Target-dependent structural changes in sensory neurons of aplysia accompany long-term heterosynaptic inhibition

doi:10.1016/0896-6273(91)90166-W

Neuron

Volume 6, Issue 5, May 1991, Pages 679-690

https://doi.org/10.1016/0896-6273(91)90166-W Get rights and content

Abstract

FMRFamide evokes both short-term and long-term inhibition of synapses between mechanosensory and motor neurons in Aplysia. We report here, using dissociated cell culture and low-light epifluorescence video microscopy, that depression lasting 24 hr of sensorimotor synapses evoked by four brief applications of FMRFamide is accompanied by a significant loss of sensory cell varicosities and neurites. These structural changes in the sensory cells require the presence of the target motor cell L7. Because the loss of structures known to contain transmitter release sites correlates significantly with the changes in the amplitude of the excitatory postsynaptic potential in L7, our results suggest that the structural changes evoked by FMRFamide reflect a loss of synaptic contacts. Thus, long-term depression parallels long-term facilitation of the sensorimotor synapse produced by serotonin in that both forms of heterosynaptic plasticity involve target-dependent modulation of the number of presynaptic varicosities.

References (47)

H. Blumenfeld et al.
Facilitatory and inhibitory transmitters modulate calcium influx during action potentials in Aplysia sensory neurons
Neuron
(1990)
D.L. Glanzman et al.
Identified target motor neuron regulates neurite outgrowth and synapse formation of Aplysia sensory neurons in vitro
Neuron
(1989)
M.P. Mattson et al.
Interactions between entorhinal axons and target hippocampal neurons: a role for glutamate in the development of hippocampal circuitry
Neuron
(1988)
D.P. McCobb et al.
Interactive effects of serotonin and acetylcholine on neurite elongation
Neuron
(1988)
F.A. Nazif et al.
cAMP induces long-term morphological changes in sensory neurons of Aplysia
Brain Res.
(1991)
T.W. Abrams et al.
Two endogenous neuropeptides modulate the gill and siphon withdrawal reflex in Aplysia by presynaptic facilitation involving cAMP-dependent closure of a serotoninsensitive potassium channel
D.L. Alkon et al.
Contraction of neuronal branching volume: an anatomic correlate of Pavlovian conditioning
C.H. Bailey et al.
Morphological basis of longterm habituation and sensitization in Aplysia
Science
(1983)
C.H. Bailey et al.
Long-term memory in Aplysia modulates the total number of varicosities of single identified sensory neurons
C.H. Bailey et al.
Morphological basis of shorterm habituation in Aplysia
J. Neurosci.
(1988)

C.H. Bailey et al.

Time course of structural changes at identified sensory neuron synapses during long-term sensitization in Aplysia

J. Neurosci.

(1989)

F. Belardetti et al.

Neuronal inhibition by the peptide FMRFamide involves opening of S-potassium channels

Nature

(1987)

L. Bernier et al.

Facilitatory transmitter causes a selective and prolonged increase in adenosine 3′:5′-monophosphate in sensory neurons mediating the gill and siphon withdrawal reflex in Aplysia

J. Neurosci.

(1982)

O. Braha et al.

Second messengers involved in the two processes of presynaptic facilitation that contribute to sensitization and dishabituation in Aplysia sensory neurons

V. Brezina et al.

Modulation of potassium conductances by an endogenous neuropeptide in neurons of Aplysia californica

J. Physiol.

(1987)

V. Brezina et al.

Suppression of calcium current by an endogenous neuropeptide in neurons of Aolysia californica

J. Physiol.

(1987)

N. Buttner et al.

Direct modulation of Aplysia S-potassium channels by a 12-lipoxygenare metabolite of arachidonic acid

Nature

(1989)

V.F. Castellucci et al.

Cellular analysis of long-term habituation of the gill-withdrawal reflex in Aglysia

Science

(1978)

N. Dale et al.

Facilitatory and inhibitory transmitters modulate spontaneous transmitter release at cultured Aplysia sensorimotor synapses

J. Physiol.

(1990)

N. Dale et al.

Long-term facilitation in Aplysia involves increase in transmitter release

Science

(1988)

P.K. Dash et al.

Injection of the cyclic AMP responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation

Nature

(1990)

B. Edmonds et al.

Contributions of two types of calcium channels to synaptic transmission and plasticity

Science

(1990)

P. Forscher et al.

Cyclic AMP induces changes in distribution and transport of organelles within growth cones of Aplysia bag cell neurons

J. Neurosci.

(1987)

Cited by (55)

Synaptic Plasticity
2014, From Molecules to Networks: An Introduction to Cellular and Molecular Neuroscience: Third Edition
Chemical synapses are not static transmitters of information. Their effectiveness waxes and wanes depending upon factors such as the frequency of stimulation and prior activity. The ability of synapses to change their strength, called synaptic plasticity, is critical not only for regulating the flow of information within neuronal circuits, but also for learning and memory. In homosynaptic plasticity, the strength of a synapse is changed as a consequence of activity in that synapse. In heterosynaptic plasticity, the strength of a synapse changes as a result of activity in a neuron or pathway extrinsic to that synapse. Both can occur over a wide range of temporal domains. Short-term plasticity refers to changes in synaptic strength that persist for seconds to minutes. Long-term plasticity refers to changes in synaptic strength that persist for hours, days to lifetimes. In this chapter, we consider the mechanisms that underlie short-term and long-term plasticity of chemical synapses.
Sensitization and habituation: Invertebrate
2007, Learning and Memory: A Comprehensive Reference
Invertebrates have been used extensively as simple model systems for the study of the mechanisms underlying learning and memory at the network, cellular, and molecular levels. In Aplysia and several other invertebrates, the two most characteristic forms of nonassociative learning, habituation and sensitization, rely on modifications of early afferent neurons and their synapses onto target cells. Whereas habituation is primarily attributed to activity-dependent synaptic depression, sensitization is often attributed to the facilitatory actions of neuromodulators, such as serotonin. This chapter reviews some of this progress with a particular emphasis on mechanisms of habituation and sensitization in the marine mollusc Aplysia.
Ubiquitin-proteasome-mediated local protein degradation and synaptic plasticity
2004, Progress in Neurobiology
A proteolytic pathway in which attachment of a small protein, ubiquitin, marks the substrates for degradation by a multi-subunit complex called the proteasome has been shown to function in synaptic plasticity and in several other physiological processes of the nervous system. Attachment of ubiquitin to protein substrates occurs through a series of highly specific and regulated steps. Degradation by the proteasome is subject to multiple levels of regulation as well. How does the ubiquitin-proteasome pathway contribute to synaptic plasticity? Long-lasting, protein synthesis-dependent, changes in the synaptic strength occur through activation of molecular cascades in the nucleus in coordination with signaling events in specific synapses. Available evidence indicates that ubiquitin-proteasome-mediated degradation has a role in the molecular mechanisms underlying synaptic plasticity that operate in the nucleus as well as at the synapse. Since the ubiquitin-proteasome pathway has been shown to be versatile in having roles in addition to proteolysis in several other cellular processes relevant to synaptic plasticity, such as endocytosis and transcription, this pathway is highly suited for a localized role in the neuron. Because of its numerous roles, malfunctioning of this pathway leads to several diseases and disorders of the nervous system. In this review, I examine the ubiquitin-proteasome pathway in detail and describe the role of regulated proteolysis in long-term synaptic plasticity. Also, using synaptic tagging theory of synapse-specific plasticity, I provide a model on the possible roles and regulation of local protein degradation by the ubiquitin-proteasome pathway.
Time windows for effects of protein synthesis inhibitors on Pavlovian conditioning in Hermissenda: Behavioral aspects
2003, Neurobiology of Learning and Memory
Inhibitors of protein and mRNA syntheses inhibit long-term memory (LTM), but we lack information about the time windows during which those inhibitors are effective.
Anisomycin (a protein synthesis translation inhibitor) was given to Hermissenda crassicornis which had received sufficient Pavlovian conditioning to produce LTM. When tested after 90 min, LTM recall was blocked when anisomycin was administered until 13 min after conditioning and from 65 to 75 min. There was good recall from 16 to 60 min.
When tested at 240 min, two periods of sensitivity to anisomycin were revealed: one finished before 20 min, while the other lasted from 60 to 220 min.
A brief study of the transcription inhibitor actinomycin-D found its action similar to that of anisomycin, except not inhibiting recall from about 160 to 220 min.
Influence of the target on distribution and functioning of the varicosities of Helix pomatia metacerebral cell C1 in dissociated cell culture
2000, Neuroscience
The serotonergic metacerebral giant cell (C1) of Helix pomatia was isolated with its bifurcate axon and plated in culture under five conditions: (i) with no target; (ii) with the appropriate target B2 near the stump of the bigger branch (CBC); (iii) with B2 near the stump of the smaller branch (CC); (iv) with a wrong target (C3) near the stump of the CBC branch and (v) with B2 and C3 positioned near the CBC and CC stump, respectively. The counting of anti-serotonin antibody-labelled varicosities of the C1 neuron showed that the presence of the appropriate target in either axonal domain both down-regulated the number of varicosities of the contralateral neuritic field, and increased their average size, whereas the wrong target induced an overall reduction of the number of C1 neuron varicosities, and inhibited the evoked transmitter release. The action potential-evoked calcium concentration increase in the neuritic terminals of the C1 neuron cultured alone, or in presence of the appropriate target, reached a value significantly higher than that reached in presence of the wrong target.
These results provide evidence that the postsynaptic neuron regulates both morphological and functional development of presynaptic terminals.
Positive and negative regulatory mechanisms that mediate long-term memory storage
1998, Brain Research Reviews
The protein kinase A pathway and the cyclic AMP-response element binding protein (CREB) appear to play a critical role in the consolidation of short-term changes in neuronal activity into long-term memory storage in a variety of systems ranging from the gill and siphon withdrawal reflex in Aplysia to olfactory conditioning in Drosophila to spatial and contextual learning in mice. In this review we describe the molecular machinery that mediates memory consolidation in each of these systems. One of the surprising findings to emerge, particularly from studies of long-term facilitation in Aplysia, is that memory storage is mediated by not only positive but also negative regulatory mechanisms, in much the same way as cell division is controlled by the proteins encoded by oncogenes and tumor suppressor genes. This suggests the interesting possibility that there are memory suppressor genes whose protein products impede memory storage.

View all citing articles on Scopus

^∗: Present address: Dipartimento di Anatomia e Fisiologia Umana, Corso Raffaello 30, 10125 Torino, Italy.

View full text

Neuron

ArticleTarget-dependent structural changes in sensory neurons of aplysia accompany long-term heterosynaptic inhibition

Abstract

Neuron

Neuron

Neuron

Neuron

Brain Res.

Two endogenous neuropeptides modulate the gill and siphon withdrawal reflex in Aplysia by presynaptic facilitation involving cAMP-dependent closure of a serotoninsensitive potassium channel

Contraction of neuronal branching volume: an anatomic correlate of Pavlovian conditioning

Morphological basis of longterm habituation and sensitization in Aplysia

Science

Long-term memory in Aplysia modulates the total number of varicosities of single identified sensory neurons

Morphological basis of shorterm habituation in Aplysia

J. Neurosci.

Time course of structural changes at identified sensory neuron synapses during long-term sensitization in Aplysia

J. Neurosci.

Neuronal inhibition by the peptide FMRFamide involves opening of S-potassium channels

Nature

Facilitatory transmitter causes a selective and prolonged increase in adenosine 3′:5′-monophosphate in sensory neurons mediating the gill and siphon withdrawal reflex in Aplysia

J. Neurosci.

Second messengers involved in the two processes of presynaptic facilitation that contribute to sensitization and dishabituation in Aplysia sensory neurons

Modulation of potassium conductances by an endogenous neuropeptide in neurons of Aplysia californica

J. Physiol.

Suppression of calcium current by an endogenous neuropeptide in neurons of Aolysia californica

J. Physiol.

Direct modulation of Aplysia S-potassium channels by a 12-lipoxygenare metabolite of arachidonic acid

Nature

Cellular analysis of long-term habituation of the gill-withdrawal reflex in Aglysia

Science

Facilitatory and inhibitory transmitters modulate spontaneous transmitter release at cultured Aplysia sensorimotor synapses

J. Physiol.

Long-term facilitation in Aplysia involves increase in transmitter release

Science

Injection of the cyclic AMP responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation

Nature

Contributions of two types of calcium channels to synaptic transmission and plasticity

Science

Cyclic AMP induces changes in distribution and transport of organelles within growth cones of Aplysia bag cell neurons

J. Neurosci.

Article
Target-dependent structural changes in sensory neurons of aplysia accompany long-term heterosynaptic inhibition