Elsevier

Physiology & Behavior

Volume 89, Issue 4, 30 November 2006, Pages 531-535
Physiology & Behavior

Gustatory reward and the nucleus accumbens

https://doi.org/10.1016/j.physbeh.2006.05.024Get rights and content

Abstract

The concept of reward is central to psychology, but remains a cipher for neuroscience. Considerable evidence implicates dopamine in the process of reward and much of the data derives from the nucleus accumbens. Gustatory stimuli are widely used for animal studies of reward, but the connections between the taste and reward systems are unknown. In a series of experiments, our laboratory has addressed this issue using functional neurochemistry and neuroanatomy. First, using microdialysis probes, we demonstrated that sapid sucrose releases dopamine in the nucleus accumbens. The effect is dependent on oral stimulation and concentration. We subsequently determined that this response was independent of the thalamocortical gustatory system, but substantially blunted by damage to the parabrachial limbic taste projection. Further experiments using c-fos histochemistry confirmed that the limbic pathway was the prime carrier for the gustatory afferent activity that drives accumbens dopamine release.

Section snippets

The problem of reward

Reward is a psychological construct still in search of neural mechanisms. The problems associated with this pursuit arise because the construct itself has several definitions. Natural rewards are produced by sensory stimuli but they are not synonymous with them. Physiological conditions and experience influence, even reverse, the reward value of stimuli. Non-natural rewards are produced by drugs and electrical stimulation acting directly on the brain. This provides strong evidence that reward

Taste as reward

The research reviewed here attempts to reduce this remoteness by tracing a well characterized sensory system, taste, to the neurons of the nucleus accumbens whose activity appears to track reward value. The first task was to determine if a normally rewarding gustatory signal, sucrose, released DA in the accumbens. Mark et al. [21] demonstrated that saccharin intake increased dopamine flux in the NAc. More importantly, when they rendered the saccharin aversive by associating it with a toxin,

The central gustatory system

In order for the forebrain to participate in assigning hedonic value to afferent activity, the sensory systems involved must interact with the neural mechanisms that elaborate reward and aversion. This interaction might occur in forebrain reward areas, such as the mesolimbic dopamine system, or in the sensory nuclei themselves. For taste, there is evidence for both, but only the former is addressed here in any detail. The first central synapse for the gustatory system is in the rostral half of

The logic of taste reward

In the present context, the bifurcated central taste projection provides two potential routes by which gustatory afferent activity could interact with central reward systems. Our research has focused on which of these routes supports the release of dopamine from nucleus accumbens when rats are licking sucrose. We chose this index because the evidence reviewed above indicates that NAc dopamine tracts the reward value of substances that taste sweet to humans. To test the route of afferent

Discussion

Taken with the dialysis data, these results add weight to the inference that the sensory activity produced by sapid sucrose reaches the nucleus accumbens via the parabrachial limbic projections rather than the thalamocortical route. The fact that all the rats were sham feeding confirms that the differential activation elicited by sucrose was due to oral sensory stimulation. The group with lateral, visceral afferent PBN lesions, which had little if any effect on c-fos labeling, adds emphasis to

Acknowledgments

This paper is based on a presentation at a workshop on Peripheral–Central Interactions in the Control of Food Intake and Energy Balance held at the Centro Stefano Franscini in Ascona, Switzerland in August 2005. The authors' research was supported by grants DC00240, DC05435 and DK065709.

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