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Dopaminergic enhancement of local food-seeking is under global homeostatic control.

ABSTRACT: Recent work has implicated dopaminergic mechanisms in overeating and obesity with some researchers suggesting parallels between the dopamine dysregulation associated with addiction and an analogous dysregulation in obesity. The precise role of dopamine in mediating reward and reinforcement, however, remains controversial. In contrast to drugs of abuse, pursuit of a natural reward, such as food, is regulated by homeostatic processes that putatively maintain a stable energy balance keeping unrestrained consumption and reward pursuit in check. Understanding how the reward system is constrained by or escapes homeostatic regulation is a critical question. The widespread use of food restriction to motivate animal subjects in behavior paradigms precludes investigation of this relationship as the homeostatic system is locked into deficit mode. In the present study, we examined the role of dopamine in modulating adaptive feeding behavior in semi-naturalistic homecage paradigms where mice earn all of their food from lever pressing. We compared consumption and meal patterning between hyperdopaminergic dopamine transporter knock-down and wild-type mice in two paradigms that introduce escalating costs for procuring food. We found that hyperdopaminergic mice exhibited similar demand elasticity, weight loss and energy balance in response to cost. However, the dopamine transporter knock-down mice showed clear differences in meal patterning. Consistent with expectations of enhanced motivation, elevated dopamine increased the meal size and reduced intrameal cost sensitivity. Nonetheless, this did not alter the overall energy balance. We conclude that elevated dopamine enhances the incentive or willingness to work locally within meals without shifting the energy balance, enhancing global food-seeking or generating an energy surplus.

SUBMITTER: Beeler JA

PROVIDER: S-EPMC3251719 | biostudies-literature | 2012 Jan

REPOSITORIES: biostudies-literature

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Dopaminergic enhancement of local food-seeking is under global homeostatic control.

Beeler Jeff A JA Frazier Cristianne R M CR Zhuang Xiaoxi X

The European journal of neuroscience 20111127 1

Recent work has implicated dopaminergic mechanisms in overeating and obesity with some researchers suggesting parallels between the dopamine dysregulation associated with addiction and an analogous dysregulation in obesity. The precise role of dopamine in mediating reward and reinforcement, however, remains controversial. In contrast to drugs of abuse, pursuit of a natural reward, such as food, is regulated by homeostatic processes that putatively maintain a stable energy balance keeping unrestr ...[more]

PMID: 22118191

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Project description:RATIONALE:Excessive intake of rewards, such as food and drugs, often has explicit negative consequences, including the development of obesity and addiction, respectively. Thus, choosing not to pursue reward is the result of a cost/benefit decision, proper execution of which requires inhibition of behavior. An extensive body of preclinical and clinical evidence implicates dopamine in certain forms of inhibition of behavior, but it is not fully known how it contributes to behavioral inhibition under threat of explicit punishment. OBJECTIVES:To assess the involvement of midbrain dopamine neurons and their corticostriatal output regions, the ventral striatum and prefrontal cortex, in control over behavior under threat of explicit (foot shock) punishment in rats. METHODS:We used a recently developed behavioral inhibition task, which assesses the ability of rats to exert behavioral restraint at the mere sight of food reward, under threat of foot shock punishment. Using in vivo fiber photometry, chemogenetics, c-Fos immunohistochemistry, and behavioral pharmacology, we investigated how dopamine neurons in the ventral tegmental area, as well as its output areas, the ventral striatum and prefrontal cortex, contribute to behavior in this task. RESULTS:Using this multidisciplinary approach, we found little evidence for a direct involvement of ascending midbrain dopamine neurons in inhibitory control over behavior under threat of punishment. For example, photometry recordings suggested that VTA DA neurons do not directly govern control over behavior in the task, as no differences were observed in neuronal population activity during successful versus unsuccessful behavioral control. In addition, chemogenetic and pharmacological manipulations of the mesocorticolimbic DA system had little or no effect on the animals' ability to exert inhibitory control over behavior. Rather, the dopamine system appeared to have a role in the motivational components of reward pursuit. CONCLUSIONS:Together, our data provide insight into the mesocorticolimbic mechanisms behind motivated behaviors by showing a modulatory role of dopamine in the expression of cost/benefit decisions. In contrast to our expectations, dopamine did not appear to directly mediate the type of behavioral control that is tested in our task.

Dataset Information

Dopaminergic enhancement of local food-seeking is under global homeostatic control.

Publications

Dopaminergic enhancement of local food-seeking is under global homeostatic control.

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