Long-term plasticity at inhibitory synapses

Castillo, Pablo E.; Chiu, Chia-Yu; Carroll, Reed C.

doi:10.1016/j.conb.2011.01.006

Cited by 203 publications

(174 citation statements)

References 96 publications

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“…Inhibitory GABAergic interneurons are highly diverse in their morphological and physiological properties (29,30) and play many roles in microcircuit computation (31,32), including balancing excitation and inhibition to sustain cortical network stability (33)(34)(35)(36). This versatility is enabled in part through a diverse set of plasticity mechanisms that allow inhibition to be modulated by sensory experience (26,(37)(38)(39)(40). Hebbian (LTP and LTD) and spike-timing-dependent forms of plasticity at inhibitory synapses have been broadly described in multiple brain areas and involve numerous induction and expression mechanisms (27,37,(41)(42)(43).…”

Section: Discussionmentioning

confidence: 99%

“…We wondered whether this might reflect developmental changes in the underlying signaling pathways that trigger plasticity at this synapse. The signaling pathways responsible for plasticity at neocortical L4 FS→SP synapses are not currently known; however, some forms of neocortical LTP of inhibition depend on GABA B R signaling (26,27), whereas some forms of neocortical LTD of inhibition depend on endocannabinoid signaling (26,28). Here we asked whether L4 FS→SP plasticity is also dependent on GABA B R signaling.…”

Section: Developmental Profile Of Long-term Plasticity At Fs→sp Synapmentioning

confidence: 98%

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Long-term inhibitory plasticity in visual cortical layer 4 switches sign at the opening of the critical period

Lefort

Gray

Turrigiano

2013

Proc. Natl. Acad. Sci. U.S.A.

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Sensory microcircuits are refined by experience during windows of heightened plasticity termed "critical periods" (CPs). In visual cortex the effects of visual deprivation change dramatically at the transition from the pre-CP to the CP, but the cellular plasticity mechanisms that underlie this change are poorly understood. Here we show that plasticity at unitary connections between GABAergic Fast Spiking (FS) cells and Star Pyramidal (SP) neurons within layer 4 flips sign at the transition between the pre-CP and the CP. During the pre-CP, coupling FS firing with SP depolarization induces longterm depression of inhibition at this synapse, whereas the same protocol induces long-term potentiation of inhibition at the opening of the CP. Despite being of opposite sign, both forms of plasticity share expression characteristics-a change in coefficient of variation with no change in paired-pulse ratio-and depend on GABA B receptor signaling. Finally, we show that the reciprocal SP→FS synapse also acquires the ability to undergo long-term potentiation at the pre-CP to CP transition. Thus, at the opening of the CP, there are coordinated changes in plasticity that allow specific patterns of activity within layer 4 to potentiate feedback inhibition by boosting the strength of FS↔SP connections.S ensory microcircuits are refined by experience during windows of heightened plasticity termed "critical periods" (CPs). In visual cortex the classical CP was defined based on when visual deprivation (VD) induces ocular dominance (OD) shifts, between approximately postnatal days (P) 20-33 (1-3). However, visual cortex is also plastic during a pre-CP between eye opening (∼P14) and the onset of the classical CP (4-6). Although both developmental windows are characterized by sensitivity to visual experience, the effects of VD change dramatically at the transition between these two developmental stages (7-10).The cellular changes that underlie the transition from pre-CP to CP plasticity remain incompletely understood, but recent work has implicated a specific inhibitory network involving parvalbumin-positive fast-spiking (FS) basket cells in this process (8,11,12). FS cells provide strong somatic inhibition onto cortical pyramidal neurons, and this inhibition matures significantly between eye opening and the opening of the classical CP (13-15). Further, reducing or enhancing this inhibition can prevent or prematurely trigger the transition from pre-CP to CP plasticity (11,(16)(17)(18). Thus, maturation of FS inhibition is thought to be causally involved in triggering CP plasticity, but exactly what aspect of this maturation drives these changes is unknown. One characteristic of this maturation is a change in the response of FS synapses to VD. Brief monocular VD during the pre-CP decreases inhibitory synaptic strength from FS to star pyramidal (SP) neurons in layer 4 (L4) of the monocular primary visual cortex [V1m (19)] but increases inhibition at the same synapse when performed during the CP (20). There is evidence that longterm potenti...

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Section: Discussionmentioning

confidence: 99%

Section: Developmental Profile Of Long-term Plasticity At Fs→sp Synapmentioning

confidence: 98%

Long-term inhibitory plasticity in visual cortical layer 4 switches sign at the opening of the critical period

Lefort

Gray

Turrigiano

2013

Proc. Natl. Acad. Sci. U.S.A.

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“…Although the vast majority of work on the mechanisms and functions of LTP and LTD have focused on excitatory synapses, potentiation and depression of inhibitory transmission (I-LTP/I-LTD) can also be observed in the brain (Castillo et al 2011). The underlying molecular mechanisms of I-LTP and I-LTD are variable, but one common feature is that they are often heterosynaptic.…”

Section: Nmdar-dependent Ltp Of Inhibitory Transmissionmentioning

confidence: 99%

NMDA Receptor-Dependent Long-Term Potentiation and Long-Term Depression (LTP/LTD)

Lüscher¹,

Malenka²

2012

Cold Spring Harbor Perspectives in Biology

850

647

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Long-term potentiation and long-term depression (LTP/LTD) can be elicited by activating N-methyl-D-aspartate (NMDA)-type glutamate receptors, typically by the coincident activity of pre-and postsynaptic neurons. The early phases of expression are mediated by a redistribution of AMPA-type glutamate receptors: More receptors are added to potentiate the synapse or receptors are removed to weaken synapses. With time, structural changes become apparent, which in general require the synthesis of new proteins. The investigation of the molecular and cellular mechanisms underlying these forms of synaptic plasticity has received much attention, because NMDA receptor-dependent LTP and LTD may constitute cellular substrates of learning and memory.L ong-term synaptic plasticity is a generic term that applies to a long-lasting experience-dependent change in the efficacy of synaptic transmission. Here we will focus on N-methyl-D-aspartate (NMDA) receptor-dependent synaptic potentiation (LTP) and depression (LTD), two forms of activity-dependent long-term changes in synaptic efficacy that have been extensively studied. Because both LTP and LTD are believed to represent cellular correlates of learning and memory, they have attracted considerable interest. In this article we will focus on the molecular and cellular mechanisms associated with LTP and LTD. As for other forms of long-term synaptic plasticity, a characterization of LTP and LTD involves describing the molecular mechanisms that are required to elicit the change (induction), followed by an investigation of the mechanism of expression (hours) and maintenance (days). The best-characterized form of NMDA receptor (NMDAR)-dependent LTP occurs between CA3 and CA1 pyramidal neurons of the hippocampus (Fig. 1). Throughout the chapter we will mostly refer to this specific form of LTP. At these CA3-CA1 Schaffer collateral synapses, the loci of both induction and expression are situated in the postsynaptic neuron. AMPA-TYPE AND NMDA-TYPE GLUTAMATE RECEPTORSAfter exocytotic release of the content of the synaptic vesicle from the presynaptic specialization (see Castillo 2012), the neurotransmitter

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“…Previous studies have shown that presynaptic LTP of GABAergic synapses usually arises from a heterosynaptic mechanism that requires retrograde signaling, which is often mediated through postsynaptic NMDA receptor activation (52,53). Although glutamate is not the main excitatory transmitter in insect brains, it is likely that NMDA receptors, which typically mediate synapse plasticity rather than synaptic depolarization (54), serve evolutionarily conserved functions in synaptic plasticity (55).…”

Section: Pn-specific Nmda Receptors May Explain Odorant Selectivity Inmentioning

confidence: 99%

Plasticity of local GABAergic interneurons drives olfactory habituation

Das

Sadanandappa

Dervan

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

203

355

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Despite its ubiquity and significance, behavioral habituation is poorly understood in terms of the underlying neural circuit mechanisms. Here, we present evidence that habituation arises from potentiation of inhibitory transmission within a circuit motif commonly repeated in the nervous system. In Drosophila, prior odorant exposure results in a selective reduction of response to this odorant. Both short-term (STH) and long-term (LTH) forms of olfactory habituation require function of the rutabaga-encoded adenylate cyclase in multiglomerular local interneurons (LNs) that mediate GABAergic inhibition in the antennal lobe; LTH additionally requires function of the cAMP response element-binding protein (CREB2) transcription factor in LNs. The odorant selectivity of STH and LTH is mirrored by requirement for NMDA receptors and GABA A receptors in odorant-selective, glomerulus-specific projection neurons (PNs). The need for the vesicular glutamate transporter in LNs indicates that a subset of these GABAergic neurons also releases glutamate. LTH is associated with a reduction of odorant-evoked calcium fluxes in PNs as well as growth of the respective odorant-responsive glomeruli. These cellular changes use similar mechanisms to those required for behavioral habituation. Taken together with the observation that enhancement of GABAergic transmission is sufficient to attenuate olfactory behavior, these data indicate that habituation arises from glomerulus-selective potentiation of inhibitory synapses in the antennal lobe. We suggest that similar circuit mechanisms may operate in other species and sensory systems.abituation is a specific form of implicit learning in which repeated exposure to an unreinforced stimulus results in a decreased behavioral response (1-3). By filtering out such constant sensory input, habituation enhances an animal's ability to focus its cognitive resources on novel or salient features of the environment. Thus, habituation serves as a building block for normal cognition (2, 4). Although it has been studied in many different contexts, causal connections between mechanisms, neuronal changes, and behavioral habituation have not been clearly identified (2). Given our current understanding, it remains unclear whether similar or distinct mechanisms underlie different forms of habituation; also unclear is how these mechanisms compare with those mechanisms used in consolidation or extinction of associative memory (1, 5).The olfactory system provides an experimentally accessible circuit in which to analyze mechanisms that underlie different timescales of behavioral habituation (4, 6, 7). Particularly useful is the adult Drosophila olfactory system, which has organization similar to that of mammals (8, 9). Here, olfactory sensory neurons (OSNs) expressing a single type of functional odorant receptor molecules (ORs) send axons to the antennal lobe and synapse onto (i) glomerulus-specific projection neurons (PNs) that project to the mushroom body and lateral horn, (ii) multiglomerular local interneurons (LNs...

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Long-term plasticity at inhibitory synapses

Cited by 203 publications

References 96 publications

Long-term inhibitory plasticity in visual cortical layer 4 switches sign at the opening of the critical period

Long-term inhibitory plasticity in visual cortical layer 4 switches sign at the opening of the critical period

NMDA Receptor-Dependent Long-Term Potentiation and Long-Term Depression (LTP/LTD)

Plasticity of local GABAergic interneurons drives olfactory habituation

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