Update articleControlling the critical period
Introduction
At no time in life is the brain so easily shaped by experience than in infancy and early childhood (Doupe and Kuhl, 1999, Daw, 1995). It is during these “critical periods” that neural circuits acquire language with native fluency, reproduce the courtship song of a parent bird, expand the representation of a stimulated whisker, or eliminate responsiveness to an occluded eye (ocular dominance, OD). Unraveling the mechanisms that limit such dramatic plasticity to early life would pave the way for novel paradigms or therapeutic agents for rehabilitation, recovery from injury, or improved learning in adulthood. Recent results primarily in the visual system indicate we are ever closer to reaching this elusive goal (Linkenhoker and Knudsen, 2002, Pizzorusso et al., 2002).
Essentially two lines of reasoning have been pursued (Fig. 1). In one view, the potential for plasticity is never lost, but merely tempered by an evolving dynamic of neural activation that can effectively tap into the process. One would thus need to identify the correct “training” regimen to coax these neural networks out of one stable state into another. It may simply be easier to do so in immature tissue, whose composition of receptors and downstream signaling machinery is actively changing. Alternatively, one may posit that amidst this molecular maelstrom appears a class of factors that are inhibitory to further plasticity, eventually preventing large-scale circuit reorganization and thereby structurally closing the critical period. Evidence has now been presented for both possibilities.
Section snippets
Stabilization of network dynamics
The most convincing demonstration that a “critical period” for plasticity exists would be the ability to directly manipulate timing of its expression. Remarkably, this has only recently been achieved in the classical model system of primary visual cortex. Converging inputs from the two eyes typically compete for connectivity (OD) with a peak sensitivity to monocular deprivation around 1 month after birth in cats and rodents (Hubel and Wiesel, 1970, Daw, 1995, Fagiolini and Hensch, 2000). Yet,
Relevance of synaptic plasticity rules
Taken together, these findings argue against a primary role for turning on and off excitatory synaptic plasticity rules to establish a critical period. Enhancing inhibition enables plasticity in visual cortex in vivo (Fagiolini and Hensch, 2000), but suppresses long-term potentiation (LTP) induced by high-frequency stimulation in vitro (Huang et al., 1999). Likewise, long-term depression (LTD) is reportedly most robust in young wild-type mice before the critical period, when OD plasticity is
Structural consolidation of circuits
A different view of critical period closure is an anatomical one (Fig. 1B). For instance, in barrel cortex the critical period refers to the capacity for anatomical expansion or contraction of individual whisker representations just after birth (Van der Loos and Woolsey, 1973, Lu et al., 2001, Datwani et al., 2002). If a row of whiskers is removed (cauterized) just after birth, barrels serving the deprived whiskers shrink while neighboring barrels from the intact whiskers expand. The degree of
Future directions
So, does the critical period permanently hard-wire our brains or can we enjoy massive plasticity throughout life by finding the right stimulation protocols? As is common in biology, both views are likely to be correct. Curiously, perineuronal nets mainly surround fast-spiking, parvalbumin-positive interneurons (Fig. 1B), whose function may be particularly sensitive to extracellular ionic balance (Hartig et al., 1999). This raises the possibility that Maffei and colleagues re-opened the critical
References (48)
- et al.
Perineuronal nets: past and present
Trends Neurosci.
(1998) - et al.
Cortical neurons immunoreactive for the potassium channel Kv3.1b subunit are predominantly surrounded by perineuronal nets presumed as a buffering system for cations
Brain Res.
(1999) - et al.
BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex
Cell
(1999) - et al.
Barrel cortex critical period plasticity is independent of changes in NMDA receptor subunit composition
Neuron
(2001) The effect of dark rearing on the time course of the critical period in cat visual cortex
Dev. Brain Res.
(1991)- et al.
Rapid development and plasticity of layer 2/3 maps in rat barrel cortex in vivo
Neuron
(2001) - et al.
Rapid ocular dominance plasticity requires cortical but not geniculate protein synthesis
Neuron
(2002) - et al.
Rapid remodeling of axonal arbors in the visual cortex
Science
(1993) - et al.
Protein synthesis and transcription-dependent LTD in mouse visual cortex
US Soc. Neurosci. Abstr.
(2002) - et al.
Synaptic modification by correlated activity: Hebb's postulate revisited
Annu. Rev. Neurosci.
(2001)
Environmental noise retards auditory cortical development
Science
Absence of long-term depression in the visual cortex of glutamic acid decarboxylase-65 knock-out mice
J. Neurosci.
Prolonged sensitivity to monocular deprivation in dark-reared cats
J. Neurophysiol.
Lesion-induced thalamocortical axonal plasticity in the S1 cortex is independent of NMDA receptor function in excitatory cortical neurons
J. Neurosci.
Visual Development
Visual Development
Birdsong and human speech: common themes and mechanisms
Annu. Rev. Neurosci.
Inhibitory threshold for critical-period induction in visual cortex
Nature
Separable features of visual cortical plasticity revealed through N-Methyl-d-aspartate receptor 2A signaling
Proc. Natl. Acad. Sci. USA
Inhibition and plasticity
Nat. Neurosci.
Spike-timing-dependent synaptic modification induced by natural spike trains
Nature
Neurogenesis in the adult brain
J. Neurosci.
Long-term dendritic spine stability in the adult cortex
Nature
Nerve growth factor-induced ocular dominance plasticity in adult cat visual cortex
Proc. Natl. Acad. Sci. USA
Cited by (64)
Critical periods and Autism Spectrum Disorders, a role for sleep
2023, Neurobiology of Sleep and Circadian RhythmsCitation Excerpt :While heightened plasticity allows us to shape neuronal circuits, this also introduces vulnerability. Therefore, disruptions early in life can result in neuronal circuits that respond differently to experiences later on (Hensch, 2003, 2004; Knudsen, 2004; Rice and Barone, 2000). In the last four decades, developmental windows for our brain's ability to attune to experience have been widely studied, emphasizing the importance of critical periods in the developing brain (Rice and Barone, 2000).
Links Between Human and Animal Models of Trauma and Psychosis: A Narrative Review
2021, Biological Psychiatry: Cognitive Neuroscience and NeuroimagingCitation Excerpt :Impairments in interneuron signaling may underlie altered gamma oscillations and working memory deficits in schizophrenia (104). Rodent studies corroborate the human findings that maturation of parvalbumin-mediated inhibitory neurons may help regulate postnatal development of synaptic plasticity in the cerebral cortex (105,106). In animal models, stress resulted in changes in the hippocampus and PFC pathway, with acute exposures modulating synaptic plasticity (107) and memory performance (108).
Potential involvement of perineuronal nets in brain aging: An anatomical point of view
2021, Factors Affecting Neurological Aging: Genetics, Neurology, Behavior, and DietA conceptualized model linking matrix metalloproteinase-9 to schizophrenia pathogenesis
2020, Schizophrenia ResearchCitation Excerpt :This sets the stage for the subsequent cascade of events that can ultimately lead to the emergence of full-blown schizophrenia a decade or two later during late adolescence and early adulthood, as persistent elevation of MMP-9 throughout postnatal development into adulthood can lead to the disruption of the periadolescent neurodevelopmental processes, resulting in the dysmaturation of cortical circuitry and thereby triggering schizophrenia onset. The postnatal maturation of cortical circuitry is a protracted process regulated in part by the progressively increased precision of perisomatic inhibition of pyramidal neurons mediated by the maturation of PV neurons and PNNs (Berardi et al., 2000; Di Cristo, 2007; Gianfranceschi et al., 2003; Hanover et al., 1999; Hensch, 2003; Huang et al., 1999; Itami et al., 2007; Jiang et al., 2005; Katagiri et al., 2007; Kirkwood et al., 1995; Tropea et al., 2006). Studies in the rodent visual cortex have revealed that the functional maturation of PV neurons during postnatal cortical development requires the homeoprotein orthodenticle homeobox2 (OTX2) (Beurdeley et al., 2012; Sugiyama et al., 2009).
Plasticity in early language acquisition: The effects of prenatal and early childhood experience
2015, Current Opinion in Neurobiology