Movement and VIP interneuron activation differentially modulate encoding in mouse auditory cortex

Abstract

Information processing in sensory cortex is highly sensitive to non-sensory variables such as anesthetic state, arousal, and task engagement. Recent work in mouse visual cortex (VCtx) suggests that evoked firing rates, stimulus-response mutual information, and encoding efficiency increase when animals are engaged in movement. A disinhibitory circuit appears central this change: inhibitory neurons expressing vasoactive intestinal peptide (VIP) are activated during movement, and disinhibit pyramidal cells by suppressing other inhibitory interneurons. Paradoxically, although movement activates a similar disinhibitory circuit in auditory cortex (ACtx), most ACtx studies report reduced spiking during movement. It is unclear whether the resulting changes in spike rates result in corresponding changes in stimulus-response mutual information. We examined ACtx responses evoked by tone cloud stimuli, in awake mice of both sexes, during spontaneous movement and still conditions. VIP+ cells were optogenetically activated on half of trials, permitting independent analysis of the consequences of movement and VIP activation, as well as their intersection. Movement decreased stimulus-related spike rates as well as mutual information and encoding efficiency. VIP interneuron activation tended to increase stimulus-evoked spike rates but not stimulus-response mutual information, thus reducing encoding efficiency. The intersection of movement and VIP activation was largely consistent with a linear combination of these main effects: VIP activation recovered movement-induced reduction in spike rates, but not information transfer.

Significance Statement The ability of the brain to represent information about the sensory environment is heavily influenced by the behavioral state of the animal. In visual cortex, it is well known that locomotor activity enhances visual stimulus processing. By contrast, the present study found that sound processing in auditory cortex is degraded during locomotor activity. Whereas enhanced stimulus processing in visual cortex is thought to depend on VIP+ interneuron activation, optogenetic activation of VIP+ interneurons in auditory cortex failed to improve stimulus processing. These findings imply that circuitry activated during movement has opposite influences on stimulus processing in visual and auditory cortices. Such differences could reflect a resource allocation shift during movement favoring spatial perception in service of the animal’s navigational needs.