Neural systems for behavioral activation and reward

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Abstract

The circuitry mediating the integration of reward perception and adaptive behavioral responses has been further refined. Recent developments indicate that the nucleus accumbens has a primary role in motivational circuitry, whereas afferents to the nucleus accumbens, in part, subserve distinct functions. Dopaminergic afferents serve to signal changes in rewarding stimuli, whereas glutamatergic input from the amygdala serves to cue behavior to conditioned reward, and afferents from the prefrontal cortex integrate information from short-term memory into behavioral responses.

Introduction

The neural substrates of behavioral activation and the perception of reward are thought to be remarkably coincident. This is most likely a consequence of two factors. First, the close temporal link between the perception of a reward and the initiation of an appropriate behavioral response to obtain or investigate a rewarding stimulus has adaptive value. Second, our emerging knowledge of the subtle topography of projections within the relevant circuitry and the synaptic organization within individual nuclei currently exceeds our technical abilities to determine the functional significance of these organizational subtleties. Thus, the appearance of anatomical coincidence may wane with the emergence of a more detailed functional analysis of the underlying circuitry.

Figure 1 illustrates the nuclei that are most frequently associated with mediating both the perception of reward and the initiation of motor behaviors. The interconnections between these nuclei form a circuit that has been termed the motive circuit [1]. Figure 1 will be used as a template to organize findings in the recent literature concerning the neural mechanisms mediating the translation of the perception of reward into behavioral activation. Following a brief historical introduction, this review will endeavor to assign the factors regulating motivated behavior, such as novelty, memory and conditioned responses, to the specific anatomical substrates illustrated in Figure 1.

Section snippets

Historical perspectives on the construction of the motive circuit

Our understanding of the neural circuits mediating reward and motor activation has emerged by distinct evolutionary routes. The involvement of extrapyramidal motor nuclei such as the caudate putamen in the motive circuit was recognized, in part, because clearly identified motor neuropathologies such as Parkinson’s disease and Huntington’s chorea are associated with lesions of this structure. In experimental rodents, the caudate putamen is generally termed the striatum and is divided into a

Ventral tegmental area

Excitatory input to dopamine neurons in the ventral tegmental area, as well as disinhibition from local or descending GABAergic inhibition, has long been known to modulate reward and motor behavior. Recent contributions by Schultz and colleagues (see [7]) have elevated our understanding of the role that dopamine neurons play in the central processing of rewarding stimuli. By making electrophysiological measurements in behaving primates, they revealed that dopamine cellular activity labels

Conclusions

Figure 1 illustrates components of a circuit thought to be integral in translating rewarding stimuli into adaptive motor responses. Even though this conceptualization has evolved over the past two decades, recent studies have provided important refinements. Notable among the refinements is the capacity to assign functional roles to various afferents of the nucleus accumbens. Dopaminergic inputs to the ventral tegmental area appear to provide a prediction error signal that cues novel aspects of

Acknowledgements

The conceptualizations present in this review were supported in part by United States Public Health Service (USPHS) grants MH-40817 and DA-03906.

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

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