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The nucleus accumbens as part of a basal ganglia action selection circuit

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Abstract

Background

The nucleus accumbens is the ventral extent of the striatum, the main input nucleus of the basal ganglia. Recent hypotheses propose that the accumbens and its dopamine projection from the midbrain contribute to appetitive behaviors required to obtain reward. However, the specific nature of this contribution is unclear. In contrast, significant advances have been made in understanding the role of the dorsal striatum in action selection and decision making.

Objective

In order to develop a hypothesis of the role of nucleus accumbens dopamine in action selection, the physiology and behavioral pharmacology of the nucleus accumbens are compared to those of the dorsal striatum.

Hypotheses

Three hypotheses concerning the role of dopamine in these structures are proposed: (1) that dopamine release in the dorsal striatum serves to facilitate the ability to respond appropriately to temporally predictable stimuli (that is, stimuli that are so predictable that animals engage in anticipatory behavior just prior to the stimulus); (2) that dopamine in the nucleus accumbens facilitates the ability to respond to temporally unpredictable stimuli (which require interruption of ongoing behavior); and (3) that accumbens neurons participate in action selection in response to such stimuli by virtue of their direct (monosynaptic inhibitory) and indirect (polysynaptic excitatory) projections to basal ganglia output nuclei.

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Notes

  1. If NAc dopamine is necessary to respond to stimuli presented at long intervals, it would seem that not just the drinking that occurs after intermittent food presentation but also the locomotion towards the food itself should be disrupted by NAc 6-OHDA lesions. In fact, exactly this effect has been shown, but unlike the long-lasting effects on SIP, the reduction in food-pellet-evoked locomotion recovered within a few days after the lesion (McCullough and Salamone 1992). This result highlights the fact that recovery of function is often observed after 6-OHDA lesions, which may be due to two effects: the animal relearns the task using circuits unaffected by the lesion, or supersensitivity of dopamine receptors develops and allows the affected circuit to function nearly normally if some dopamine terminals are spared by the lesion. Therefore, one possibility is that SIP and pellet-induced locomotion are differentially sensitive to reduction of NAc dopamine function. This could be tested by microinjecting dopamine receptor antagonists into the NAc to determine whether locomotion in response to intermittent food presentation is inhibited at higher doses than those required to inhibit SIP.

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Acknowledgements

This work was supported by funds provided by the State of California for medical research on alcohol and substance abuse through the University of California, San Francisco, and by National Institute of Health grant DA019473. The author is grateful to Drs. F. Ambroggi, C. Boettiger, L. Corbit, P. Dayan, H. Fields, G. Hjelmstad, F.W. Hopf, P. Janak, Y. Niv, P. Redgrave, S. Taha, and R. Turner for comments on the manuscript.

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Nicola, S.M. The nucleus accumbens as part of a basal ganglia action selection circuit. Psychopharmacology 191, 521–550 (2007). https://doi.org/10.1007/s00213-006-0510-4

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