Trends in Neurosciences

Trends in Neurosciences

Volume 38, Issue 9, September 2015, Pages 524-534
Journal home page for Trends in Neurosciences

Review
The neuronal identity bias behind neocortical GABAergic plasticity

https://doi.org/10.1016/j.tins.2015.07.008Get rights and content

Highlights

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    Cortical circuits result from highly specific connections between inhibitory and excitatory neuron subtypes.

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    Different neocortical principal neuron (PN) subtypes are preferentially targeted by specific basket cell classes.

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    PNs in different cortical layers express either depression or potentiation of perisomatic inhibition.

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    PNs relaying to subcortical areas tend to potentiate their perisomatic inhibition.

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    PNs connecting to other cortical areas tend to depress their perisomatic inhibition.

In the neocortex, different types of excitatory and inhibitory neurons connect to one another following a detailed blueprint, defining functionally-distinct subnetworks, whose activity and modulation underlie complex cognitive functions. We review the cell-autonomous plasticity of perisomatic inhibition onto principal excitatory neurons. We propose that the tendency of different cortical layers to exhibit depression or potentiation of perisomatic inhibition is dictated by the specific identities of principal neurons (PNs). These are mainly defined by their projection targets and by their preference to be innervated by specific perisomatic-targeting basket cell types. Therefore, principal neurons responsible for relaying information to subcortical nuclei are differentially inhibited and show specific forms of plasticity compared to other PNs that are specialized in more associative functions.

Section snippets

Information flow across neocortical layers

Higher brain functions, such as conscious perception and cognition, result from the correct flow of information between different neuronal cortical circuits. These circuits are composed of highly interconnected neurons, about 80% of which are glutamatergic (excitatory) PNs that are functionally and anatomically organized in six radial layers [1]. Cortical layer identity is defined by the density of specific PNs as well as by their afferent and efferent projections, thereby conferring each layer

Functional diversity of cortical inhibitory circuits and their plasticity

Neocortical interneurons are highly heterogeneous and can be classified by several anatomical and functional features 33, 34, 35, 36, 37 (Table 1). Despite the great diversity, however, one relevant functional classification relies on their specialized connectivity pattern with specific domains of PNs. Indeed, basket cells (BCs) predominantly form synapses onto the perisomatic region of PNs, making them ideally suited to control PN spike timing 38, 39, 40, 41, 42, 43, 44, 45. In particular, BCs

Is there a layer-specificity of cell-autonomous cortical GABAergic plasticity? The case of CB1+ and CB1− BCs

Neocortical GABAergic synapses can be potentiated or depressed in response to several conditioning protocols, such as, for example, those involving simultaneous activation of pre- and postsynaptic neurons, including spike timing-dependent plasticity (similar to associative or Hebbian plasticity; see Glossary) 62, 63, 64. However, GABAergic synapses can undergo short (seconds)- or long (hours)-term changes in their strength in a cell-autonomous, non-associative manner; in other words, GABAergic

Is cortical GABAergic plasticity determined by postsynaptic PN identity?

Recent work suggests that neurons do not connect to other components of the neuronal network indiscriminately, but follow a detailed blueprint. This is true for specific connections between specific interneuron subtypes 54, 55, 56, resulting in highly defined disinhibitory circuits. Likewise, PNs prefer to connect to other PNs that share specific projection targets 107, 108, a common progenitor 109, 110, or a tendency to be activated by specific external stimuli 111, 112, 113, 114. Moreover,

Functional relevance

Given the staggering diversity of synaptic properties originating from different neuronal types, identifying the function of plasticity of a specific synapse can be a daunting task and, for this reason, the functional role of plasticity at GABAergic inhibitory synapses remains poorly understood. Recently developed technologies that allow the identification and manipulation of specific subsets of neurons in the mouse brain provide an unprecedented opportunity to probe the role of GABAergic

Concluding remarks and future directions

In this review we have attempted to find a rule underlying the layer-segregation of cell-autonomous non-associative plasticity of perisomatic GABAergic synapses originating from different populations of inhibitory neurons impinging onto different subtypes of neocortical PNs. We have highlighted layer- and cell type-specificity of preferential GABAergic innervation of PNs by distinct interneuron classes. This specialized connectivity scheme can result in finely tuned forms of GABAergic

Acknowledgments

We thank Vikaas Sohal, Giovanni Marsicano, Charlotte Deleuze, and Andrea Barberis for critically reading this manuscript. Our laboratory is supported by the Giovanni Armenise-Harvard Foundation: Career Development Award; European Research Council (ERC) under the European Commission 7th Framework Programmme (FP7/2007-2013)/ERC grant 200808); ‘Investissements d’Avenir’ ANR-10-IAIHU-06; Agence Nationale de la Recherche (ANR-13-BSV4-0015-01); and a grant from the ICM (Paris).

Glossary

Associative or Hebbian plasticity
the ability to change the strength of synaptic transmission (either potentiating or depressing it) via the coordinated activity of pre- and postsynaptic neurons, based on Donald Hebb's definition. In the case of inhibitory synapses, the application of this rule is somewhat paradoxical because increased activation of inhibitory synapses results in decreased postsynaptic excitability.
Interneurons
originally described by Santiago Ramón y Cajal as small neurons with

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