Dopaminergic mechanisms in actions and habits

Abstract

Recent studies suggest new ways to interpret dopaminergic actions in goal-directed performance and habitual responding. In the early stages of learning dopamine plays an essential role, but with extended training dopamine appears to play a decreasing role in response expression. Experimental manipulation of dopamine levels alters the correlation of cortical and striatal neural activity in behaving animals, and these dopamine-dependent changes in corticostriatal correlations may be reflected in changes in action selection in the basal ganglia. Consistent with this hypothesis, changes in dopamine signaling brought about by sensitization with amphetamine mimic the transition from goal-directed to habit-based instrumental performance. At the cellular level, dopamine-dependent synaptic plasticity may be important initially, and subsequently lead to more persistent changes that no longer require dopamine. The locus of these actions within the cortical and corticostriatal circuitry is a focus on ongoing research.

Figure 1.

Strengthening corticostriatal connections can lead to increased correlation of cortical and striatal activity, and a shift to S–R responding. The upward arrow indicates that the glutamatergic corticostriatal synapse (GLU) is strengthened by dopaminergic activity (DA), which may also facilitate information transmission by changing the excitability of striatal cells. Connections are shown from the cortex to the striatum and back to cortex via the globus pallidus and thalamus (unlabeled). One possibility would be that DA-mediated strengthening of task-relevant corticostriatal synapses would eventually render striatal neurons able to fire in the absence of concomitant dopamine release. This strengthening could, with repetition, extend to different striatal subregions than the ones encoding the initial goal-directed behavior (Miyachi et al., 1997; Yin et al., 2004), which would account for the findings that performance of the well established behavior is no longer outcome mediated and less DA dependent. Another possibility would be that direct S–R connections (dotted line) are formed, for example, by the establishment of corticocortical connections (Ashby et al., 2007; Carelli et al., 1997). Neurotransmission via these latter connections would also account for the finding that performance of the well established behavior is no longer outcome mediated.