Neuronal responses of medullary relay cells to controlled stretches of forearm muscles in the monkey

Abstract

Single units were recorded extracellularly from the external cuneate nucleus and from the main cuneate nucleus in anesthetized monkeys. The aim was to study the properties of the subpopulation of neurones which transmit “deep” (proprioceptive) information to the thalamus and the cerebral cortex, and to compare the results with previous studies in neurones of the higher “proprioceptive” centres. The neurones were characterized according to their location, their projection to the thalamus and the cerebellum, and their sensitivity to controlled displacements of the extensor digitorum communis muscle. Forty-nine neurones were allocated to the main cuneate nucleus. They occupied the pars triangularis which surrounds the pars rotunda laterally and ventrally. Fifty-six units were classified as external cuneate neurones. Among the external cuneate neurones, 14 neurones were excited antidromically by cerebellar and 8 neurones by thalamic stimulation; two further units responded antidromically to both cerebellar and thalamic stimulation. This observation is in agreement with previous anatomical evidence that part of the external cuneate neurones project to the ventrobasal complex of the thalamus. Possibly, some of these neurones may have bifurcating axons projecting to both targets. More than half of the main cuneate neurones were antidromically excited from the thalamus; three units were backfired from the cerebellum and two units were backfired from both targets. With controlled longitudinal displacements of the extensor digitorum communis tendon, the response patterns of the proprioceptive neurones were similar in both nuclei. Evidence is presented that part of the synaptic effects are likely to be mediated by group I afferents (responses to stretch amplitudes of less than 50 μm and to electrical stimulation of the muscle nerve at intensities below twitch threshold, dynamic response patterns to small amplitude vibratory stimuli). Most units which were responding to stretches of the extensor digitorum communis muscle did not respond when other tendons of the forearm were pulled. Only 15 out of 54 neurones tested exhibited a possible convergence. This was confined to a few neighbouring muscles (extensors and flexors) and only two of these had also cutaneous receptive fields. It cannot be excluded, however, that some of these responses were due to physical spread of the mechanical stimulus. Comparison with previous similar studies on neurones of the brainstem nuclei of cats revealed striking similarities of the neural properties in the two species. The present findings were also very similar to those obtained, with the same techniques, in the proprioceptive relay of the thalamus and in cortical area 3a. This suggests that the transmission in the ascending proprioceptive system occurs with little modulation and with high synaptic efficacy, providing the cerebral cortex with precise, musculotopic information about small changes of muscle length.