Distinct recruitment of dorsomedial and dorsolateral striatum erodes with extended training

Abstract

Hypotheses of striatal orchestration of behavior ascribe distinct functions to striatal subregions, with the dorsolateral striatum (DLS) especially implicated in habitual and skilled performance. Thus neural activity patterns recorded from the DLS, but not the dorsomedial striatum (DMS), should be correlated with habitual and automatized performance. Here, we recorded DMS and DLS neural activity in rats during training in a task promoting habitual lever pressing. Despite improving performance across sessions, clear changes in corresponding neural activity patterns were not evident in DMS or DLS during early training. Although DMS and DLS activity patterns were distinct during early training, their activity was similar following extended training. Finally, performance after extended training was not associated with DMS disengagement, as would be predicted from prior work. These results suggest that behavioral sequences may continue to engage both striatal regions long after initial acquisition, when skilled performance is consolidated.

The basal ganglia can control learned motor sequences independently of motor cortex

“…That unit activity in the DLS is significantly modulated during the execution of the learned motor sequences is largely in agreement with previous reports on the involvement of the DLS, but not the DMS, in over-trained behaviors 25,57 (but see reference 58 ). However, the way in which population activity in the DLS varies over the time-course of the behavior differs markedly across paradigms 13,22,23,59 , a difference which has inspired the two major models of BG function ( Figure 1A).…”

“…Results supporting the 'action selection' model show that neurons in the DLS are preferentially active at the beginning and end of over-trained motor sequences [22][23][24] . We note that the repetitive behaviors used in these tasks -locomotion and simple lever pressing -can be executed without BG involvement 13,58,60,61 , likely by mid-brain and brainstem motor controllers.…”

“…At first, our findings may seem at odds with prior studies, which have come to different conclusions regarding BG's function in motor skill execution. There is indeed a heterogeneity of results and conclusions to consider, even if we limit ourselves to studies in which rodents are tasked with pressing a lever or joystick 12,23,24,58 . In most cases experimental outcomes have conformed to one of the established models of BG function -the 'action selection' or the 'vigor' hypotheses 12,15,23,24,58,72 .…”

“…For instance, several studies ascribing an 'action selection' role to the BG reward animals for producing kinematically and temporally unconstrained repetitive lever pressing behaviors 23,24,27 . Repetitive lever pressing itself is likely 'solved' by midbrain/brainstem/spinal motor circuits and does not seem to require the BG 58,60,61 . This is further supported by our study, in which DLS lesioned rats, incapable of executing the previously acquired sequences, were perfectly capable of repetitive lever pressing ( Figure 7).…”

“…That the idiosyncratic motor sequences that emerge from training in our timed lever pressing task are qualitatively different from the behaviors in the oft-used repetitive lever pressing tasks, and that the BG 'treat' these tasks differently, is evident also when comparing the neural representations in the DLS and DMS 58 across the tasks. For example, over-trained repetitive lever pressing behaviors appear to be encoded in a very similar manner in both the DLS and the DMS 58 , wherein SPNs preferentially encode the start and stop of the sequence 23,58 . This lack of a more detailed representation in both dorsal striatal subregions is consistent with neither area being required for the control of the behavior 58,60 .…”