Two inhibitory neuronal classes govern acquisition and recall of spinal sensorimotor adaptation

• Published in: Science Vol. 384; no. 6692; pp. 194 - 201
• Main Authors: Lavaud, Simon, Bichara, Charlotte, D’Andola, Mattia, Yeh, Shu-Hao, Takeoka, Aya
• Format: Journal Article
• Language: English
• Published: United States American Association for the Advancement of Science (AAAS) 12.04.2024; The American Association for the Advancement of Science
• Subjects: Adaptation, Physiological; Animal models; Animals; Circuits; Dorsal horn; Electrophysiology; Genetics; Information processing; Interneurons; Learning; Mental Recall - physiology; Mice; Motor Neurons - physiology; Motor skill; Motor skill learning; Movement; Neural Inhibition; Optics; Renshaw cells; Renshaw Cells - physiology; Sensorimotor system; Spinal cord; Spinal Cord - physiology; Transcription Factors - genetics; Transgenic mice
• ISSN: 0036-8075; 1095-9203; 1095-9203
• DOI: 10.1126/science.adf6801

Spinal circuits are central to movement adaptation, yet the mechanisms within the spinal cord responsible for acquiring and retaining behavior upon experience remain unclear. Using a simple conditioning paradigm, we found that dorsal inhibitory neurons are indispensable for adapting protective limb-withdrawal behavior by regulating the transmission of a specific set of somatosensory information to enhance the saliency of conditioning cues associated with limb position. By contrast, maintaining previously acquired motor adaptation required the ventral inhibitory Renshaw cells. Manipulating Renshaw cells does not affect the adaptation itself but flexibly alters the expression of adaptive behavior. These findings identify a circuit basis involving two distinct populations of spinal inhibitory neurons, which enables lasting sensorimotor adaptation independently from the brain. Motor learning requires the acquisition and retention of motor skills obtained through practice and repetition. The circuits and cell populations in the spinal cord involved in the different steps of motor learning have not been fully elucidated. Using a variety of transgenic mouse models, optogenetics, and electrophysiology, Lavaud et al . identified a population of dorsal horn interneurons in the spinal cord that are necessary for the acquisition of motor learning. A different population of interneurons, Renshaw cells, was critical for retaining and recalling the learned motor skills. The results highlight the contribution of spinal cord circuits in motor learning and memory. Targeting these circuits might have therapeutic value during motor rehabilitation. —Mattia Maroso