Striatal bilateral control of skilled forelimb movement

• Published in: Cell reports (Cambridge) Vol. 34; no. 3; p. 108651
• Main Authors: Lopez-Huerta, Violeta G., Denton, Jai A., Nakano, Yoko, Jaidar, Omar, Garcia-Munoz, Marianela, Arbuthnott, Gordon W.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 19.01.2021
• Subjects: Animals; basal ganglia; Corpus Striatum - physiology; direct pathway; Forelimb - physiology; forelimb kinematics; indirect pathway; Mice; motor learning; Movement - physiology; optogenetics; plasticity; reach to grasp; reciprocal collateral inhibition; striatum; basal ganglia; striatum; motor learning; optogenetics; forelimb kinematics; plasticity; reach to grasp; direct pathway; reciprocal collateral inhibition; indirect pathway
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2020.108651

Skilled motor behavior requires bihemispheric coordination, and participation of striatal outputs originating from two neuronal groups identified by distinctive expression of D1 or D2 dopamine receptors. We trained mice to reach for and grasp a single food pellet and determined how the output pathways differently affected forelimb trajectory and task efficiency. We found that inhibition and excitation of D1-expressing spiny projection neurons (D1SPNs) have a similar effect on kinematics results, as if excitation and inhibition disrupt the whole ensemble dynamics and not exclusively one kind of output. In contrast, D2SPNs participate in control of target accuracy. Further, ex vivo electrophysiological comparison of naive mice and mice exposed to the task showed stronger striatal neuronal connectivity for ipsilateral D1 and contralateral D2 neurons in relation to the paw used. In summary, while the output pathways work together to smoothly execute skill movements, practice of the movement itself changes synaptic patterns. [Display omitted] •Ipsilateral and contralateral striatal outputs control skilled forepaw movement•Direct and indirect striatal projection neurons differentially affect skilled movements•D1SPN projections control trajectory, whereas D2SPNs influence the target•Performance of learned skilled movements modifies striatal synaptic connectivity Lopez-Huerta et al. motivate mice to use their preferred paw to reach and grasp. Optogenetic manipulation of striatal D1 output neurons induces trajectory errors and D2 inhibition improves whereas activation disrupts target success. Performance modifies connectivity bilaterally among striatal output neurons recorded ex vivo.