Cortical inhibitory interneurons control sensory processing

Abstract

Inhibitory and excitatory neurons form intricate interconnected circuits in the mammalian sensory cortex. Whereas the function of excitatory neurons is largely to integrate and transmit information within and between brain areas, inhibitory neurons are thought to shape the way excitatory neurons integrate information, and they exhibit context-specific and behavior-specific responses. Over the last few years, work across sensory modalities has begun unraveling the function of distinct types of cortical inhibitory neurons in sensory processing, identifying their contribution to controlling stimulus selectivity of excitatory neurons and modulating information processing based on the behavioral state of the subject. Here, we review results from recent studies and discuss the implications for the contribution of inhibition to cortical circuit activity and information processing.

Figure 1

Sensory tuning of neurons in the cortex (example: frequency tuning in the auditory cortex) is shaped by the interactions of excitatory (Exc) inputs (blue), and inhibitory (Inh) inputs (red) from several neuronal cell types, including PVs and SOMs, which themselves exhibit stimulus selectivity. A. Suppression (green) or activation (cyan) of inhibitory interneurons selectively (top right) or uniformly (bottom right) modulates responses of inhibitory neurons, which control frequency selectivity and signal-to-noise ratio of responses of excitatory neurons. Modulation of selective inhibition can affect tuning width, whereas broad inhibition modulation can affect signal-to-noise ratio. Both of these effects can change the sensitivity of neuronal populations to stimuli. S: signal, N: noise; W: tuning width; SNR: signal-to-noise ratio. B. Example neuron showing increasing levels of PV activation in visual cortex decreases firing rate and orientation tuning width in putative excitatory cells. [Adapted from 38]. C. Example neuron showing increasing levels of SOM activation in visual cortex decreases firing rate, but has no effect on orientation tuning width. Adapted from Lee et al., 2014. D. Example unit showing activation of VIP interneurons in visual cortex decreases orientation selectivity. Adapted from [Adapted from 46]. E. Example units showing activation of PV interneurons in auditory cortex has both multiplicative and linear effects on frequency selectivity. Adapted from [21]. F. Example units showing activation of SOM interneurons in auditory cortex has both multiplicative and linear effects on frequency selectivity [Adapted from 21]. G. Activation of VIP interneurons in auditory cortex causes an additive shift in frequency selectivity (n = 28). [Adapted from 14]. H. Inactivation of SOM interneurons in piriform cortex causes a subtractive shift in odor tuning (n = 29). [Adapted from 45].

Figure 2

PVs and SOMs inhibit excitatory neurons in sensory cortex (A) whereas VIPs in primary somatosensory cortex preferentially target SOMs. VIPs receive input directly from primary vibrissal motor cortex (vM1) during active and passive whisker movement thus decreasing SOM activity [C – 61]. During ongoing locomotion, auditory and visual cortex receives input from cholinergic neurons in the basal forebrain (BF) [B – 47] and auditory cortex receives input from secondary motor cortex (M2) which conveys information about motor planning. Cholinergic activity also conveys information about feedback signals during behavioural training [64] and preferentially target VIPs, VIPs thus respond to feedback signals [D – 14]. (A) Simplified circuit diagram of sensory cortex, solid circles indicate interneurons (VIP, SOM and PV) which target excitatory cells (Exc) and each other. Dashed circles indicate other brain areas which project to sensory cortex. (B) Activity in cholinergic axons in auditory cortex (purple shows a single example axon) correlates with small movements (licking, paw movements etc.) of the mouse (red). [Adapted from 47]. (C) SOM (yellow) spiking activity is decreased during passive and active whisker movement (green indicates angle of whisker, Vm = membrane potential). [Adapted from 61]. (D) VIP interneurons respond to behavioural feedback signals. They show shallow sustained response to water rewards in hit trials (cyan) and strong, sharp response to air puff or mild shock during in false alarm trials (magenta). [Adapted from 14].