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Clarke's column neurons as the focus of a corticospinal corollary circuit

Nature Neuroscience volume 13, pages 1233–1239 (2010)Cite this article

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Abstract

Proprioceptive sensory signals inform the CNS of the consequences of motor acts, but effective motor planning involves internal neural systems capable of anticipating actual sensory feedback. Just where and how predictive systems exert their influence remains poorly understood. We explored the possibility that spinocerebellar neurons that convey proprioceptive sensory information also integrate information from cortical command systems. Analysis of the circuitry and physiology of identified dorsal spinocerebellar tract neurons in mouse spinal cord revealed distinct populations of Clarke's column neurons that received direct excitatory and/or indirect inhibitory inputs from descending corticospinal axons. The convergence of these descending inhibitory and excitatory inputs to Clarke's column neurons established local spinal circuits with the capacity to mark or modulate incoming proprioceptive input. Together, our genetic, anatomical and physiological results indicate that Clarke's column spinocerebellar neurons nucleate local spinal corollary circuits that are relevant to motor planning and evaluation.

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Figure 1: Anatomic and genetic characterization of postnatal mouse dSC neurons.
Figure 2: Anatomy of proprioceptive inputs to dSC neurons.
Figure 3: Physiology of proprioceptive and cortical inputs to dSC neurons.
Figure 4: Anatomy of cortical inputs to dSC neurons.
Figure 5: Anatomy of cortically evoked inhibition of dSC neurons.
Figure 6: Physiology of cortically evoked inhibition of dSC neurons.
Figure 7: Cortical inhibition of sensory-evoked responses in dSC neurons.

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Acknowledgements

We thank B. Han and K. Miao for technical assistance, J. de Nooij and G. Sürmeli for help in retrograde labeling of proprioceptive afferents, J. Kirkland and M. Mendelsohn for animal care, and K. MacArthur and I. Schieren for help in preparing the manuscript. We are grateful to S. Arber, N. Asai, C. Cebrian, Z.J. Huang, J. Milbrandt, J. Sanes, G. Szabo and MMRCC-GENSAT for mouse lines, and especially to F. Costantini for permission to use unpublished Gdnf∷CreERT2 mice. We thank R. Axel, M. Churchland, K. Franks, S. Grillner, J. Krakauer, C. Miall, S. Poliak, K. Ritola, D. Stettler and D. Wolpert for discussion and/or comments on the manuscript. A.W.H. was supported by the Howard Hughes Medical Institute and the Robert Leet and Clara Guthrie Patterson Trust Fellowship. T.M.J. was supported by grants from the National Institute of Neurological Disorders and Stroke, the Wellcome Trust, the G. Harold and Leila Y. Mathers Foundation, Project A.L.S. and is an investigator of the Howard Hughes Medical Institute.

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  1. Departments of Neuroscience and Biochemistry and Molecular Biophysics, Howard Hughes Medical Institute, Kavli Institute for Brain Science, Columbia University, New York, New York, USA

    Adam W Hantman & Thomas M Jessell

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  1. Adam W Hantman
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Contributions

A.W.H. and T.M.J. conceived of the project and planned the experiments. A.W.H. performed the experiments. A.W.H. and T.M.J. analyzed the data and wrote the manuscript.

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Correspondence to Thomas M Jessell.

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Supplementary Text and Figures

Supplementary Figures 2–6 and Supplementary Results (PDF 7077 kb)

Supplementary Figure 1

Distribution of corticospinal terminals on dSC neurons. (PPT 26901 kb)

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Hantman, A., Jessell, T. Clarke's column neurons as the focus of a corticospinal corollary circuit. Nat Neurosci 13, 1233–1239 (2010). https://doi.org/10.1038/nn.2637

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