Prolonged dopamine signalling in striatum signals proximity and value of distant rewards

Abstract

Predictions about future rewarding events have a powerful influence on behaviour. The phasic spike activity of dopamine-containing neurons, and corresponding dopamine transients in the striatum, are thought to underlie these predictions, encoding positive and negative reward prediction errors1–5. Many behaviours, however, are directed toward distant goals, for which transient signals might fail to provide sustained drive. Here we report a novel, extended mode of reward-predictive dopamine signalling in the striatum that emerged as rats moved toward distant goals. These dopamine signals, which were detected with fast-scan cyclic voltammetry (FSCV), gradually increased or--in rare instances--decreased as the animals navigated mazes to reach remote rewards, rather than having phasic or steady tonic profiles. These dopamine increases (ramps) scaled flexibly with both the distance and size of the rewards. During learning, these dopamine signals exhibited spatial preferences for goals in different locations and readily changed in magnitude to reflect changing values of the distant rewards. Such prolonged dopamine signalling could provide sustained motivational drive, a control mechanism that may be important for normal behaviour and that can be impaired in a range of neurologic and neuropsychiatric disorders.

Surprise! Dopamine signals mix action, value and error

“…Because RPEs are inherently deviations in reward value, Hamid et al 5 reasoned that this analysis could obscure the true nature of DA signals in terms of value. Moreover, a previous study suggested that DA levels ramp up as animals approach a rewarding location, as is consistent with a signal related to reward expectation 11 .…”

Cross-hemispheric dopamine projections have functional significance

“…FSCV has been used to measure dopamine fluctuations in a number of studies; however, to date, all awake-animal measurements have been restricted to a single hemisphere (1)(2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(31)(32)(33)(34)(35). To investigate connectivity between hemispheres, we measured dopamine transients bilaterally in the NAc of freely moving rats.…”

Ramping ensemble activity in dorsal anterior cingulate neurons during persistent commitment to a decision

“…One method of maintaining motivation would be to maintain some representation of the reward as progress is made toward it, such that the progress itself is rewarding (Hillman and Bilkey 2010; Howe et al 2013). Such a signal could potentially act as a control signal, keeping the animal motivated to perform a particular action.…”

“…One possibility is that brain activation elicited by an expected reward may serve to maintain motivation and ensure successful persistence (Howe et al 2013). One way it could do this is to actively maintain a value signal that allows for decision-makers to overcome a tendency to succumb to temptation (Hillman and Bilkey 2010).…”