Behavioral modulation of gustatory cortical activity

Abstract

Our perception of the sensory world is constantly modulated by the environment surrounding us and by our psychological state; each encounter with the same stimulus can in fact evoke very different perceptions. This phenomenological richness correlates well with the plasticity and the state-dependency observed in neural responses to sensory stimuli. This article reviews recent results on how the processing of sensory inputs varies depending on the internal state of the animal. Specifically it focuses on the gustatory system and on data showing that levels of attention and expectation modulate taste processing and gustatory cortical activity in meaningful ways. Mounting experimental evidence suggesting that expectation-dependent changes in gustatory cortical activity result from changes in the coupling between the amygdala and the cortex will also be discussed. The results presented here begin to paint a complex picture of taste, which goes beyond the framework of classical coding theories.

Figure 1

Attention levels modulate gustatory processing: (A) Left panel: Patterns of local field potential activity observed in the gustatory cortex of rats during different phases of a tasting session. Each trace represents a 2 s long recording during a period characterized by fast, desynchronized activity (top) or during a period dominated by 7–12 Hz mu-like oscillations. Right panel: Correlation between mu-like activity in the early (first hour) and late part of the tasting session and reaction times to the stimulus presented directly in the mouth of the animal. Left y-axis (and light gray histograms): amount of time per s in which mu-like rhythms were observed. Right y-axis (and dark gray points superimposed on the histograms): Latency of the first purposeful orofacial movement following stimulus presentation. (B) Principal components analysis of neural activity showing how the “distance” between tastes in a hypothetical stimulus space changes depending on attention. Left panel: Distance (i.e., the dissimilarity) between quinine (Q and Q′) and sucrose (S and S′), tastes with opposing palatability, increases with inattention (the ′ denotes the position of the taste during inattention). Right panel: Distance between quinine (Q and Q′) and citric acid (CA and CA′) decreases once the animal becomes inattentive. The ′ denotes the taste during inattention. (C) Analysis of orofacial behaviors during attention and inattention showing independent evidence for a rearrangement of the taste space according to palatability. Left panel: Ratio between sucrose and quinine for the number of tongue protrusions evoked. The ratio increases during inattention, reflecting an increased dissimilarity between the two stimuli. In contrast, tastes with similar palatability (right panel) show more similar orofacial reactions as the animal becomes inattentive. The ratio between quinine and citric acid for number of gapes evoked decreases with inattention.