Encoding of limb state by single neurons in the cuneate nucleus of awake monkeys

• Published in: Journal of neurophysiology Vol. 126; no. 2; pp. 693 - 706
• Main Authors: Versteeg, Christopher, Rosenow, Joshua M., Bensmaia, Sliman J., Miller, Lee E.
• Format: Journal Article
• Language: English
• Published: United States American Physiological Society 01.08.2021
• Series: Sensory Processing
• Subjects: Animals; Extremities - innervation; Extremities - physiology; Female; Macaca mulatta; Male; Medulla Oblongata - cytology; Medulla Oblongata - physiology; Muscle, Skeletal - innervation; Muscle, Skeletal - physiology; Neurons - physiology; Proprioception; Wakefulness; reaching; sensory gain modulation; monkey; cuneate nucleus; proprioception
• ISSN: 0022-3077; 1522-1598; 1522-1598
• DOI: 10.1152/jn.00568.2020

The cuneate nucleus (CN) is the somatosensory gateway into the brain, and only recently has it been possible to record these signals from an awake animal. We recorded single CN neurons in monkeys. Proprioceptive CN neurons appear to receive input from very few muscles, and their sensitivity to movement changes reliably during reaching relative to passive arm perturbations. Sensitivity is generally increased, but not exclusively so, as though CN “spotlights” critical proprioceptive information during reaching. The cuneate nucleus (CN) is among the first sites along the neuraxis where proprioceptive signals can be integrated, transformed, and modulated. The objective of the study was to characterize the proprioceptive representations in CN. To this end, we recorded from single CN neurons in three monkeys during active reaching and passive limb perturbation. We found that many neurons exhibited responses that were tuned approximately sinusoidally to limb movement direction, as has been found for other sensorimotor neurons. The distribution of their preferred directions (PDs) was highly nonuniform and resembled that of muscle spindles within individual muscles, suggesting that CN neurons typically receive inputs from only a single muscle. We also found that the responses of proprioceptive CN neurons tended to be modestly amplified during active reaching movements compared to passive limb perturbations, in contrast to cutaneous CN neurons whose responses were not systematically different in the active and passive conditions. Somatosensory signals thus seem to be subject to a “spotlighting” of relevant sensory information rather than uniform suppression as has been suggested previously. NEW & NOTEWORTHY The cuneate nucleus (CN) is the somatosensory gateway into the brain, and only recently has it been possible to record these signals from an awake animal. We recorded single CN neurons in monkeys. Proprioceptive CN neurons appear to receive input from very few muscles, and their sensitivity to movement changes reliably during reaching relative to passive arm perturbations. Sensitivity is generally increased, but not exclusively so, as though CN “spotlights” critical proprioceptive information during reaching.