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

Howe MW, Tierney PL, Sandberg SG, Phillips PE, Graybiel AM - Nature (2013)

Bottom Line: 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.During learning, these dopamine signals showed 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.

View Article: PubMed Central - PubMed

Affiliation: McGovern Institute for Brain Research and Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.

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 errors. However, many behaviours are directed towards distant goals, for which transient signals may fail to provide sustained drive. Here we report an extended mode of reward-predictive dopamine signalling in the striatum that emerged as rats moved towards 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 showed 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.

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Dopamine ramping is sensitive to reward magnitudea, b, Average dopamine signals from a VMS probe, for consecutive T-maze (a) and M-maze (b) sessions with asymmetric rewards. Asterisks indicate the goal with larger reward. Red arrows (and Switch) indicate reversal of reward amounts. c, Dopamine signals from a different rat running in the S-maze. White arrows indicate run direction. d, Average (± s.e.m.) peak dopamine across all value experiments (n = 4 rats). e, Average (± s.e.m.) VMS dopamine during T-maze (n = 44 sessions in 3 rats, black) and M-maze (n = 17, blue) sessions in same rats. f, g, Average (± s.e.m.) peak dopamine signals for the sessions plotted in a (f) and b (g) for trials to left (blue) and right (red) goals. Shading indicates arm with larger reward. h, i, Average normalized dopamine (h) and running speed (i) for runs to high (light green) and low (dark green) reward goals in the M-maze. Vertical lines indicate turns. j, k, Average normalized dopamine (j) and running speed (k) in the S-maze (n = 9 sessions in 2 rats), plotted as in h and i.
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Figure 3: Dopamine ramping is sensitive to reward magnitudea, b, Average dopamine signals from a VMS probe, for consecutive T-maze (a) and M-maze (b) sessions with asymmetric rewards. Asterisks indicate the goal with larger reward. Red arrows (and Switch) indicate reversal of reward amounts. c, Dopamine signals from a different rat running in the S-maze. White arrows indicate run direction. d, Average (± s.e.m.) peak dopamine across all value experiments (n = 4 rats). e, Average (± s.e.m.) VMS dopamine during T-maze (n = 44 sessions in 3 rats, black) and M-maze (n = 17, blue) sessions in same rats. f, g, Average (± s.e.m.) peak dopamine signals for the sessions plotted in a (f) and b (g) for trials to left (blue) and right (red) goals. Shading indicates arm with larger reward. h, i, Average normalized dopamine (h) and running speed (i) for runs to high (light green) and low (dark green) reward goals in the M-maze. Vertical lines indicate turns. j, k, Average normalized dopamine (j) and running speed (k) in the S-maze (n = 9 sessions in 2 rats), plotted as in h and i.

Mentions: Given that phasic responses of dopamine-containing neurons can reflect the relative value of stimuli21, we asked, in a subset of rats, whether the ramping dopamine signals could also be modulated by the size of the delivered rewards (Methods). We used mazes with T, M or S configurations and different total lengths (Fig. 3, Extended Data Fig. 8). We required the animals to run toward one or the other maze-end and varied the rewards available at the alternate goal-regions. With all three mazes, dopamine ramping became strongly biased toward the goal with the larger reward (Fig. 3, Extended Data Fig. 8). Run speed was slightly higher for the high-reward maze arms (Fig. 3i,k), but these small differences were unlikely to account fully for the large differences in the dopamine signals recorded. When we then reversed the locations of the small and large rewards, the ramping signals also shifted, across sessions or just a few trials, so as to favour the new high-value maze-arm (Fig. 3, Extended Data Fig. 8). These bias effects were statistically significant for each experimental paradigm (Extended Data Fig. 8h–j, Mann-Whitney U-test, P < 0.05) and across all rats (Fig. 3d, n = 4, Mann-Whitney U-test, P = 0.02).


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

Howe MW, Tierney PL, Sandberg SG, Phillips PE, Graybiel AM - Nature (2013)

Dopamine ramping is sensitive to reward magnitudea, b, Average dopamine signals from a VMS probe, for consecutive T-maze (a) and M-maze (b) sessions with asymmetric rewards. Asterisks indicate the goal with larger reward. Red arrows (and Switch) indicate reversal of reward amounts. c, Dopamine signals from a different rat running in the S-maze. White arrows indicate run direction. d, Average (± s.e.m.) peak dopamine across all value experiments (n = 4 rats). e, Average (± s.e.m.) VMS dopamine during T-maze (n = 44 sessions in 3 rats, black) and M-maze (n = 17, blue) sessions in same rats. f, g, Average (± s.e.m.) peak dopamine signals for the sessions plotted in a (f) and b (g) for trials to left (blue) and right (red) goals. Shading indicates arm with larger reward. h, i, Average normalized dopamine (h) and running speed (i) for runs to high (light green) and low (dark green) reward goals in the M-maze. Vertical lines indicate turns. j, k, Average normalized dopamine (j) and running speed (k) in the S-maze (n = 9 sessions in 2 rats), plotted as in h and i.
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Figure 3: Dopamine ramping is sensitive to reward magnitudea, b, Average dopamine signals from a VMS probe, for consecutive T-maze (a) and M-maze (b) sessions with asymmetric rewards. Asterisks indicate the goal with larger reward. Red arrows (and Switch) indicate reversal of reward amounts. c, Dopamine signals from a different rat running in the S-maze. White arrows indicate run direction. d, Average (± s.e.m.) peak dopamine across all value experiments (n = 4 rats). e, Average (± s.e.m.) VMS dopamine during T-maze (n = 44 sessions in 3 rats, black) and M-maze (n = 17, blue) sessions in same rats. f, g, Average (± s.e.m.) peak dopamine signals for the sessions plotted in a (f) and b (g) for trials to left (blue) and right (red) goals. Shading indicates arm with larger reward. h, i, Average normalized dopamine (h) and running speed (i) for runs to high (light green) and low (dark green) reward goals in the M-maze. Vertical lines indicate turns. j, k, Average normalized dopamine (j) and running speed (k) in the S-maze (n = 9 sessions in 2 rats), plotted as in h and i.
Mentions: Given that phasic responses of dopamine-containing neurons can reflect the relative value of stimuli21, we asked, in a subset of rats, whether the ramping dopamine signals could also be modulated by the size of the delivered rewards (Methods). We used mazes with T, M or S configurations and different total lengths (Fig. 3, Extended Data Fig. 8). We required the animals to run toward one or the other maze-end and varied the rewards available at the alternate goal-regions. With all three mazes, dopamine ramping became strongly biased toward the goal with the larger reward (Fig. 3, Extended Data Fig. 8). Run speed was slightly higher for the high-reward maze arms (Fig. 3i,k), but these small differences were unlikely to account fully for the large differences in the dopamine signals recorded. When we then reversed the locations of the small and large rewards, the ramping signals also shifted, across sessions or just a few trials, so as to favour the new high-value maze-arm (Fig. 3, Extended Data Fig. 8). These bias effects were statistically significant for each experimental paradigm (Extended Data Fig. 8h–j, Mann-Whitney U-test, P < 0.05) and across all rats (Fig. 3d, n = 4, Mann-Whitney U-test, P = 0.02).

Bottom Line: 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.During learning, these dopamine signals showed 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.

View Article: PubMed Central - PubMed

Affiliation: McGovern Institute for Brain Research and Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.

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 errors. However, many behaviours are directed towards distant goals, for which transient signals may fail to provide sustained drive. Here we report an extended mode of reward-predictive dopamine signalling in the striatum that emerged as rats moved towards 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 showed 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.

Show MeSH