Reward-guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico-basal ganglia networks

Abstract

Here we challenge the view that reward-guided learning is solely controlled by the mesoaccumbens pathway arising from dopaminergic neurons in the ventral tegmental area and projecting to the nucleus accumbens. This widely accepted view assumes that reward is a monolithic concept, but recent work has suggested otherwise. It now appears that, in reward-guided learning, the functions of ventral and dorsal striata, and the cortico-basal ganglia circuitry associated with them, can be dissociated. Whereas the nucleus accumbens is necessary for the acquisition and expression of certain appetitive Pavlovian responses and contributes to the motivational control of instrumental performance, the dorsal striatum is necessary for the acquisition and expression of instrumental actions. Such findings suggest the existence of multiple independent yet interacting functional systems that are implemented in iterating and hierarchically organized cortico-basal ganglia networks engaged in appetitive behaviors ranging from Pavlovian approach responses to goal-directed instrumental actions controlled by action-outcome contingencies.

Figure 1

Major functional domains of the striatum. An illustration of the striatum from a coronal section showing half of the brain (Paxinos and Franklin, 2003). Note that these four functional domains are anatomically continuous, and roughly correspond to what are commonly known as nucleus accumbens shell and core (limbic striatum), dorsomedial (DMS, association) striatum, and dorsolateral (DLS, sensorimotor) striatum. We have not included other ventral striatal regions (e.g. areas posterior to the nucleus accumbens) which are not well understood. According to our framework, these limbic striatal areas should be broadly similar to the ccumbens in function.

Figure 2

The cortico-basal ganglia networks An illustration of the major corticostriatal projections and dopaminergic projections in terms of the four major cortico-basal ganglia networks and their corresponding behavioral functions. Pallidal, thalamic, and other structures have been omitted for the sake of clarity. Emphasis is placed on the spiraling midbrain-striatum-midbrain projections, which allows information to be propagated forward in a hierarchical manner. Note that this is only one possible neural implementation; interactions via different thalamo-cortico-thalamic projections are also possible (Haber, 2003). BLA, basolateral amygdale complex; mPFC, medial prefrontal cortex; vPFC, ventral prefrontal cortex; SI/MI, primary sensory and motor cortices; DLS, dorsolateral striatum; DMS, dorsomedial striatum; shell, nucleus accumbens shell; core, nucleus accumbens core.