Previous studies indicate that the dorsolateral striatum (DLS) integrates sensorimotor information from cortical and thalamic regions to learn and execute motor habits. However, the exact contribution of sensory representations to this process is still unknown. Here we explore the role of the forelimb somatosensory flow in the DLS during the learning and execution of motor habits. First, we compare rhythmic somesthetic representations in the DLS and primary somatosensory cortex in anesthetized rats, and find that sequential and temporal stimuli contents are more strongly represented in the DLS. Then, using a behavioral protocol in which rats developed a stereotyped motor sequence, functional disconnection experiments, and pharmacologic and optogenetic manipulations in apprentice and expert animals, we reveal that somatosensory thalamic- and cortical-striatal pathways are indispensable for the temporal component of execution. Our results indicate that the somatosensory flow in the DLS provides the temporal reference for the development and execution of motor habits.
Movement initiation and control require the orchestrated activity of sensorimotor cortical and subcortical regions. However, the exact contribution of specific pathways and interactions to the final behavioral outcome are still under debate. Here, by combining structural lesions, pathway-specific optogenetic manipulations and freely moving electrophysiological recordings in rats, we studied cortico-striatal interactions in the context of forelimb bilaterally coordinated movements. We provide evidence indicating that bilateral actions are initiated by motor cortical regions where intratelencephalic bilateral cortico-striatal (bcs-IT) projections recruit the sensorimotor striatum to provide stability and duration to already commanded bilateral movements. Furthermore, striatal spiking activity was correlated with movement duration and kinematic parameters of the execution. bcs-IT stimulation affected only the representation of movement duration but spared that of kinematics. Our findings confirm the modular organization of information processing in the striatum and its involvement in moment-to-moment movement control but not initiation or selection.
The substantia nigra pars reticulata (SNr), where the basal ganglia (BG) direct and indirect pathways converge, contains among the highest expression of cannabinoid receptor type 1 (CB1r) in the brain. Hence, SNr is an ideal locus to study pathway interactions and cannabinergic modulations. The objective of this study was to characterize the effects of systemic injections of the CB1r agonist (CP55940) on the balanced activity of the direct/indirect pathways in the SNr and its associated behaviors. To this aim, we recorded somatosensory and pathway-specific representations in the spiking activity of the SNr of male rats under CP55940. CB1r activation mainly decreased the inhibitory, potentially direct pathway component while sparing the excitatory, potentially indirect pathway component of somatosensory responses. As a result, cutaneous stimulation produced unbalanced responses favoring increased SNr firing rates, suggesting a potential locus for cannabinergic motorrelated effects. To test this hypothesis, we implemented an ad hoc behavioral protocol for rats in which systemic administration of CP55940 produced kinematic impairments that were completely reverted by nigral injections of the CB1r antagonist (AM251). Our data suggest that cannabinoid-related motor effects are associated with unbalanced direct/indirect pathway activations that may be reverted by CB1r manipulation at the SNr.
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