Dynamic representation of taste-related decisions in the gustatory insular cortex of mice

Abstract

<jats:title>SUMMARY</jats:title><jats:p>Research over the past decade has established the gustatory insular cortex (GC) as a model for studying how primary sensory cortices integrate multiple sensory, affective and cognitive signals. This integration occurs through time varying patterns of neural activity. Selective silencing of GC activity during specific temporal windows provided evidence for GC’s role in mediating taste palatability and expectation. Recent results also suggest that this area may play a role in decision making. However, existing data are limited to GC involvement in controlling the timing of stereotyped, orofacial reactions to aversive tastants during consumption. Here we present electrophysiological, chemogenetic and optogenetic results demonstrating the key role of GC in the execution of a taste-guided, reward-directed decision making task. Mice were trained in a taste-based, two-alternative choice task, in which they had to associate tastants sampled from a central spout with different actions (i.e., licking either a left or a right spout). Stimulus sampling and action were separated by a delay period. Electrophysiological recordings of single units revealed chemosensory processing during the sampling period and the emergence of task-related, cognitive signals during the delay period. Chemogenetic silencing of GC impaired task performance. Optogenetic silencing of GC allowed us to tease apart the contribution of activity during the sampling and the delay periods. While silencing during the sampling period had no effect, silencing during the delay period significantly impacted behavioral performance, demonstrating the importance of the cognitive signals processed by GC during this temporal window in driving decision making.</jats:p><jats:p>Altogether, our data highlight a novel role of GC in controlling taste-guided, reward-directed choices and actions.</jats:p>

Parvalbumin interneuron inhibition onto anterior insula neurons projecting to the basolateral amygdala drives aversive taste memory retrieval

“…11 As recent findings elegantly demonstrate, optogenetic activation of aIC PV does not affect chemosensation itself but can disrupt cognitive signals that drive the execution of tasteguided, reward-directed decision making. 48 Thus, activation of aIC PV during CTA retrieval likely represents a memorydependent halt in taste-guided drives toward the CS through the fine-tuning of synaptic activity on aIC-BLA-projecting neurons.…”

Behavioral Approaches to Study Top-Down Influences on Active Listening

“…Our approach to studying perceptual expectations in headfixed mice was inspired by previous human psychophysical studies (Wright and Fitzgerald, 2004;Best et al, 2007). While head-fixed mice can perform two-alternative forced choice tasks (Sanders and Kepecs, 2012;Burgess et al, 2017;Vincis et al, 2020), we used Go/No-Go task designs which could be learned over the course of one to two weeks, allowing us to layer manipulations of perceptual expectations on top of basic detection or discrimination tasks (Guo et al, 2014;McGinley et al, 2015;Kuchibhotla et al, 2017). As appetitive Go/No-Go behaviors typically result in a bias toward responding (Gomez et al, 2007), the role of baseline response bias and motivational structure introduced by our task designs likely played a role in the expectation-related effects we observed.…”

Primate anterior insular cortex represents economic decision variables postulated by Prospect theory

“…This fits with a recent primate neuroimaging study that showed strong activation of this entire region by visual cues indicating reward, as well as reward delivery 20 . Insula has long been known to be strongly connected with the neighboring gustatory cortex 34,35 . Recently, several lines of studies have demonstrated that neurons in the gustatory cortex not only engage the primary processing of gustatory inputs, but also involve multisensory integration 15,16 , as well as higher cognitive functions like decision-making 13,35 .…”

“…Insula has long been known to be strongly connected with the neighboring gustatory cortex 34,35 . Recently, several lines of studies have demonstrated that neurons in the gustatory cortex not only engage the primary processing of gustatory inputs, but also involve multisensory integration 15,16 , as well as higher cognitive functions like decision-making 13,35 . This suggests that primate insular cortex and the neighboring gustatory cortex are strongly interconnected and form an interacting distributed network during decision making.…”