A specific role for posterior dorsolateral striatum in human habit learning

Abstract

Habits are characterized by an insensitivity to their consequences and, as such, can be distinguished from goal-directed actions. The neural basis of the development of demonstrably outcome-insensitive habitual actions in humans has not been previously characterized. In this experiment, we show that extensive training on a free-operant task reduces the sensitivity of participants' behavior to a reduction in outcome value. Analysis of functional magnetic resonance imaging data acquired during training revealed a significant increase in task-related cue sensitivity in a right posterior putamen-globus pallidus region as training progressed. These results provide evidence for a shift from goal-directed to habit-based control of instrumental actions in humans, and suggest that cue-driven activation in a specific region of dorsolateral posterior putamen may contribute to the habitual control of behavior in humans.

Fig. 1

Illustration of free-operant VI-10 task. A fractal image remained present throughout the block. The filled-in yellow square indicated which button to press. Responses were self-paced. After non-rewarded responses, a dark gray circle was presented for 50 ms. A reward became available with a probability of 0.1 per second. After the subsequent button press, a picture of an M&M or Frito was shown for 1 s, indicating a food reward of the corresponding type. The two stimulus-response-outcome pairings used for each subject remained consistent throughout the experiment. A third fractal, shown with empty yellow squares, indicated a rest block.

Fig. 2

Behavioral results. During the last session of training, prior to the devaluation procedure (left), there are no significant differences in response rates between groups or when responding for the two food rewards (one which will be devalued through selective satiation and one which will not). During the extinction test following the devaluation procedure, response rates for the still-valued outcome remained high, as did response rates for the devalued outcome for the 3-day group. In contrast, response rates for the 1-day group for the devalued outcome are reduced, producing a significant training by devaluation interaction (P < 0.05).

Fig. 3

Neural correlates of habit learning, as revealed by an increasing response with training to the onset of task blocks relative to the onset of rest blocks in the 3-day group. (A) The right posterior putamen showed a significant increase in the [task onset — rest onset] contrast from the first two sessions to the final two sessions of training (x = 33, y = −24, z = 0; P < 0.001, P(cor) < 0.05). The blue crosshairs mark the voxels with the peak contrast value. (B) A plot of the contrast estimates for [task onset — rest onset] for each session of training is shown for the region displayed in (A). Contrast estimates for the 2 sessions from the 1-day group are also shown.

Fig. 4

Nucleus accumbens region displaying a phasic response to reward presentation. (A) The nucleus accumbens displayed a significant response to reward presentation for both the 1-day group (left; x = −12, y = 3, z = −3; P < 0.001) and the 3-day group (right; x = −6, y = 6, z = −6; P < 0.001). The blue crosshairs mark the voxels with the peak contrast value. (B) A plot of the contrast estimates for the reward contrast for each training session is shown for the regions displayed in (A). The contrast magnitude remained consistent over training.

Fig. 5

Neural correlates of goal representation, as revealed by increased activation as anticipation of an upcoming reward increases. (A) A plot of the contrast estimates for the region in the vmPFC showing an effect of the “ramp” modulator for the first two sessions of training for all subjects is shown. This modulator indicates the number of seconds since the previous reward presentation or start of the block during performance of task blocks. The contrast estimates for each of the remaining training sessions for the 3-day group is also shown (top right). There is no clear pattern of change in this contrast over the course of training. (B) The vmPFC region showing a significant effect of the ramp modulator in all subjects over the first 2 sessions of training is shown (x = −3, y = 45, z = −18; P < 0.001). The blue crosshair marks the voxel with the peak contrast value.