Corticospinal populations broadcast complex motor signals to coordinated spinal and striatal circuits

• Published in: Nature neuroscience Vol. 24; no. 12; pp. 1721 - 1732
• Main Authors: Nelson, Anders, Abdelmesih, Brenda, Costa, Rui M.
• Format: Journal Article
• Language: English
• Published: New York Nature Publishing Group US 01-12-2021; Nature Publishing Group
• Subjects: 14/1; 14/19; 14/34; 14/35; 14/69; 631/378/2632/1323; 631/378/2632/1663; 631/378/2632/1823; 64/60; 9/74; Activity patterns; Animal Genetics and Genomics; Animals; Axon collaterals; Axons - physiology; Behavioral Sciences; Biological Techniques; Biomedical and Life Sciences; Biomedicine; Brain research; Circuits; Corpus Striatum; Cortex (somatosensory); Forebrain; Functional morphology; Human mechanics; Innervation; Mice; Motor cortex; Motor task performance; Movement; Neostriatum; Neural circuitry; Neural networks; Neurobiology; Neurons; Neurons - physiology; Neurosciences; Physiological aspects; Populations; Pyramidal tracts; Pyramidal Tracts - physiology; Spinal cord; Spinal Cord - physiology; United States
• ISSN: 1097-6256; 1546-1726
• DOI: 10.1038/s41593-021-00939-w

Many models of motor control emphasize the role of sensorimotor cortex in movement, principally through the projections that corticospinal neurons (CSNs) make to the spinal cord. Additionally, CSNs possess expansive supraspinal axon collaterals, the functional organization of which is largely unknown. Using anatomical and electrophysiological circuit-mapping techniques in the mouse, we reveal dorsolateral striatum as the preeminent target of CSN collateral innervation. We found that this innervation is biased so that CSNs targeting different striatal pathways show biased targeting of spinal cord circuits. Contrary to more conventional perspectives, CSNs encode not only individual movements, but also information related to the onset and offset of motor sequences. Furthermore, similar activity patterns are broadcast by CSN populations targeting different striatal circuits. Our results reveal a logic of coordinated connectivity between forebrain and spinal circuits, where separate CSN modules broadcast similarly complex information to downstream circuits, suggesting that differences in postsynaptic connectivity dictate motor specificity.
The authors detail principles underlying the innervation of spinal and striatal circuits by populations of corticospinal neurons, and characterize the behavioral information broadcast through this motor control network.