Impact of precisely-timed inhibition of gustatory cortex on taste behavior depends on single-trial ensemble dynamics

Abstract

Sensation and action are necessarily coupled during stimulus perception – while tasting, for instance, perception happens while an animal decides to expel or swallow the substance in the mouth (the former via a behavior known as ‘gaping’). Taste responses in the rodent gustatory cortex (GC) span this sensorimotor divide, progressing through firing-rate epochs that culminate in the emergence of action-related firing. Population analyses reveal this emergence to be a sudden, coherent and variably-timed ensemble transition that reliably precedes gaping onset by 0.2–0.3s. Here, we tested whether this transition drives gaping, by delivering 0.5s GC perturbations in tasting trials. Perturbations significantly delayed gaping, but only when they preceded the action-related transition - thus, the same perturbation impacted behavior or not, depending on the transition latency in that particular trial. Our results suggest a distributed attractor network model of taste processing, and a dynamical role for cortex in driving motor behavior.

Perturbation of amygdala-cortical projections reduces ensemble coherence of palatability coding in gustatory cortex

“…In summary, 2.5-sec perturbations of BLA input to GC change taste-driven activity in ways that are both non-random and complex-firing is modulated in specific relation to the dynamics that characterize GC taste processing. Such results imply, consistent with previous work (Schoenbaum et al, 1998;Pare et al, 2002;Piette et al, 2012), that disruptions of the BLA→GC pathway might have distinct consequences for different functional aspects of GC taste responses (aspects that have been shown to "live" in the different response epochs; see Sadacca et al, 2016;Mukherjee et al, 2019); more speculatively, they imply that the dynamic nature of GC taste responses might itself be the product of interactions between the cortex and amygdala. Below, we test these two hypotheses.…”

“…This fact is perhaps somewhat surprising given the well-known importance of amygdala for emotion processing (e.g., Quirk et al, 1995;Schoenbaum et al, 1998;LeDoux, 2000;Wang et al, 2005;Wassum and Izquierdo, 2015;Beyeler et al, 2018), and findings suggesting that BLA-GC circuitry is vital for palatability-related behavior (CTA learning and taste neophobia; Gallo et al, 1992;Lin and Reilly, 2012;Levitan et al, 2020). Our recent data suggest a possible explanation, however: as previously discussed, the emergence of Late-epoch palatability coding is revealed, using single-trial analyses involving Hidden Markov Modeling (HMM), to be a sudden transition into a new ensemble state, in which firing-rate changes occur simultaneously in multiple GC neurons (Jones et al, 2007;Miller and Katz, 2010;Sadacca et al, 2016); it is this sudden transition itself that directly drives behavior (Mukherjee et al, 2019). Perhaps the true extent of the perturbation effect is best apprehended, not in terms of changes in the magnitudes of palatability coding, but in terms of the ensemble coherence and/or suddenness of the transition into palatability-related firing.…”

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

“…Recent evidence also suggests that GC can be involved in taste-based decision making [16, 33]. Recordings from GC of rats consuming tastants delivered through an intraoral cannula demonstrate that sudden and coherent changes in ensemble activity predict gapes – an innate orofacial behavior aimed at expelling aversive tastants [16]. Optogenetic experiments, showing that silencing GC prior to this transition in activity delays the onset of gapes, confirm the importance of this area in driving this ingestive decision.…”

“…The third epoch (palatability) begins about a second after stimulus delivery and relates to the processing of taste palatability. This coding scheme has been further refined through trial-by-trial ensemble analyses and has been extensively validated by experimental evidence in rats and mice [6, 7, 16, 29, 30]. Alas, one of the limitations of this model has been its exclusive reliance on experiments in which rodents consume tastants that are flushed directly into the oral cavity through a surgically implanted intraoral cannula.…”

“…GC has been implicated in multiple functions related to taste processing, taste learning and taste expectation [1, 9, 31, 32]. Recent evidence also suggests that GC can be involved in taste-based decision making [16, 33]. Recordings from GC of rats consuming tastants delivered through an intraoral cannula demonstrate that sudden and coherent changes in ensemble activity predict gapes – an innate orofacial behavior aimed at expelling aversive tastants [16].…”