Abstract
Reward associations during auditory learning induce cortical plasticity in the primary auditory cortex. A prominent source of such influence is the ventral tegmental area (VTA), which conveys a dopaminergic teaching signal to the primary auditory cortex. Yet, it is unknown, how the VTA influences cortical frequency processing and spectral integration. Therefore, we investigated the temporal effects of direct optogenetic stimulation of the VTA onto spectral integration in the auditory cortex on a synaptic circuit level by current-source-density analysis in anesthetized Mongolian gerbils. While auditory lemniscal input predominantly terminates in the granular input layers III/IV, we found that VTA-mediated modulation of spectral processing is relayed by a different circuit, namely enhanced thalamic inputs to the infragranular layers Vb/VIa. Activation of this circuit yields a frequency-specific gain amplification of local sensory input and enhances corticocortical information transfer, especially in supragranular layers I/II. This effects persisted over more than 30 minutes after VTA stimulation. Altogether, we demonstrate that the VTA exhibits a long-lasting influence on sensory cortical processing via infragranular layers transcending the signaling of a mere reward-prediction error. We thereby demonstrate a cellular and circuit substrate for the influence of reinforcement-evaluating brain systems on sensory processing in the auditory cortex.
Highlights
The sensory cortex receives both bottom-up input relaying stimulus information from the sensory epithelia and top-down input from, for example, reinforcement-evaluating brain structures[1]
Activity in layer VIb showed a prominent increase during ventral tegmental area (VTA) stimulation selectively for the non-best frequency (BF) bin (Fig. 3; bottom right), and, in accordance, we found slopes to be significantly decreased during laser stimulation, which recovered after 30 minutes
The VTA is a key structure to convey information about stimulus salience and value to target areas distributed throughout the brain in the awake individual[2]
Summary
The sensory cortex receives both bottom-up input relaying stimulus information from the sensory epithelia and top-down input from, for example, reinforcement-evaluating brain structures[1]. Among the latter, the ventral tegmental area (VTA) is a key structure associated with the coding of reward, reward prediction, and reward prediction error[2]. In order to determine the contribution of VTA projections to these cortical effects of dopamine, we optogenetically stimulated the projection neurons of the VTA in adult male Mongolian gerbils (Meriones unguiculatus) and measured the layer-specific processing in the auditory cortex by tone-evoked current-source density (CSD) analysis. Reward-modulated sensory input in deep layer neurons might provide a cellular substrate for integrating sensory and task-related information in the service of sensory-based decision-making and reinforcement learning
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