Analysis of taste processing in rat gustatory cortex

Abstract

Gustatory perception is a complex phenomenon involving the recognition of sensory properties of a food (taste modality and intensity, flavour, texture, fat content, temperature) as well as its reward value (pleasantness and nutritional value). The sense of taste lies at the core of this process and has the fundamental task of guiding the individual towards the decision on which substances to ingest and which others to reject. Remarkable progress has been made through molecular and genetic manipulations in the understanding of the coding of taste at the receptor level. However, much less is known about the cortical processing of taste sensation and the organizing principles of the gustatory cortex (GC). Functional maps are evident in many sensory regions of the neocortex, where neurons are arranged in spatially distinct networks to process sensory inputs. In contrast, in the GC, the existence of functional domains encoding different taste modalities has not been shown yet. In this thesis we used in vivo optical imaging techniques to investigate the functional architecture of the GC in regard to pure taste attributes (modality and intensity) and stimulus hedonic value (or pleasantness). In a first study we found that four of the primary taste modalities (sweet, bitter, salty and sour) are represented by distinctive spatial patterns, but that no region was specific to a single modality. In addition, we found that two tastants of similar hedonic value (pleasant or unpleasant) activated areas with more common regions than two tastants with opposite hedonic value. To better investigate the role of GC in representing the hedonic value, in a second study we coupled intrinsic imaging with conditioned taste aversion (CTA), a learning paradigm whereby a subject learns to avoid a taste stimulus previously associated with visceral malaise. We imaged intrinsic signals from the rat GC after inducing CTA to a pleasant stimulus (saccharin) and compared the resulting map to the response to a naturally unpleasant compound (quinine). Our results show that saccharin maps undergo plastic changes after CTA acquisition and after the extinction of the aversion, although this second change did not seem to reflect a simple reversal of the CTA acquisition. This result would be consistent with the evidence that extinction represents a new state of learning. Interestingly, this GC maps plasticity appears to be strongly correlated with the behavioral changes in the stimulus hedonic value. When saccharin shifts from attractive (Ctrl) to aversive (CTA acquisition) and attractive again (CTA extinction) its cortical representation changes in its relative position with respect to the pattern of the reference aversive stimulus, becoming highly correlated to the quinine pattern only after the CTA acquisition. In summary, we propose that the specific cortical patterns can be used to discriminate among various taste modalities, according to a spatial model of taste coding. We also show that GC maps reshape following conditioned learning induced by an internal state of malaise. Overall the present thesis provides new evidence for the GC as a site where multiple taste attributes are processed, including taste modality, intensity, aversive memory and hedonic value.