Forebrain taste information processing is accomplished mainly by three reciprocally connected forebrain regions -primary gustatory cortex (GC), (basolateral) amygdala (AM), and orbitofrontal cortex (OFC)- loosely characterized as the neural sources of sensory, palatability-related, and cognitive information, respectively. It has been proposed that the perception of complex taste stimuli involves an intricate flow of information between these regions in real time. However, empirical confirmation of this hypothesis and a detailed analysis of the multidirectional flow of information during taste perception have not yet been presented before. We have simultaneously recorded local field potentials from GC, AM, and OFC in awake behaving rats under two conditions as controlled aliquots of either preferred or not preferred taste stimuli were placed directly on their tongues via intra-oral cannulae. Half of the deliveries were active, as the rat pressed a bar to receive the taste upon receiving an auditory ‘go’ signal, the other half of deliveries were passive when the rat received a tastant at random times. Peri-delivery signals from the three areas were analyzed by computing transfer entropy, a method that measures directional information transfer between coupled dynamic systems by assessing the reduction of uncertainty in predicting the current state of the systems based on their previous states. The results of this analysis reveal the complexity and context specificity of perceptual neural taste processing. Passive taste deliveries caused an immediate and strong flow of information that ascended from GC to both AM and OFC (p<0.001). However, within the 1.5-2.0 sec in which our rats typically identified and acted on (swallowing or expelling) the tastes, feedback from AM to GC became a prominent feature of the field potential activity (p<0.001). This finding confirms and extends earlier single cell results showing that palatability-related information appears in AM single- neuron responses soon after taste delivery, and that there is a sudden shift in the content of both GC and AM single-neuron responses at ~1.0 sec following delivery, as palatability-related information appears in GC and subsides in AM. The neural response to active taste deliveries differed from that to passive deliveries in important ways. The massive immediate GC to AM/OFC flow was greatly decreased and delayed. Instead, there was an increased and lasting information flow from OFC to GC (p<0.01) immediately after the tone. The likely reason for this reduction was obvious: tone onset led to an anticipation of taste delivery that activated a descending flow of information from the cognitive centers in OFC to the primary sensory cortex, which greatly changed the actual neural processing of the stimulus itself in GC. These results place earlier single-neuron findings into a functional dynamic framework, and offer an explanation of how the parts of the sensory system work together to give rise to complex perception. They suggest that perception is not a simple bottom-up process in which a stimulus is coded by progressively higher centers of the brain, rather various bottom-up and top-down effects jointly define and greatly alter stimulus processing as early as in the primary sensory areas. In agreement with our predictions, we found that the distribution of speech- evoked activity is consistently more similar to spontaneous activity than the distribution of noise-evoked activity, for both the instantaneous distribution of activity and for transition probability. These results provide new evidence for stimulus specific adaptation in the cortex that leads to preference for natural stimuli, and also provide additional support for the sampling hypothesis. Our findings in A1 complement our earlier data from V1, suggesting that the match between spontaneous and evoked activity might be a universal hallmark of representation and computation in sensory cortex.

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