. doi:10.1038/261467a0 pmid:819835
    OpenUrlCrossRefPubMed
  169. ↵
    1. Reiter HO,
    2. Waitzman DM,
    3. Stryker MP
    (1986) Cortical activity blockade prevents ocular dominance plasticity in the kitten visual cortex. Exp Brain Res 65:182–188. doi:10.1007/bf00243841 pmid:3803504
    OpenUrlCrossRefPubMed
  170. ↵
    1. Risher WC,
    2. Eroglu C
    (2012) Thrombospondins as key regulators of synaptogenesis in the central nervous system. Matrix Biol 31:170–177. doi:10.1016/j.matbio.2012.01.004 pmid:22285841
    OpenUrlCrossRefPubMed
  171. ↵
    1. Russell FA,
    2. Moore DR
    (1995) Afferent reorganisation within the superior olivary complex of the gerbil: development and induction by neonatal, unilateral cochlear removal. J Comp Neurol 352:607–625. doi:10.1002/cne.903520409 pmid:7722003
    OpenUrlCrossRefPubMed
  172. ↵
    1. Saab AS,
    2. Tzvetanova ID,
    3. Nave KA
    (2013) The role of myelin and oligodendrocytes in axonal energy metabolism. Curr Opin Neurobiol 23:1065–1072. doi:10.1016/j.conb.2013.09.008 pmid:24094633
    OpenUrlCrossRefPubMed
  173. ↵
    1. Salter MW,
    2. Stevens B
    (2017) Microglia emerge as central players in brain disease. Nat Med 23:1018–1027. doi:10.1038/nm.4397 pmid:28886007
    OpenUrlCrossRefPubMed
  174. ↵
    1. Schafer DP,
    2. Stevens B
    (2010) Synapse elimination during development and disease: immune molecules take centre stage. Biochem Soc Trans 38:476–481. doi:10.1042/BST0380476 pmid:20298206
    OpenUrlAbstract/FREE Full Text
  175. ↵
    1. Schafer DP,
    2. Stevens B
    (2015) Microglia function in central nervous system development and plasticity. Cold Spring Harb Perspect Biol 7:a020545. doi:10.1101/cshperspect.a020545 pmid:26187728
    OpenUrlAbstract/FREE Full Text
  176. ↵
    1. Schafer DP,
    2. Lehrman EK,
    3. Kautzman AG,
    4. Koyama R,
    5. Mardinly AR,
    6. Yamasaki R,
    7. Ransohoff RM,
    8. Greenberg ME,
    9. Barres BA,
    10. Stevens B
    (2012) Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74:691–705. doi:10.1016/j.neuron.2012.03.026 pmid:22632727
    OpenUrlCrossRefPubMed
  177. ↵
    1. Schafer DP,
    2. Lehrman EK,
    3. Heller CT,
    4. Stevens B
    (2014) An engulfment assay: a protocol to assess interactions between CNS phagocytes and neurons. J Vis Exp. Advance online publication. Retrieved June 8, 2014. doi: 10.3791/51482.
    OpenUrlCrossRef
  178. ↵
    1. Scholz J,
    2. Klein MC,
    3. Behrens TE,
    4. Johansen-Berg H
    (2009) Training induces changes in white-matter architecture. Nat Neurosci 12:1370–1371. doi:10.1038/nn.2412 pmid:19820707
    OpenUrlCrossRefPubMed
  179. ↵
    1. Shatz CJ
    (1990) Impulse activity and the patterning of connections during CNS development. Neuron 5:745–756. doi:10.1016/0896-6273(90)90333-B pmid:2148486
    OpenUrlCrossRefPubMed
  180. ↵
    1. Shatz CJ,
    2. Stryker MP
    (1988) Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science 242:87–89. doi:10.1126/science.3175636 pmid:3175636
    OpenUrlAbstract/FREE Full Text
  181. ↵
    1. Sherk H,
    2. Stryker MP
    (1976) Quantitative study of cortical orientation selectivity in visually inexperienced kitten. J Neurophysiol 39:63–70. doi:10.1152/jn.1976.39.1.63 pmid:1249604
    OpenUrlCrossRefPubMed
  182. ↵
    1. Song J,
    2. Sun J,
    3. Moss J,
    4. Wen Z,
    5. Sun GJ,
    6. Hsu D,
    7. Zhong C,
    8. Davoudi H,
    9. Christian KM,
    10. Toni N,
    11. Ming GL,
    12. Song H
    (2013) Parvalbumin interneurons mediate neuronal circuitry-neurogenesis coupling in the adult hippocampus. Nat Neurosci 16:1728–1730. doi:10.1038/nn.3572 pmid:24212671
    OpenUrlCrossRefPubMed
  183. ↵
    1. Spitzer SO,
    2. Sitnikov S,
    3. Kamen Y,
    4. Evans KA,
    5. Kronenberg-Versteeg D,
    6. Dietmann S,
    7. de Faria O Jr.,
    8. Agathou S,
    9. Káradóttir RT
    (2019) Oligodendrocyte progenitor cells become regionally diverse and heterogeneous with age. Neuron 101:459–471.e5. doi:10.1016/j.neuron.2018.12.020 pmid:30654924
    OpenUrlCrossRefPubMed
  184. ↵
    1. Sretavan D,
    2. Shatz CJ
    (1984) Prenatal development of individual retinogeniculate axons during the period of segregation. Nature 308:845–848. doi:10.1038/308845a0 pmid:6201743
    OpenUrlCrossRefPubMed
  185. ↵
    1. Sretavan DW,
    2. Shatz CJ
    (1986) Prenatal development of retinal ganglion cell axons: segregation into eye-specific layers within the cat's lateral geniculate nucleus. J Neurosci 6:234–251. doi:10.1523/JNEUROSCI.06-01-00234.1986 pmid:3944621
    OpenUrlAbstract/FREE Full Text
  186. ↵
    1. Sretavan DW,
    2. Shatz CJ,
    3. Stryker MP
    (1988) Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin. Nature 336:468–471. doi:10.1038/336468a0 pmid:2461517
    OpenUrlCrossRefPubMed
  187. ↵
    1. Steadman PE,
    2. Xia F,
    3. Ahmed M,
    4. Mocle AJ,
    5. Penning AR,
    6. Geraghty AC,
    7. Steenland HW,
    8. Monje M,
    9. Josselyn SA,
    10. Frankland PW
    (2019) Disruption of oligodendrogenesis impairs memory consolidation in adult mice. Neuron. Advance online publication. Retrieved Nov 4, 2019. doi: 10.1016/j.neuron.2019.10.013. doi:10.1016/j.neuron.2019.10.013 pmid:31753579
    OpenUrlCrossRefPubMed
  188. ↵
    1. Stephan AH,
    2. Barres BA,
    3. Stevens B
    (2012) The complement system: an unexpected role in synaptic pruning during development and disease. Annu Rev Neurosci 35:369–389. doi:10.1146/annurev-neuro-061010-113810 pmid:22715882
    OpenUrlCrossRefPubMed
  189. ↵
    1. Stevens B,
    2. Porta S,
    3. Haak LL,
    4. Gallo V,
    5. Fields RD
    (2002) Adenosine: a neuron–glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 36:855–868. doi:10.1016/S0896-6273(02)01067-X pmid:12467589
    OpenUrlCrossRefPubMed
  190. ↵
    1. Stevens B,
    2. Allen NJ,
    3. Vazquez LE,
    4. Howell GR,
    5. Christopherson KS,
    6. Nouri N,
    7. Micheva KD,
    8. Mehalow AK,
    9. Huberman AD,
    10. Stafford B,
    11. Sher A,
    12. Litke AM,
    13. Lambris JD,
    14. Smith SJ,
    15. John SW,
    16. Barres BA
    (2007) The classical complement cascade mediates CNS synapse elimination. Cell 131:1164–1178. doi:10.1016/j.cell.2007.10.036 pmid:18083105
    OpenUrlCrossRefPubMed
  191. ↵
    1. Strack S,
    2. Colbran RJ
    (1998) Autophosphorylation-dependent targeting of calcium/calmodulin-dependent protein kinase II by the NR2B subunit of the N-methyl-d-aspartate receptor. J Biol Chem 273:20689–20692. doi:10.1074/jbc.273.33.20689 pmid:9694809
    OpenUrlAbstract/FREE Full Text
  192. ↵
    1. Sturrock RR
    (1980) Myelination of the mouse corpus callosum. Neuropathol Appl Neurobiol 6:415–420. doi:10.1111/j.1365-2990.1980.tb00219.x pmid:7453945
    OpenUrlCrossRefPubMed
  193. ↵
    1. Sutton MA,
    2. Schuman EM
    (2006) Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127:49–58. doi:10.1016/j.cell.2006.09.014 pmid:17018276
    OpenUrlCrossRefPubMed
  194. ↵
    1. Tang SJ,
    2. Reis G,
    3. Kang H,
    4. Gingras AC,
    5. Sonenberg N,
    6. Schuman EM
    (2002) A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc Natl Acad Sci U S A 99:467–472. doi:10.1073/pnas.012605299 pmid:11756682
    OpenUrlAbstract/FREE Full Text
  195. ↵
    1. Tauber H,
    2. Waehneldt TV,
    3. Neuhoff V
    (1980) Myelination in rabbit optic nerves is accelerated by artificial eye opening. Neurosci Lett 16:235–238. doi:10.1016/0304-3940(80)90003-8 pmid:6302574
    OpenUrlCrossRefPubMed
  196. ↵
    1. Theodosis DT,
    2. Poulain DA,
    3. Oliet SH
    (2008) Activity-dependent structural and functional plasticity of astrocyte-neuron interactions. Physiol Rev 88:983–1008. doi:10.1152/physrev.00036.2007 pmid:18626065
    OpenUrlCrossRefPubMed
  197. ↵
    1. Tomassy GS,
    2. Berger DR,
    3. Chen HH,
    4. Kasthuri N,
    5. Hayworth KJ,
    6. Vercelli A,
    7. Seung HS,
    8. Lichtman JW,
    9. Arlotta P
    (2014) Distinct profiles of myelin distribution along single axons of pyramidal neurons in the neocortex. Science 344:319–324. doi:10.1126/science.1249766 pmid:24744380
    OpenUrlAbstract/FREE Full Text
  198. ↵
    1. Tozuka Y,
    2. Fukuda S,
    3. Namba T,
    4. Seki T,
    5. Hisatsune T
    (2005) GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47:803–815. doi:10.1016/j.neuron.2005.08.023 pmid:16157276
    OpenUrlCrossRefPubMed
  199. ↵
    1. Trachtenberg JT,
    2. Chen BE,
    3. Knott GW,
    4. Feng G,
    5. Sanes JR,
    6. Welker E,
    7. Svoboda K
    (2002) Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420:788–794. doi:10.1038/nature01273 pmid:12490942
    OpenUrlCrossRefPubMed
  200. ↵
    1. Tremblay MÈ,
    2. Lowery RL,
    3. Majewska AK
    (2010) Microglial interactions with synapses are modulated by visual experience. PLoS Biol 8:e1000527. doi:10.1371/journal.pbio.1000527 pmid:21072242
    OpenUrlCrossRefPubMed
  201. ↵
    1. Tripathi RB,
    2. Jackiewicz M,
    3. McKenzie IA,
    4. Kougioumtzidou E,
    5. Grist M,
    6. Richardson WD
    (2017) Remarkable stability of myelinating oligodendrocytes in mice. Cell Rep 21:316–323. doi:10.1016/j.celrep.2017.09.050 pmid:29020619
    OpenUrlCrossRefPubMed
  202. ↵
    1. Turrigiano GG
    (1999) Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci 22:221–227. doi:10.1016/S0166-2236(98)01341-1 pmid:10322495
    OpenUrlCrossRefPubMed
  203. ↵
    1. Ullian EM,
    2. Sapperstein SK,
    3. Christopherson KS,
    4. Barres BA
    (2001) Control of synapse number by glia. Science 291:657–661. doi:10.1126/science.291.5504.657 pmid:11158678
    OpenUrlAbstract/FREE Full Text
  204. ↵
    1. Ullian EM,
    2. Christopherson KS,
    3. Barres BA
    (2004) Role for glia in synaptogenesis. Glia 47:209–216. doi:10.1002/glia.20082 pmid:15252809
    OpenUrlCrossRefPubMed
  205. ↵
    1. Van Harreveld A,
    2. Fifkova E
    (1975) Swelling of dendritic spines in the fascia dentata after stimulation of the perforant fibers as a mechanism of post-tetanic potentiation. Exp Neurol 49:736–749. doi:10.1016/0014-4886(75)90055-2 pmid:173566
    OpenUrlCrossRefPubMed
  206. ↵
    1. Ventura R,
    2. Harris KM
    (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19:6897–6906. doi:10.1523/JNEUROSCI.19-16-06897.1999 pmid:10436047
    OpenUrlAbstract/FREE Full Text
  207. ↵
    1. Wake H,
    2. Lee PR,
    3. Fields RD
    (2011) Control of local protein synthesis and initial events in myelination by action potentials. Science 333:1647–1651. doi:10.1126/science.1206998 pmid:21817014
    OpenUrlAbstract/FREE Full Text
  208. ↵
    1. Wake H,
    2. Moorhouse AJ,
    3. Miyamoto A,
    4. Nabekura J
    (2013) Microglia: actively surveying and shaping neuronal circuit structure and function. Trends Neurosci 36:209–217. doi:10.1016/j.tins.2012.11.007 pmid:23260014
    OpenUrlCrossRefPubMed
  209. ↵
    1. Wake H,
    2. Ortiz FC,
    3. Woo DH,
    4. Lee PR,
    5. Angulo MC,
    6. Fields RD
    (2015) Nonsynaptic junctions on myelinating glia promote preferential myelination of electrically active axons. Nat Commun 6:7844. doi:10.1038/ncomms8844 pmid:26238238
    OpenUrlCrossRefPubMed
  210. ↵
    1. Wang HC,
    2. Bergles DE
    (2015) Spontaneous activity in the developing auditory system. Cell Tissue Res 361:65–75. doi:10.1007/s00441-014-2007-5 pmid:25296716
    OpenUrlCrossRefPubMed
  211. ↵
    1. Wang X,
    2. Lou N,
    3. Xu Q,
    4. Tian GF,
    5. Peng WG,
    6. Han X,
    7. Kang J,
    8. Takano T,
    9. Nedergaard M
    (2006) Astrocytic Ca2+ signaling evoked by sensory stimulation in vivo. Nat Neurosci 9:816–823. doi:10.1038/nn1703 pmid:16699507
    OpenUrlCrossRefPubMed
  212. ↵
    1. Watt AJ,
    2. Cuntz H,
    3. Mori M,
    4. Nusser Z,
    5. Sjöström PJ,
    6. Häusser M
    (2009) Traveling waves in developing cerebellar cortex mediated by asymmetrical Purkinje cell connectivity. Nat Neurosci 12:463–473. doi:10.1038/nn.2285 pmid:19287389
    OpenUrlCrossRefPubMed
  213. ↵
    1. Wiesel TN,
    2. Hubel DH
    (1963a) Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol 26:1003–1017. doi:10.1152/jn.1963.26.6.1003 pmid:14084161
    OpenUrlCrossRefPubMed
  214. ↵
    1. Wiesel TN,
    2. Hubel DH
    (1963b) Effects of visual deprivation on morphology and physiology of cells in the cats lateral geniculate body. J Neurophysiol 26:978–993. doi:10.1152/jn.1963.26.6.978 pmid:14084170
    OpenUrlCrossRefPubMed
  215. ↵
    1. Wong RO,
    2. Meister M,
    3. Shatz CJ
    (1993) Transient period of correlated bursting activity during development of the mammalian retina. Neuron 11:923–938. doi:10.1016/0896-6273(93)90122-8 pmid:8240814
    OpenUrlCrossRefPubMed
  216. ↵
    1. Wong RO,
    2. Chernjavsky A,
    3. Smith SJ,
    4. Shatz CJ
    (1995) Early functional neural networks in the developing retina. Nature 374:716–718. doi:10.1038/374716a0 pmid:7715725
    OpenUrlCrossRefPubMed
  217. ↵
    1. Xu T,
    2. Yu X,
    3. Perlik AJ,
    4. Tobin WF,
    5. Zweig JA,
    6. Tennant K,
    7. Jones T,
    8. Zuo Y
    (2009) Rapid formation and selective stabilization of synapses for enduring motor memories. Nature 462:915–919. doi:10.1038/nature08389 pmid:19946267
    OpenUrlCrossRefPubMed
  218. ↵
    1. Yakovlev P,
    2. Lecours A
    (1967) The myelogenetic cycles of regional maturation of the brain. In: Resional development of the brain in early life (Minkowski A, ed), pp 3–70. Oxford: Blackwell.
  219. ↵
    1. Yang G,
    2. Pan F,
    3. Gan WB
    (2009) Stably maintained dendritic spines are associated with lifelong memories. Nature 462:920–924. doi:10.1038/nature08577 pmid:19946265
    OpenUrlCrossRefPubMed
  220. ↵
    1. Yin JC,
    2. Wallach JS,
    3. Del Vecchio M,
    4. Wilder EL,
    5. Zhou H,
    6. Quinn WG,
    7. Tully T
    (1994) Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79:49–58. doi:10.1016/0092-8674(94)90399-9 pmid:7923376
    OpenUrlCrossRefPubMed
  221. ↵
    1. Yuste R,
    2. Peinado A,
    3. Katz LC
    (1992) Neuronal domains in developing neocortex. Science 257:665–669. doi:10.1126/science.1496379 pmid:1496379
    OpenUrlAbstract/FREE Full Text
  222. ↵
    1. Zhang Y,
    2. Barres BA
    (2010) Astrocyte heterogeneity: an underappreciated topic in neurobiology. Curr Opin Neurobiol 20:588–594. doi:10.1016/j.conb.2010.06.005 pmid:20655735
    OpenUrlCrossRefPubMed
Back to top

In this issue

The Journal of Neuroscience: 40 (5)
Journal of Neuroscience
Vol. 40, Issue 5
29 Jan 2020
  • Table of Contents
  • Table of Contents (PDF)
  • About the Cover
  • Index by author
  • Advertising (PDF)
  • Ed Board (PDF)
Email

Thank you for sharing this Journal of Neuroscience article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
Activity Shapes Neural Circuit Form and Function: A Historical Perspective
(Your Name) has forwarded a page to you from Journal of Neuroscience
(Your Name) thought you would be interested in this article in Journal of Neuroscience.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Print
View Full Page PDF
Citation Tools
Activity Shapes Neural Circuit Form and Function: A Historical Perspective
Yuan Pan, Michelle Monje
Journal of Neuroscience 29 January 2020, 40 (5) 944-954; DOI: 10.1523/JNEUROSCI.0740-19.2019

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Respond to this article
Request Permissions
Share
Activity Shapes Neural Circuit Form and Function: A Historical Perspective
Yuan Pan, Michelle Monje
Journal of Neuroscience 29 January 2020, 40 (5) 944-954; DOI: 10.1523/JNEUROSCI.0740-19.2019
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Google Plus One

Jump to section

  • Article
    • Abstract
    • Introduction
    • Footnotes
    • References
  • Figures & Data
  • Info & Metrics
  • eLetters
  • PDF

Responses to this article

Respond to this article

Jump to comment:

No eLetters have been published for this article.

Related Articles

Cited By...

More in this TOC Section

  • A Proposed Role for Interactions between Argonautes, miRISC, and RNA Binding Proteins in the Regulation of Local Translation in Neurons and Glia
  • Stopping Interference in Response Inhibition: Behavioral and Neural Signatures of Selective Stopping
  • From the Neuroscience of Individual Variability to Climate Change
Show more Viewpoints

Subjects

  • 50th Anniversary
  • Home
  • Alerts
  • Visit Society for Neuroscience on Facebook
  • Follow Society for Neuroscience on Twitter
  • Follow Society for Neuroscience on LinkedIn
  • Visit Society for Neuroscience on Youtube
  • Follow our RSS feeds

Content

  • Early Release
  • Current Issue
  • Issue Archive
  • Collections

Information

  • For Authors
  • For Advertisers
  • For the Media
  • For Subscribers

About

  • About the Journal
  • Editorial Board
  • Privacy Policy
  • Contact
(JNeurosci logo)
(SfN logo)

Copyright © 2022 by the Society for Neuroscience.
JNeurosci Online ISSN: 1529-2401

The ideas and opinions expressed in JNeurosci do not necessarily reflect those of SfN or the JNeurosci Editorial Board. Publication of an advertisement or other product mention in JNeurosci should not be construed as an endorsement of the manufacturer’s claims. SfN does not assume any responsibility for any injury and/or damage to persons or property arising from or related to any use of any material contained in JNeurosci.