Abstract
Background and objectives
The idea that nucleus accumbens (Acb) dopamine transmission contributes to the neural mediation of reward, at least in a general sense, has achieved wide acceptance. Nevertheless, debate remains over the precise nature of dopamine’s role in reward and even over the nature of reward itself. In the present article, evidence is reviewed from studies of food intake, feeding microstructure, instrumental responding for food reinforcement, and dopamine efflux associated with feeding, which suggests that reward processing in the Acb is best understood as an interaction among distinct processes coded by discrete neurotransmitter systems.
Results
In agreement with several theories of Acb dopamine function, it is proposed here that allocation of motor effort in seeking food or food-associated conditioned stimuli can be dissociated from computations relevant to the hedonic evaluation of food during the consummatory act. The former appears to depend upon Acb dopamine transmission and the latter upon striatal opioid peptide release. Moreover, dopamine transmission may play a role in ‘stamping in’ associations between motor acts and goal attainment and perhaps also neural representations corresponding to rewarding outcomes. Finally, evidence is reviewed that amino acid transmission specifically in the Acb shell acts as a central ‘circuit breaker’ to flexibly enable or terminate the consummatory act, via descending connections to hypothalamic feeding control systems.
Conclusions
The heuristic framework outlined above may help explain why dopamine-compromising manipulations that strongly diminish instrumental goal-seeking behaviors leave consummatory activity relatively unaffected.
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Notes
For the purposes of this review, we will use the terms ‘appetitive’ and ‘consummatory’ to distinguish behaviors leading up to goal attainment from those that involve actual commerce with the goal object (Craig 1918). Unless otherwise specified, the term ‘appetitive phase’ is meant, in a broad sense, to include specific preparatory behaviors, instrumental goal-seeking behaviors, as well as the spontaneous investigatory responses characteristic of motivational arousal. The term ‘consummatory phase’ is used in the spirit of Craig’s “phase II” of a motivated behavior “cycle” in which the “reception of the appeted stimulus” is followed by a “consummatory reaction in response to that stimulus” (see Craig 1918, p 101). The appetitive/consummatory distinction can refer to the temporal organization of behavior in which the consummatory reaction is that which terminates the behavioral sequence but can also refer to qualitative differences between the flexible behaviors leading up to goal attainment vs the relatively stereotyped action patterns observed during commerce with the goal (Craig 1918). Our usage conforms more to the latter theme. Hence, we use ‘consummatory phase’ to designate the period in which repetitive, relatively inflexible motor acts occur during actual contact with the food; chewing, licking, swallowing, etc. In the context of ingestive behavior (which involves actual consumption), the term ‘consumatory’ is sometimes preferred to ‘consummatory’ (see Smith 1995), but we will use the latter term simply to imply the generalizability of our proposed framework to other motivated behaviors, such as sexual behavior.
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Acknowledgements
This work was supported by National Institute on Drug Abuse grant DA 09311 (A.E.K.) and National Institute on Mental Health grant MH 74723 (B.A.B).
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Baldo, B.A., Kelley, A.E. Discrete neurochemical coding of distinguishable motivational processes: insights from nucleus accumbens control of feeding. Psychopharmacology 191, 439–459 (2007). https://doi.org/10.1007/s00213-007-0741-z
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DOI: https://doi.org/10.1007/s00213-007-0741-z