Associatively Learned Representations of Taste Outcomes Activate Taste-Encoding Neural Ensembles in Gustatory Cortex

Abstract

Through learning processes, cues associated with emotionally salient reinforcing outcomes can come to act as substitutes for the reinforcer itself. According to one account of this phenomenon, the predictive cue associatively elicits a representation of the expected outcome by reactivating cells responsible for encoding features of the primary reinforcer. We tested this hypothesis by examining the role of neural ensembles in gustatory cortex (GC) during receipt of gustatory stimuli (sucrose and water) and cues associated with those stimuli using the immediate early genes (IEGs) Arc and Homer1a. Because these plasticity-related IEGs are expressed in the neuronal nucleus 5 and 30 min, respectively, after salient events, we examined how individual neurons encoded these stimuli in two separate behavioral epochs. In experiment 1, we showed that tasting identical sucrose solutions, but not tasteless water, in the two epochs increased both IEG activity and the degree of overlap between neural ensembles in GC. In experiment 2, odor cues associated with sucrose, but not water, evoked potentiation of IEG activity in GC similar to sucrose itself. Surprisingly, lesions of the basolateral amygdala had minimal effects on associative encoding in GC. Finally, these associatively driven representations of sucrose appeared to be outcome specific, as neural ensembles that were activated by the sucrose-associated cue were also activated by sucrose itself. This degree of overlap between associative and primary taste activity at the ensemble level suggests that GC neurons encode important information about anticipated outcomes. Such representations may provide outcome-specific information for guiding goal-directed behavior.

Familiar taste induces higher dendritic levels of activity-regulated cytoskeleton-associated protein in the insular cortex than a novel one

“…Sparse, discrete units were detected, sometimes with dendritic immunoreactivity (data not shown). Cell counting analysis on saccharin-drinking animals revealed that on average, 22.28% of neurons were found to be Arc+ after novel (N) taste (263 + 44 neurons/animal, n ¼ 5) and 20.67% after familiar (F5) taste (288 + 38 neurons/animal, n ¼ 5), both figures being very similar to what has been reported in other studies on taste learning that evaluated Arc mRNA levels (Barot et al 2008;Saddoris et al 2009). When comparing the percentage of neurons expressing Arc protein in both conditions, no difference was detected between N and F5 (t (8) ¼ 0.96, P ¼ 0.37), indicating that the same proportion of neurons were activated in the IC by a familiar and a novel taste stimulus (Fig.…”

“…Also, in vivo intrinsic imaging experiments showed that the anterior part of the IC responded best to taste modalities (Accolla et al 2007). Further, a more recent study using neuronal activity mapping with Arc mRNA (Saddoris et al 2009) indicates that the integration of taste-related information mostly occurs in the anterior dysgranular region of the IC. Finally, based on early electrophysiological evidence (Yamamoto et al 1989), as well as in preliminary findings from our lab with Arc immunohistochemistry, we determined that layers IV/V best responded to taste stimulation.…”

Central role for the insular cortex in mediating conditioned responses to anticipatory cues

“…Recent studies using rats have shown that neurons in the IC can change their firing in response to auditory cues anticipating the availability of taste (26,29,30). To determine whether IC activity could also be modulated by anticipatory cues in the present experimental conditions, we implanted 14 mice with movable bundles of 8 or 16 electrodes.…”

The Origins and Organization of Vertebrate Pavlovian Conditioning

“…Indeed, food-paired CSs can activate the gustatory region of the insular cortex (GC) in both rodents (Dardou et al 2006(Dardou et al , 2007 and humans (Veldhuizen et al 2007;Small et al 2008). Importantly, these CSs activate the very same neuronal ensembles in the GC that were activated by the food US itself, providing a neural substrate of CS retrieval of a reward representation (Saddoris et al 2009). …”