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Review
. 2014 Mar 28:8:93.
doi: 10.3389/fncel.2014.00093. eCollection 2014.

Modulating excitation through plasticity at inhibitory synapses

Vivien Chevaleyre  1 , Rebecca Piskorowski  1
Affiliations
Review

Modulating excitation through plasticity at inhibitory synapses

Vivien Chevaleyre et al. Front Cell Neurosci. .

Abstract

Learning is believed to depend on lasting changes in synaptic efficacy such as long-term potentiation and long-term depression. As a result, a profusion of studies has tried to elucidate the mechanisms underlying these forms of plasticity. Traditionally, experience-dependent changes at excitatory synapses were assumed to underlie learning and memory formation. However, with the relatively more recent investigation of inhibitory transmission, it had become evident that inhibitory synapses are not only plastic, but also provide an additional way to modulate excitatory transmission and the induction of plasticity at excitatory synapses. Thanks to recent technological advances, progress has been made in understanding synaptic transmission and plasticity from particular interneuron subtypes. In this review article, we will describe various forms of synaptic plasticity that have been ascribed to two fairly well characterized populations of interneurons in the hippocampus, those expressing cholecystokinin (CCK) and parvalbumin (PV). We will discuss the resulting changes in the strength and plasticity of excitatory transmission that occur in the local circuit as a result of the modulation of inhibitory transmission. We will focus on the hippocampus because this region has a relatively well-understood circuitry, numerous forms of activity-dependent plasticity and a multitude of identified interneuron subclasses.

Keywords: CCK+; PV+; hippocampus; inhibition; plasticity.

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Figures

Figure 1
Figure 1
Modulation and roles of GABA release from CCK+ interneurons. CCK+ interneurons target pyramidal cell soma (basket cell, BS) or dendrites (Schaffer collateral-associated cell, SC-A and lacunosum moleculare-radiatum-perforant path-associated cell, LM-R-PP-A) (see Somogyi and Klausberger, 2005). The release of GABA from CCK+ cell terminals is mediated by N-type calcium channels, which provide a loose coupling between calcium influx and exocytosis and partially underlie the asynchronous release of GABA by these cells. GABA release is negatively controlled by the activation of several receptors: CB1 cannabinoid receptors, GABAB receptors and kainate receptors. The decrease in GABA release differently impacts excitatory synapses depending on which subset of CCK+ interneuron synapses are depressed. A decrease in dendritic-targeting CCK+ synapse facilitates LTP induction at SC-CA1 synapses and increases the ability of an excitatory post synaptic potential (EPSP) to evoke an action potential (E-S coupling). When GABA release at somatic-targeting CCK+ synapses is depressed, a large increase in the amplitude of the SC EPSPs is observed, but distal perforant path (PP) EPSPs are unaltered.
Figure 2
Figure 2
Modulation and roles of GABA release from PV+ interneurons. PV+ interneurons target either the soma (basket cell, BS), the axon (axo-axonic cell, AA) or the dendrites (bistratified cell, BS and oriens-lacunosum moleculare cell, OLM) of pyramidal cells (see Somogyi and Klausberger, 2005). The release of GABA from PV+ cell terminals is mediated by P/Q-type calcium channels. The tight coupling between calcium influx and exocytosis machinery results in precisely timed vesicle release. The release of GABA at PV+ cell synapses is negatively controlled by diverse receptors including mu- and delta-opioid receptors (MOR and DOR) and muscarinic M2 receptors. Conversely, GABA release from PV cells is increased by activation of the Neuregulin 1 receptor ErbB4. LTP induction at SC-CA1 synapses is impaired following ErB4 activation in PV+ cells due to increased pre-synaptic GABA release by PV+ cells.
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