Elsevier

Physiology & Behavior

Volume 86, Issue 5, 15 December 2005, Pages 717-730
Physiology & Behavior

Neural bases of food-seeking: Affect, arousal and reward in corticostriatolimbic circuits

https://doi.org/10.1016/j.physbeh.2005.08.061Get rights and content

Abstract

Recent studies suggest that there are multiple ‘reward’ or ‘reward-like’ systems that control food seeking; evidence points to two distinct learning processes and four modulatory processes that contribute to the performance of food-related instrumental actions. The learning processes subserve the acquisition of goal-directed and habitual actions and involve the dorsomedial and dorsolateral striatum, respectively. Access to food can function both to reinforce habits and as a reward or goal for actions. Encoding and retrieving the value of a goal appears to be mediated by distinct processes that, contrary to the somatic marker hypothesis, do not appear to depend on a common mechanism but on emotional and more abstract evaluative processes, respectively. The anticipation of reward on the basis of environmental events exerts a further modulatory influence on food seeking that can be dissociated from that of reward itself; earning a reward and anticipating a reward appear to be distinct processes and have been doubly dissociated at the level of the nucleus accumbens. Furthermore, the excitatory influence of reward-related cues can be both quite specific, based on the identity of the reward anticipated, or more general based on its motivational significance. The influence of these two processes on instrumental actions has also been doubly dissociated at the level of the amygdala. Although the complexity of food seeking provides a hurdle for the treatment of eating disorders, the suggestion that these apparently disparate determinants are functionally integrated within larger neural systems may provide novel approaches to these problems.

Introduction

There has been a recent trend towards identifying the processes involved in obesity with those associated with addictive behavior generally and with drug addiction in particular. For example, in a recent series of papers, Volkow and colleagues have established that binding at the dopamine D2 receptor in obese subjects, i.e., those with a body mass index over 30, is reduced in similar fashion to that of individuals addicted to drugs of abuse [119], [120], [121], [122]. A feature of these, and similar [24], accounts is that, often in the interests of a simple story, they focus on one factor, brain dopamine, as the causal factor, not just in pathological food intake but in its sequelae, notably in food seeking or pursuit. The operation of the reward system is commonly argued to link intake and pursuit and, indeed, since the discovery of self-stimulation, students of neuroscience have felt strongly predisposed to the view that there is a central reward system in the brain, that it is monolithic and that it involves midbrain dopaminergic neurons and particularly their projection via the medial forebrain bundle to limbic structures in the ventral forebrain [61], [87], [137].

It has appeared, therefore, to be a reasonable leap to propose that pathologies of brain dopamine are associated, more or less directly, with pathologies of the ‘reward system’ and so with pathological food seeking [44]. Indeed, evidence that, in addition to reduced D2 receptor binding, drug addicts have increased genetic variation associated with the D2 receptor has raised the specter of a ‘reward gene’ [25], [26]. Of course, it is equally possible that this evidence points to a corollary of addiction rather than its efficient cause. But these issues aside, the real problem with this approach is that it over-simplifies our understanding of the complex nature of the processes that contribute to both normal and abnormal food seeking. A number of recent papers have, as a consequence, unnecessarily conflated the processes that contribute to the compulsive pursuit of food with those that control goal-directed actions [63], [66], [85] and still further with those that control responses elicited by stimuli associated with food [74]. Although the operation of these processes objectively affects the rate of food seeking, recent evidence suggests that they each have distinct determinants. This review will attempt to tease these various influences apart with reference to recent research that has identified not one but potentially five ‘reward’ or ‘reward-related’ processes in the brain; that is to say, five systems that function to influence food seeking either directly, through learning, or indirectly, by modifying performance.

Section snippets

Reward and reinforcement

The recent literature concerning drug seeking in addicts has focused attention on the compulsive or habitual nature of these responses revealed particularly in their persistence, even in the face of sometimes quite extreme negative consequences, and their sensitivity to drug-related cues, an observation that has informed various theories of relapse [29], [54], [95], [107]. Many of the ideas that have been expressed in these recent papers have their root in now classical theories of habit

Behavioral considerations

Instrumental conditioning in rodents provides a very accurate model of goal-directed action in humans. Not only are rodent actions sensitive to changes in the value of the goal or outcome with which they are associated but they are also highly sensitive to changes in their causal consequences; rats will stop responding if performance no longer delivers the instrumental outcome and will stop responding even faster if their responding cancels an otherwise freely available food [45], [53]. Hammond

Reward and desire: instrumental incentives

The foregoing discussion suggests that, in instrumental conditioning, animals encode the relationship between specific actions and outcomes and are sensitive to the contingent relation between an action and goal delivery. It has long been recognized, however, that the encoding of an action–outcome association is not sufficient to determine the performance of an action. Any learning that takes the form ‘action A leads to outcome O′ can be used both to perform A and to avoid performing A. What is

Affect and arousal: Pavlovian incentives

Perhaps the most potent factor affecting addictive behavior and the one most often cited as the cause of failures to adjust to treatment is the effect that cues associated with drug delivery have on drug seeking or, in the current context, the effect that cues associated with access to specific foods have on food seeking. In fact, the idea that a stimulus associated with a positive reinforcer or reward exerts a motivational effect on behavior originates with an early study by Estes [58]. He

Dissociating instrumental and Pavlovian incentive processes

Evidence from PIT provides, perhaps, the strongest support for the claim that Pavlovian and instrumental conditioning share a common reward mechanism, making plausible the general claim that it is largely Pavlovian CS's embedded in the instrumental situation that provide the motivational support for instrumental performance. Indeed, from this perspective one may go so far as to claim that it is the effect of outcome devaluation on the motivational impact of Pavlovian cues rather than on the

Conclusion

As it stands, therefore, there is evidence of at least five distinct reward or reward-related processes that contribute to food seeking in rats. The distinct circuitry contributing to the acquisition of goal-directed and habitual actions and the dissociable effects of lesions within these circuits, notably within the dorsolateral and dorsomedial striatum, provides the basis for distinguishing the effects of the reinforcing and the rewarding functions of instrumental outcomes. The latter reward

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    The preparation of this manuscript was supported by NIMH grant #56446.

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