Corticostriatal connectivity underlies individual differences in the balance between habitual and goal-directed action control

Abstract

Why are some individuals more susceptible to the formation of inflexible habits than others? In the present study, we used diffusion tensor imaging to demonstrate that brain connectivity predicts individual differences in relative goal-directed and habitual behavioral control in humans. Specifically, vulnerability to habitual "slips of action" toward no-longer-rewarding outcomes was predicted by estimated white matter tract strength in the premotor cortex seeded from the posterior putamen (as well as by gray matter density in the posterior putamen as determined with voxel-based morphometry). In contrast, flexible goal-directed action was predicted by estimated tract strength in the ventromedial prefrontal cortex seeded from the caudate. These findings suggest that integrity of dissociable corticostriatal pathways underlies individual differences in action control in the healthy population, which may ultimately mediate vulnerability to impulse control disorders.

Figure 1.

Illustration of instrumental task. a, contains an illustration of the instrumental learning stage. In this example, grapes (on the outside of the box) signal that pressing the right key will be rewarded with an orange (inside the box) and credits, whereas pressing the left key will not be rewarded. b contains a schematic depiction of the congruent, standard, and incongruent contingencies. c illustrates the slips-of-action test. In this example, the initial instruction screen shows the pineapple and pear outcomes with a cross superimposed, indicating that these will now lead to the subtraction of credits. The other four fruit outcomes are still valuable. After the instruction screen, participants are presented with a rapid succession of fruit stimuli (on the outside of the boxes) and are asked to press the correct keys when a stimulus signals the availability of a still-valuable outcome inside the box (“Go”) but to refrain from responding when the outcome inside the box has been devalued (“No-Go”). In this particular example, participants should press when the grapes stimulus is presented but refrain from responding on trials with the bananas stimulus. d shows the dual systems that are hypothesized to underlie performance on the slips-of-action test, with the S–O–R goal-directed system allowing for successful test performance based on outcome anticipation and evaluation, but the S–R habitual system activating responses directly and thereby giving rise to slips of action toward no-longer-valuable outcomes.

Figure 2.

Striatal tractography. Raw tractography data shown separately for the three striatal seed regions, at x = −18, y = −2, z = −12 (thresholded at 0.02% of total samples sent from the seed mask). Results are shown in neurological convention (right is right).

Figure 3.

Behavioral performance on the instrumental task. a shows mean levels of performance during instrumental training, separately for the congruent (open circles), standard (open squares), and incongruent (filled circles) trials, across six consecutive blocks. b shows the mean difference scores (responding toward valuable minus devalued outcomes/stimuli) for the slips-of-action test (filled bars) and the baseline test (open bars). For both a and b, error bars reflect SEMs, and these graphs have a non-zero origin at 50% (which denotes chance level for the training stage, whereas chance-level performance on the slips-of-action test would be at 0).

Figure 4.

Significant relationships between performance on the slips-of-action test and estimated white matter tract strength in corticostriatal pathways. a depicts our main tractography findings: whereas estimated caudate–vmPFC tract strength (shown here at x = −12, y = 48, z = −2) was a positive predictor of goal-directed performance (as reflected in difference scores on the standard trials of the slips-of-action test), connectivity between posterior putamen and PMC (shown at x = 34, y = −6, z = 56) was a negative predictor. b shows scatter plots with the corresponding connectivity–behavior correlations. The negative correlation between performance and posterior putamen–PMC tract strength (illustrated in the bottom scatter plot) remained significant after removing the outlier (R² = 0.34).

Figure 5.

Scatter plot with brain connectivity–behavior correlation for resolution of outcome-induced response conflict. The mean estimated tract strength (from all significant clusters) between the caudate and all significant clusters within the ACC (depicted on the right, shown at the peak voxel at x = −4, y = 38, z = 20) correlated positively with successful conflict resolution (as reflected in the difference scores on incongruent trials of the slips-of-action test). This graph has a non-zero origin.

Figure 6.

Scatter plot with gray matter–behavior correlation for goal-directed action. Gray matter density in the posterior putamen (depicted on the right, shown at the peak voxel at x = 22, y = 0, z = 2) was a negative predictor of goal-directed performance (as reflected in the difference scores on standard trials of the slips-of-action test). In the scatter plot, circles drawn around the dots indicate additional data points at those values. This graph has a non-zero origin.