Abstract

The nucleus accumbens core (NAcc) has been implicated in learning associations between sensory cues and profitable motor responses. However, the precise mechanisms that underlie these functions remain unclear. We recorded single-neuron activity from the NAcc of primates trained to perform a visual-motor associative learning task. During learning, we found two distinct classes of NAcc neurons. The first class demonstrated progressive increases in firing rates at the go-cue, feedback/tone and reward epochs of the task, as novel associations were learned. This suggests that these neurons may play a role in the exploitation of rewarding behaviors. In contrast, the second class exhibited attenuated firing rates, but only at the reward epoch of the task. These findings suggest that some NAcc neurons play a role in reward-based reinforcement during learning.

Highlights

  • The process of associative learning, whereby the brain links sensory stimuli with specific motor behaviors and expected rewards, is fundamental to adaptation and survival

  • The second class exhibited attenuated firing rates, but only at the reward epoch of the task. These findings suggest that some nucleus accumbens core (NAcc) neurons play a role in reward-based reinforcement during learning

  • Evidence suggests that a critical portion of this process is encoded in the nucleus accumbens core (NAcc) and is in part mediated through the actions of the neurotransmitter dopamine (Schultz, 1998, 2000; Ikemoto and Panksepp, 1999; Bar-Gad et al, 2003; Wise, 2004; Graybiel, 2005; Frank and O’Reilly, 2006; Daniel and Pollmann, 2010) the precise role of dopamine in this process is a source of considerable debate (Salamone et al, 2005)

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Summary

Introduction

The process of associative learning, whereby the brain links sensory stimuli with specific motor behaviors and expected rewards, is fundamental to adaptation and survival. The NAcc receives glutamatergic inputs from orbitofrontal/prefrontal cortex, basolateral amygdala, and hippocampus (areas involved with stimulus properties, preferences, and memories), while dopaminergic input is received from ventral tegmental area neurons (Poletti and Creswell, 1977; Beckstead, 1979; Russchen et al, 1985; Selemon and Goldman-Rakic, 1985; Haber et al, 1990; Brog et al, 1993; Wright and Groenewegen, 1995; Fudge and Haber, 2002). NAcc outputs include projections to the ventral pallidum, the dorsomedial thalamus (which projects back to the orbitofrontal cortex), pedunculopontine tegmentum, and a significant projection to dopaminergic areas of the midbrain (Groenewegen and Russchen, 1984; Haber et al, 1990; Heimer et al, 1991; Nicola et al, 2000; Zahm, 2000; Wise, 2004). The NAcc is positioned to receive diverse information from brain regions believed to encode aspects of reward-related information, while its projections can modulate nuclei associated with generation of motor behaviors and dopamine release (Joel and Weiner, 2000; Sesack and Grace, 2010)

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