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Skilled reaching relies on a V2a propriospinal internal copy circuit.

Azim E, Jiang J, Alstermark B, Jessell TM - Nature (2014)

Bottom Line: The precision of skilled forelimb movement has long been presumed to rely on rapid feedback corrections triggered by internally directed copies of outgoing motor commands, but the functional relevance of inferred internal copy circuits has remained unclear.Moreover, optogenetic activation of the PN internal copy branch recruits a rapid cerebellar feedback loop that modulates forelimb motor neuron activity and severely disrupts reaching kinematics.Our findings implicate V2a PNs as the focus of an internal copy pathway assigned to the rapid updating of motor output during reaching behaviour.

View Article: PubMed Central - PubMed

Affiliation: Howard Hughes Medical Institute, Kavli Institute for Brain Science, Mortimer B. Zuckerman Mind Brain Behavior Institute, Departments of Neuroscience and Biochemistry and Molecular Biophysics, Columbia University, New York, New York 10032, USA.

ABSTRACT
The precision of skilled forelimb movement has long been presumed to rely on rapid feedback corrections triggered by internally directed copies of outgoing motor commands, but the functional relevance of inferred internal copy circuits has remained unclear. One class of spinal interneurons implicated in the control of mammalian forelimb movement, cervical propriospinal neurons (PNs), has the potential to convey an internal copy of premotor signals through dual innervation of forelimb-innervating motor neurons and precerebellar neurons of the lateral reticular nucleus. Here we examine whether the PN internal copy pathway functions in the control of goal-directed reaching. In mice, PNs include a genetically accessible subpopulation of cervical V2a interneurons, and their targeted ablation perturbs reaching while leaving intact other elements of forelimb movement. Moreover, optogenetic activation of the PN internal copy branch recruits a rapid cerebellar feedback loop that modulates forelimb motor neuron activity and severely disrupts reaching kinematics. Our findings implicate V2a PNs as the focus of an internal copy pathway assigned to the rapid updating of motor output during reaching behaviour.

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3D kinematics of mouse reachinga, Following training, mice exhibited a high degree of variability in success in the multi-reach assay (37.0% +/− 10.4% s.d.; n = 13). Error bars indicate s.d. The mean s.d. of reach success from day to day across mice was 10.2% +/− 4.1% s.d. (n = 13). b, Individual reach plots of paw distance to pellet, velocity vs. time and velocity vs. distance to pellet from a representative mouse. Transition from the early reach phase to the late grab phase of the movement is delineated by the box opening (large dashes). Velocity crossings of zero (small dashes) indicate reversals in direction toward or away from the pellet. See Fig. 3d for mean plots from the same mouse.
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Figure 8: 3D kinematics of mouse reachinga, Following training, mice exhibited a high degree of variability in success in the multi-reach assay (37.0% +/− 10.4% s.d.; n = 13). Error bars indicate s.d. The mean s.d. of reach success from day to day across mice was 10.2% +/− 4.1% s.d. (n = 13). b, Individual reach plots of paw distance to pellet, velocity vs. time and velocity vs. distance to pellet from a representative mouse. Transition from the early reach phase to the late grab phase of the movement is delineated by the box opening (large dashes). Velocity crossings of zero (small dashes) indicate reversals in direction toward or away from the pellet. See Fig. 3d for mean plots from the same mouse.

Mentions: To evaluate the behavioral role of PNs we developed a three-dimensional kinematic assay of paw position during a goal-directed reaching task (Fig. 3a,b, Supplementary Videos 1,2, Methods)33,34. We delineated three modular aspects of movement: an early proximal ‘reach’ phase, from forelimb lift to the point that the paw passes through the access window; a late distal ‘grab’ phase, in which the arm is fully extended and the paw pronates in anticipation of pellet retrieval; and a digit abduction phase, during grasp. Task success, defined by pellet retrieval, was assessed in a multi-reach assay that tolerates numerous reach attempts34, and a more stringent single trial kinematic reach assay (Supplementary Note 4). In both assays the incidence of trial success varied considerably between animals (Extended Data Fig. 2a)33, leading us to compare behavior within individual mice, before and after experimental perturbation.


Skilled reaching relies on a V2a propriospinal internal copy circuit.

Azim E, Jiang J, Alstermark B, Jessell TM - Nature (2014)

3D kinematics of mouse reachinga, Following training, mice exhibited a high degree of variability in success in the multi-reach assay (37.0% +/− 10.4% s.d.; n = 13). Error bars indicate s.d. The mean s.d. of reach success from day to day across mice was 10.2% +/− 4.1% s.d. (n = 13). b, Individual reach plots of paw distance to pellet, velocity vs. time and velocity vs. distance to pellet from a representative mouse. Transition from the early reach phase to the late grab phase of the movement is delineated by the box opening (large dashes). Velocity crossings of zero (small dashes) indicate reversals in direction toward or away from the pellet. See Fig. 3d for mean plots from the same mouse.
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Related In: Results  -  Collection

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Figure 8: 3D kinematics of mouse reachinga, Following training, mice exhibited a high degree of variability in success in the multi-reach assay (37.0% +/− 10.4% s.d.; n = 13). Error bars indicate s.d. The mean s.d. of reach success from day to day across mice was 10.2% +/− 4.1% s.d. (n = 13). b, Individual reach plots of paw distance to pellet, velocity vs. time and velocity vs. distance to pellet from a representative mouse. Transition from the early reach phase to the late grab phase of the movement is delineated by the box opening (large dashes). Velocity crossings of zero (small dashes) indicate reversals in direction toward or away from the pellet. See Fig. 3d for mean plots from the same mouse.
Mentions: To evaluate the behavioral role of PNs we developed a three-dimensional kinematic assay of paw position during a goal-directed reaching task (Fig. 3a,b, Supplementary Videos 1,2, Methods)33,34. We delineated three modular aspects of movement: an early proximal ‘reach’ phase, from forelimb lift to the point that the paw passes through the access window; a late distal ‘grab’ phase, in which the arm is fully extended and the paw pronates in anticipation of pellet retrieval; and a digit abduction phase, during grasp. Task success, defined by pellet retrieval, was assessed in a multi-reach assay that tolerates numerous reach attempts34, and a more stringent single trial kinematic reach assay (Supplementary Note 4). In both assays the incidence of trial success varied considerably between animals (Extended Data Fig. 2a)33, leading us to compare behavior within individual mice, before and after experimental perturbation.

Bottom Line: The precision of skilled forelimb movement has long been presumed to rely on rapid feedback corrections triggered by internally directed copies of outgoing motor commands, but the functional relevance of inferred internal copy circuits has remained unclear.Moreover, optogenetic activation of the PN internal copy branch recruits a rapid cerebellar feedback loop that modulates forelimb motor neuron activity and severely disrupts reaching kinematics.Our findings implicate V2a PNs as the focus of an internal copy pathway assigned to the rapid updating of motor output during reaching behaviour.

View Article: PubMed Central - PubMed

Affiliation: Howard Hughes Medical Institute, Kavli Institute for Brain Science, Mortimer B. Zuckerman Mind Brain Behavior Institute, Departments of Neuroscience and Biochemistry and Molecular Biophysics, Columbia University, New York, New York 10032, USA.

ABSTRACT
The precision of skilled forelimb movement has long been presumed to rely on rapid feedback corrections triggered by internally directed copies of outgoing motor commands, but the functional relevance of inferred internal copy circuits has remained unclear. One class of spinal interneurons implicated in the control of mammalian forelimb movement, cervical propriospinal neurons (PNs), has the potential to convey an internal copy of premotor signals through dual innervation of forelimb-innervating motor neurons and precerebellar neurons of the lateral reticular nucleus. Here we examine whether the PN internal copy pathway functions in the control of goal-directed reaching. In mice, PNs include a genetically accessible subpopulation of cervical V2a interneurons, and their targeted ablation perturbs reaching while leaving intact other elements of forelimb movement. Moreover, optogenetic activation of the PN internal copy branch recruits a rapid cerebellar feedback loop that modulates forelimb motor neuron activity and severely disrupts reaching kinematics. Our findings implicate V2a PNs as the focus of an internal copy pathway assigned to the rapid updating of motor output during reaching behaviour.

Show MeSH