Abstract

The activation of the ventral tegmental area (VTA) can rebuild the tonotopic representation in the primary auditory cortex (A1), but the cellular mechanisms remain largely unknown. Here, we investigated the firing patterns and membrane potential dynamics of neurons in A1 under the influence of VTA activation using in vivo intracellular recording. We found that VTA activation can significantly reduce the variability of sound evoked responses and promote the firing precision and strength of A1 neurons. Furthermore, the compressed response window was caused by an early hyperpolarization as a result of enhanced circuit inhibition. Our study suggested a possible mechanism of how the reward system affects information processing in sensory cortex: VTA activation strengthens cortical inhibition, which shortens the response window of post-synaptic cortical neurons and further promotes the precision and strength of neuronal activity.

Highlights

  • There are numerous functional and anatomical connections between the sensory system and the reward system

  • ventral tegmental area (VTA) ACTIVATION COMPRESSED SPIKING ACTIVITY IN A1 NEURONS After the implantation of a stimulator in the VTA and the localization of A1, two groups of stimulation protocols were used to test the ability of VTA activation to modulate neuronal activity in A1: sound stimulation only and paired VTA-sound stimulation (Figures 1A–D, see Materials and Methods for details)

  • We found that the amplitude of sound evoked EPSPs and the latency of the first spiking response did not change significantly (sound only/paired VTA-sound: EPSP amplitudes 9.4 ± 2.6/9.8 ± 1.8 mV, p = 0.5; FIGURE 2 | Spiking response of A1 neurons was compressed by paired VTA-sound stimulation. (A) Example of an intracellular recording from a neuron in rat A1: top, sound only group; bottom, paired VTA-sound group; left, single trace of response; right, five superimposed traces

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Summary

Introduction

There are numerous functional and anatomical connections between the sensory system and the reward system. Dopaminergic reward signals selectively gate cortical plasticity (Arsenault et al, 2013) and visual learning is mediated by stimulus-reward pairing in the absence of attention (Seitz et al, 2009). During stimulus-reward associative learning, the auditory cortex shows rapid plasticity in the spectrotemporal receptive field (David et al, 2012). Dopaminergic modulation influences neural activity and induces learningdependent plasticity in the auditory cortex (Weis et al, 2012; Puschmann et al, 2013). These reports suggest that the dopaminergic reward system may play an important role in auditory processing

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