Dynamic Representation of Taste-Related Decisions in the Gustatory Insular Cortex of Mice

Abstract

SUMMARY Research over the past decade has established the gustatory insular cortex (GC) as a model for studying howprimary sensory cortices integrate sensory,affective, and cognitive signals. This integration occurs through time-varyingpatterns of neural activity. Selective silencing of GC activity during specific temporal windows provided evidence forGC’s role in mediating taste palatability and expectation. Recent results also suggest that this areamay 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 GCin the executionof a taste-guided, reward-directed decision-making task. Mice were trained in a 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 revealed chemosensory processing during the sampling period and the emergence of task-related, cognitive signals during the delay period. Chemogenetic silencing of GCimpaired task performance. Optogenetic silencing of GC allowed us to tease apart the contribution of activity during sampling and delay periods. Although 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 in driving decision making. Altogether, our data highlight a novel role ofGCin controlling taste-guided, reward-directed choices and actions.

Prior cocaine exposure increases firing to immediate reward while attenuating cue and context signals related to reward value in anterior insula

“…Similar to recent work from the Fontanini group (Vincis et al, 2020), our study found that insula encoded predicted outcomes during the presentation of reward-predictive odor cues, and fired in anticipation of reward after completion of an instrumental response. Further, we showed that firing was higher for cues that predicted high-valued reward in both delay and size domains.…”

“…Traditionally, the insula has been described as an interoceptive center (Craig, 2010, 2002; Damasio et al, 2000; Naqvi and Bechara, 2010), but is also thought to contribute to functions related to reward processing and decision-making (Burke and Tobler, 2011; Droutman et al, 2015; Mesulam and Mufson, 1982; Ongur and Price, 2000; Preuschoff et al, 2008; Rogers-Carter and Christianson, 2019). Consistent with these functions, recent work has shown that firing in insula correlates to the anticipation and delivery of both positive and negative outcomes (Guillem et al, 2010; Jo and Jung, 2016; Kusumoto-Yoshida et al, 2015; Mizoguchi et al, 2015; Moschak et al, 2018; Samuelsen et al, 2012; Vincis et al, 2020; Wittmann et al, 2020). Here, we ask if outcome-related neural correlates in insula are disrupted by chronic cocaine-self administration in rats performing a reward-guided decision-making task.…”

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 decisionmaking 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 decisionmaking 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.…”

Spatially distributed representation of taste quality in the gustatory insular cortex of awake behaving mice

“…A subset of the non-responsive neurons may be involved in encoding this information and participate in the perception of flavor [32,33] and the formation of associative representations triggered by anticipatory cues [20,21,26]. Moreover, GC neurons have been shown to encode cognitive variables associated with decision making [27,34].…”