Cortical interneurons that specialize in disinhibitory control

By H. Pi, B. Hangya, D. Kvitsiani, Joshua I. Sanders, Z. J. Huang, Adam Kepecs. 2013

1,117 citations recorded by the source corpus.

In the mammalian cerebral cortex the diversity of interneuronal subtypes underlies a division of labour subserving distinct modes of inhibitory control. A unique mode of inhibitory control may be provided by inhibitory neurons that specifically suppress the firing of other inhibitory neurons. Such disinhibition could lead to the selective amplification of local processing and serve the important computational functions of gating and gain modulation. Although several interneuron populations are known to target other interneurons to varying degrees, little is known about interneurons specializing in disinhibition and their in vivo function. Here we show that a class of interneurons that express vasoactive intestinal polypeptide (VIP) mediates disinhibitory control in multiple areas of neocortex and is recruited by reinforcement signals. By combining optogenetic activation with single-cell recordings, we examined the functional role of VIP interneurons in awake mice, and investigated the underlying circuit mechanisms in vitro in auditory and medial prefrontal cortices. We identified a basic disinhibitory circuit module in which activation of VIP interneurons transiently suppresses primarily somatostatin- and a fraction of parvalbumin-expressing inhibitory interneurons that specialize in the control of the input and output of principal cells, respectively. During the performance of an auditory discrimination task, reinforcement signals (reward and punishment) strongly and uniformly activated VIP neurons in auditory cortex, and in turn VIP recruitment increased the gain of a functional subpopulation of principal neurons. These results reveal a specific cell type and microcircuit underlying disinhibitory control in cortex and demonstrate that it is activated under specific behavioural conditions.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience, Neuroscience

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Citations in the corpus

Recurrent World Models Facilitate Policy Evolution (2018, background): “Primary sensory neurons are released from inhibition when rewards are received, which suggests that they generally learn task-relevant features, rather than just any features, at least in adulthood [65].”
World Models (2018, background): “Primary sensory neurons are released from inhibition when rewards are received, which suggests that they generally learn task-relevant features, rather than just any features, at least in adulthood (Pi et al., 2013).”
Parallel processing by cortical inhibition enables context-dependent behavior (2016, neutral): “These three interneuron subtypes are thought to make up a canonical cortical circuit 7,31,36 .”
Interaction of feedforward and feedback streams in visual cortex in a firing-rate model of columnar computations (2014, background): “Recent evidence suggests that such specific local inhibitory-toinhibitory cell connections build local microcircuit modules to implement in vivo disinhibitory mechanisms (Jiang, Wang, Lee, Stornetta, & Zhu, 2013; Pi et al., 2013).”
Cortical membrane potential signature of optimal states for sensory signal detection (2015, background): “One possible circuit involved in arousal-associated changes in cortical responsiveness is the cholinergic activation of inhibitory interneurons in layer 1, whose activity inhibits the activity of other classes of interneurons in layers 2/3 (Fu et al., 2014; Lee et al., 2013; Pi et al., 2013).”
A cortical circuit for gain control by behavioral state (2014, background): “It has recently been shown that VIP neurons also inhibit SST neurons in prefrontal and auditory cortices and that activating VIP neurons increases auditory responses (Pi et al., 2013).”
Structured Connectivity in Cerebellar Inhibitory Networks (2014, background): “Recently, the interaction between the different types of cortical interneurons and its functional implications have attracted interest (Jiang et al., 2013; Letzkus et al., 2011; Pi et al., 2013).”
Neural Elements for Predictive Coding (2016, background): “Whereas PV and SST cells contact both pyramidal cells and interneurons, the third class solely contacts other interneurons (i.e., PV and SST cells) (Pi et al., 2013), immediately excluding it from consideration for the role described above.”
Waking State: Rapid Variations Modulate Neural and Behavioral Responses (2015, positive): “Neural Control of Waking State—Local Circuit Mechanisms Several recent studies, in somatosensory, auditory, and visual cortical areas, have revealed a disinhibitory pathway, the activation of which can increase the level of excitability of cortical pyramidal cells to sensory stimuli (Fu et al., 2014”
Principles of connectivity among morphologically defined cell types in adult neocortex (2015, positive): “Connectivity patterns of three molecularly identified interneuronal types (PV + , SOM + , and VIP + ) in the developing neocortex have been recently revealed by optogenetic studies (28– 30).”