Sensory Cortical Activity Is Related to the Selection of a Rhythmic Motor Action Pattern

Abstract

Rats produce robust, highly distinctive orofacial rhythms in response to taste stimuli-responses that aid in the consumption of palatable tastes and the ejection of aversive tastes, and that are sourced in a multifunctional brainstem central pattern generator. Several pieces of indirect evidence suggest that primary gustatory cortex (GC) may be a part of a distributed forebrain circuit involved in the selection of particular consumption-related rhythms, although not in the production of individual mouth movements per se. Here, we performed a series of tests of this hypothesis. We first examined the temporal relationship between GC activity and orofacial behaviors by performing paired single-neuron and electromyographic recordings in awake rats. Using a trial-by-trial analysis, we found that a subset of GC neurons shows a burst of activity beginning before the transition between nondistinct and taste-specific (i.e., consumption-related) orofacial rhythms. We further showed that shifting the latency of consumption-related behavior by selective cueing has an analogous impact on the timing of GC activity. Finally, we showed the complementary result, demonstrating that optogenetic perturbation of GC activity has a modest but significant impact on the probability that a specific rhythm will be produced in response to a strongly aversive taste. GC appears to be a part of a distributed circuit that governs the selection of taste-induced orofacial rhythms.

Single and population coding of taste in the gustatory-cortex of awake mice

“…As the sense with (arguably) the tightest link to behavior and learning (Carleton et al, 2010;Maffei et al, 2012;Katz & Sadacca, 2010), taste is a particularly good system with which to study these topics in a unified manner. Furthermore, this work can take advantage of the extensive progress that has been made toward understanding key principles of taste coding in awake rats (Accolla et al, 2007;Bahar et al, 2004;Fontanini and Katz., 2006;Jones et al, 2007;Katz et al, 2001;Li et al, 2016;Moran & Katz., 2014;Sadacca et al, 2012;Samuelsen et al, 2012). It is somewhat surprising, therefore, that there has been almost no electrophysiological work done on mouse cortical taste coding, and that the imaging studies performed thus far have failed to provide consensus on basic features of gustatory sensory coding (Chen et al, 2011;Fletcher et al, 2017).…”

“…"Time course of palatability-related responding." Taking a cue from our work on rats (e.g., Fontanini et al, 2009;Piette et al, 2012;Sadacca et al, 2012;Li et al, 2016;Sadacca et al, 2016), we used a moving-window analysis to identify the times at which GC taste responses reflected the hedonic value of the tastes. We first ranked the taste stimuli based on their palatability (see below); the ranking of palatability of tastes used herein is, from highest to lowest, sucrose, NaCl, citric acid and quinine.…”

“…But the prior work on rats further demonstrates that such analyses are inadequate to describe GC taste responses, in that they ignore meaningful response changes that occur across the first 1.5s of post-stimulus time (the period leading up to the making of consumption decisions and production of consumption-related behaviors, see Grill & Noregren, 1978;Travers and Norgren., 1986;Li et al, 2016). The complete range of the information carried in rat GC taste responses can be appreciated only when reliable, phasic modulations of firing rate-the temporal dimension of taste responses-are considered (Katz et al, 2001;Fontanini & Katz, 2006;Piette et al, 2012;Sadacca et al, 2012;Maier & Katz, 2013;Li et al, 2016;Baez-Santiago et al, 2016).…”

“…To evaluate the temporal evolution of these responses in relation to the sensory and psychological properties of taste perception, we first ascertained mouse behavioral preferences for our battery of four tastes (which differed in both chemical identity and palatability, sucrose and sodium-chloride representing palatable tastes and citric acid and quinine representing non-palatable tastes) using a single-bottle consumption test. We then correlated this vector of palatabilities with the vector of firing rates to the same battery of tastes in small bins of the 2-sec response epoch (using a moving-window analysis as explained in the Methods and used previously in Fontanini et al, 2009;Piette et al, 2012;Sadacca et al, 2012;Li et al, 2016;Sadacca et al, 2016). An example of the result of this analysis is shown in Figure 5A2 (with the taste preference data presented as an inset): for this single neuron, firing did not become significantly palatability-related (green dots) until several hundred msec after the onset of taste responsiveness, and reached a peak of palatability-relatedness a full sec after taste delivery; inspection of Figure 5A1 suggests that the responses were taste-specific prior to the emergence of palatabilityrelatedness, but that firing rates shifted between 0.5 and 1.0 sec into the response such that the order of response magnitudes came to reflect palatability (in this case the ordering was "aversive high," which appeared with approximately the same frequency in our neural sample as "aversive low").…”

“…In contrast, a good deal of coherent progress has been made toward characterizing primary gustatory cortical (GC) taste responses in awake rats, mainly (but not ubiquitously) using electrophysiology. This work has exposed reliable properties of taste spiking activity in relation to behavior, specifically revealing: 1) that single-neuron taste responses vary widely in breadth, with responses to multiple tastes appearing in the same region, and even within the same single neurons (Katz et al, 2001;Fontanini & Katz, 2006;Accolla et al, 2007;Samuelsen et al, 2013); 2) that these responses progress through a series of firing-rate "epochs," coding in turn the presence, physical properties, and palatability of a taste across 1-1.5s (Katz et al, 2001;Bahar et al, 2004;Sadacca et al, 2012;Maier & Katz, 2013;Samuelsen et al, 2013); 3) that the late-epoch palatabilityrelated firing is uniquely affected by experience-driven shifts of taste palatability (Bahar et al, 2004;Fontanini & Katz, 2006;Grossman et al, 2008;Moran and Katz., 2014); and 4) that in single trials the onset of palatability is a sudden, coherent network phenomenon, the timing of which predicts and impacts behavior (Jones et al, 2007;Sadacca et al, 2016;Li et al, 2016). A test of whether mouse GC neurons respond in a like manner has not yet been performed.…”