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The Responses of Ventral Tegmental Area Neurons to Appetitive and Aversive Conditioned Cues

Abstract

While the ventral tegmental area (VTA) and its dopamine (DA) projections have been implicated strongly in reward processing, and more tentatively in fear conditioning, the response time course of all of the many types of VTA neurons to rewards, aversive events, and cues predictive of such outcomes is still unclear. To this end, extracellular recordings of VTA neural activity were conducted during appetitive and aversive Pavlovian conditioning in awake, behaving rats. Two populations of VTA neurons were excited by a visual reward-predictive cue: a Congruent population excited by reward, as well as an Incongruent population inhibited by reward. The Congruent population displayed cue response characteristics often ascribed to presumed DA neurons, such as learning-related enhancement, extinction-related decrement, correlation with motivation, and a negative reward prediction error signal. The Incongruent population did not display these cue response characteristics, and may encode the sensory salience of the cue. In the Pavlovian fear conditioning procedure, phasic responses to visual and auditory cues predicting footshock delivery were found. The proportion of cue inhibitions, and the strength of cue excitations, encoded behaviorally expressed cue-elicited fear. Conditioned phasic responses to appetitive and aversive cues were very similar, and most cells excited by the fear-conditioned cue were excited during reward consumption. Taken together, our findings suggest that VTA neurons whose responses change with learning are not generally selective for the hedonic valence of events, but may instead reflect the motivational salience of both rewarding and aversive events.

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