Putative γ‐aminobutyric acid neurons in the ventral tegmental area have a similar pattern of plasticity as dopamine neurons during appetitive and aversive learning

Abstract

Dopamine influences affective, motor and cognitive processing, and multiple forms of learning and memory. This multifaceted functionality, which operates across long temporal windows, is broader than the narrow and temporally constrained role often ascribed to dopamine neurons as reward prediction error detectors. Given the modulatory nature of dopamine neurotransmission, that dopamine release is activated by both aversive and appetitive stimuli, and that dopamine receptors are often localized extrasynaptically, a role for dopamine in transmitting precise error signals has been questioned. Here we recorded from ventral tegmental area (VTA) neurons, while exposing rats to novel stimuli that were predictive of an appetitive or aversive outcome in the same behavioral session. The VTA contains dopamine and -aminobutyric acid (GABA) neurons that project to striatal and cortical regions and are strongly implicated in learning and affective processing. The response of VTA neurons, regardless of whether they had putative dopamine or GABA waveforms, transformed flexibly as animals learned to associate novel stimuli from different sensory modalities to appetitive or aversive outcomes. Learning the appetitive association led to larger excitatory VTA responses, whereas acquiring the aversive association led to a biphasic response of brief excitation followed by sustained inhibition. These responses shifted rapidly as outcome contingencies changed. These data suggest that VTA neurons interface sensory information with representational memory of aversive and appetitive events. This pattern of plasticity was not selective for putative dopamine neurons and generalized to other cells, suggesting that the temporally precise information transfer from the VTA may be mediated by faster acting GABA neurons.