Spinal premotor interneurons controlling antagonistic muscles are spatially intermingled

Author:

Ronzano Remi1ORCID,Skarlatou Sophie2,Barriga Bianca K34,Bannatyne B Anne5,Bhumbra Gardave Singh6,Foster Joshua D6,Moore Jeffrey D7,Lancelin Camille1,Pocratsky Amanda M1,Özyurt Mustafa Görkem1,Smith Calvin Chad1,Todd Andrew J5ORCID,Maxwell David J5,Murray Andrew J8,Pfaff Samuel L3ORCID,Brownstone Robert M1ORCID,Zampieri Niccolò2ORCID,Beato Marco6ORCID

Affiliation:

1. Department of Neuromuscular Diseases, University College London

2. Max Delbruck Center for Molecular Medicine

3. Gene Expression Laboratory, Salk Institute for Biological Studies

4. Biological Sciences Graduate Program, University of California, San Diego

5. Institute of Neuroscience and Psychology, College of Medical, Veterinary and Life Sciences, University of Glasgow

6. Department of Neuroscience Physiology and Pharmacology, University College London

7. Howard Hughes Medical Institute and Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University

8. Sainsbury Wellcome Centre for Neural Circuits and Behaviour, University College London

Abstract

Elaborate behaviours are produced by tightly controlled flexor-extensor motor neuron activation patterns. Motor neurons are regulated by a network of interneurons within the spinal cord, but the computational processes involved in motor control are not fully understood. The neuroanatomical arrangement of motor and premotor neurons into topographic patterns related to their controlled muscles is thought to facilitate how information is processed by spinal circuits. Rabies retrograde monosynaptic tracing has been used to label premotor interneurons innervating specific motor neuron pools, with previous studies reporting topographic mediolateral positional biases in flexor and extensor premotor interneurons. To more precisely define how premotor interneurons contacting specific motor pools are organized, we used multiple complementary viral-tracing approaches in mice to minimize systematic biases associated with each method. Contrary to expectations, we found that premotor interneurons contacting motor pools controlling flexion and extension of the ankle are highly intermingled rather than segregated into specific domains like motor neurons. Thus, premotor spinal neurons controlling different muscles process motor instructions in the absence of clear spatial patterns among the flexor-extensor circuit components.

Funder

Biotechnology and Biological Sciences Research Council

Leverhulme Trust

Wellcome Trust

Jane Coffin Childs Memorial Fund for Medical Research

Eunice Kennedy Shriver National Institute of Child Health and Human Development

University of California, San Diego

Timken-Sturgis foundation

Salk Institute for Biological Studies

Marguerite Vogt Award

Brain Research UK

Deutsche Forschungsgemeinschaft

Benjamin Lewis Chair in Neuroscience

Sol Goldman Charitable Trust

National Institute of health

National institute of health

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

Reference54 articles.

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