Complementary Control over Habits and Behavioral Vigor by Phasic Activity in the Dorsolateral Striatum

Abstract

Despite clear evidence linking the basal ganglia to the control of outcome insensitivity (i.e., habit) and behavioral vigor (i.e., its behavioral speed/fluidity), it remains unclear whether or how these functions relate to one another. Here, using male Long-Evans rats in response-based and cue-based maze-running tasks, we demonstrate that phasic dorsolateral striatum (DLS) activity occurring at the onset of a learned behavior regulates how vigorous and habitual it is. In a response-based task, brief optogenetic excitation at the onset of runs decreased run duration and the occurrence of deliberative behaviors, whereas midrun stimulation carried little effect. Outcome devaluation showed these runs to be habitual. DLS inhibition at run start did not produce robust effects on behavior until after outcome devaluation. At that time, when the DLS was plausibly most critically required for performance (i.e., habitual), inhibition reduced performance vigor measures and caused a dramatic loss of habitual responding (i.e., animals quit the task). In a second cue-based "beacon" task requiring behavior initiation at the start of the run and again in the middle of the run, DLS excitation at both time points could improve the vigor of runs. Postdevaluation testing showed behavior on the beacon task to be habitual as well. This pattern of results suggests that one role for phasic DLS activity at behavior initiation is to promote the execution of the behavior in a vigorous and habitual fashion by a diverse set of measures.SIGNIFICANCE STATEMENT Our research expands the literature twofold. First, we find that features of a habitual behavior that are typically studied separately (i.e., maze response performance, deliberation movements, running vigor, and outcome insensitivity) are quite closely linked together. Second, efforts have been made to understand "what" the dorsolateral striatum (DLS) does for habitual behavior, and our research provides a key set of results showing "when" it is important (i.e., at behavior initiation). By showing such dramatic control over habits by DLS activity in a phasic time window, plausible real-world applications could involve more informed DLS perturbations to curb intractably problematic habits.

Keywords: basal ganglia; deliberation (VTE); dorsolateral striatum; goal-directed action; habit; optogenetics; outcome insensitivity; plus-maze; vigor.

Figure 1.

Response task. A, Top, Maze task schematic illustrating left-turn example (green, gates). Middle, Example protocol of five-trial blocks with start locations for a session. Bottom left, Session order for task acquisition (through 3 d of ≥75% accuracy) and baseline test (fiber cables connected but no light delivery). Bottom right, example DLS manipulation protocol (continuous 0.5 s of light delivery) on test days. B, Run accuracy in 12 sessions leading up to the final day of criterion performance, separated by ChR2 (blue), control (gray), and eNpHR3.0 (yellow) groups. Lines and errors show mean ± SEM. Groups were not different. C, Histology maps showing expression areas of ChR2-EYFP, EYFP control, and eNpHR3.0-EYFP across animals. Semitransparent shading denotes expression per animal; shading is overlaid across animals. Numbers denote anteroposterior plane in millimeters relative to bregma. X, fiber implant placements. D, Example confocal images of DLS: EYFP, NeuroTrace, low-magnitude overlay, high-magnitude overlay. Arrows show the same neuron examples across labeling.

Figure 2.

ChR2-evoked stimulation of DLS neurons with continuous 0.5 s blue light. Histograms (0.02 s bins) of all single recorded units that were responsive to blue light. Firing rate (Hz) is shown 0.5 s before, during, and after light delivery. A, Units recorded under anesthesia (n = 9). B, Units recorded during free behavior (n = 3). A, B, Columns show the same unit recorded when light was delivered for 0.5 s every 1 min (left columns) and when light was delivered in a 0.5 s on/off cycle (right columns). Gaps denote units that were not stable or were not detected during that light delivery protocol. Although not all units responded to light immediately, they nonetheless exhibited response excitation as confirmation of ChR2-mediated stimulation of the DLS. Units with activity inhibited by light were not observed.

Figure 3.

Changes in response maze behavior with DLS manipulations. A, Duration of maze runs (seconds). DLS stimulation reduced run duration if given at run start or cycled. DLS inhibition could increase run duration marginally when given midrun and when cycled. B, Percentage of trials with deliberations. Increases and decreases in deliberation generally followed increases and decreases in run duration. C, Percentage of correct running across the baseline and illumination test days. DLS manipulations did not affect run accuracy. Bars and errors show mean ± SEM; asterisks denote significant post hoc comparisons (*p < 0.05, **p < 0.01, ***p < 0.001); lack of asterisks denotes lack of significance.

Figure 4.

Response maze behavior related to outcome devaluation. A, Devaluation testing timeline. Light was given at run start in a predevaluation extinction session (followed by a no-light retraining session) and postdevaluation extinction and reacquisition (pellets delivered) sessions. Gray, controls; blue, ChR2; yellow, eNpHR3.0. B, Pellet consumption during each of the three pellet/LiCl pairings to cause devaluation. All animals rejected pellets by the third pairing. C, Accuracy of maze running in trials in which runs occurred. No group differences. D, Percentage of trials in each session completed before quitting the task. Animals ran all trials before outcome devaluation. After devaluation, animals ran by habit in ChR2 and control groups, but animals with DLS inhibition ran very few trials, showing devaluation sensitivity. E, Average cumulative duration of trial runs (seconds). DLS made animals faster on each day, whereas DLS inhibition made animals slower. F, Percentage change in cumulative duration relative to controls. Blue, ChR2 group versus control; yellow, eNpHR3.0 versus control. G, Percentage of trials with deliberation. These again mirrored changes in run duration. H, Percentage of pellets consumed in task (before task quitting), which was reduced across groups and trials from predevaluation to postdevaluation with illumination at run start. Groups did not differ in reduced pellet consumption after devaluation. Bars and errors show mean ± SEM; asterisks denote significant post hoc comparisons (*p < 0.05, **p < 0.01, ***p < 0.001); lack of asterisks denotes lack of significance. ns, Not significantly different.

Figure 5.

Beacon task. A, Maze setup and schematics for trial blocks, training, and DLS manipulation testing as in Figure 1A. B, Histological maps showing control and ChR2 expression, as in Figure 1C. D, Run accuracy in 12 sessions leading up to the final day of criterion performance, separated by ChR2 (blue) and control (gray) groups (no group differences). Lines and errors show mean ± SEM.

Figure 6.

Changes in beacon maze-running behavior with DLS manipulation. A, Average cumulative duration of maze runs (seconds). DLS stimulation reduced run duration whether given at run start, midrun, or cycled. Blue, ChR2; gray, controls. B, Percentage of trials with deliberation, which DLS stimulation also reduced. C, Percentage of trials run correctly, which did not differ between groups. Asterisks denote significant post hoc comparisons (*p < 0.05, **p < 0.01, **p < 0.001).

Figure 7.

Beacon task related to outcome devaluation. A, Devaluation testing timeline, as in Figure 4. B, Pellet consumption during each pellet/LiCl pairing day to devalue rat groups. Consumption fell to zero in both groups. C, Performance accuracy when rats ran, which was high and stable, suggesting habitual performance by both groups. Blue, ChR2; gray, controls. D, Percentage of trials completed before quitting. Both groups ran nearly all trial opportunities. E, Average cumulative duration of trial runs (seconds). DLS stimulation reduced it on each day. F, Percentage change in cumulative duration in animals with ChR2-mediated stimulation relative to controls (blue). G, Percentage of trials with deliberation, which DLS stimulation reduced. H, Percentage of pellets consumed on task (before quitting a run), which was reduced equivalently across groups from predevaluation to postdevaluation. Asterisks denote significant post hoc comparisons (*p < 0.05, **p < 0.01, **p < 0.001). ns, Not significantly different.