Transmission Security for Single Kinesthetic Afferent Fibers of Joint Origin and Their Target Cuneate Neurons in the Cat

Transmission between single identified, kinesthetic afferent fibers of joint origin and their central target neurons of the cuneate nucleus was examined in anesthetized cats by means of paired electrophysiological recording. Fifty-three wrist joint afferent-cuneate neuron pairs were isolated in which the single joint afferent fiber exerted suprathreshold excitatory actions on the target cuneate neuron. For each pair, the minimum kinesthetic input, a single spike, was sufficient to generate cuneate spike output, often amplified as a pair or burst of spikes, particularly at input rates up to 50-100 impulses per second. The high security was confirmed quantitatively by construction of stimulus-response relationships and calculation of transmission security measures in response to both static and dynamic vibrokinesthetic disturbances applied to the joint capsule. Graded stimulus-response relationships demonstrated that the output for this synaptic connection between single joint afferents and cuneate neurons could provide a sensitive indicator of the strength of joint capsule stimuli. The transmission security measures, calculated as the proportion of joint afferent spikes that generated cuneate spike output, were high (>85-90%) even at afferent fiber discharge rates up to 100-200 impulses per second. Furthermore, tight phase locking in the cuneate responses to vibratory stimulation of the joint capsule demonstrated that the synaptic linkage preserved, with a high level of fidelity, the temporal information about dynamic kinesthetic perturbations that affected the joint. The present study establishes that single kinesthetic afferents of joint origin display a capacity similar to that of tactile afferent fibers for exerting potent synaptic actions on central target neurons of the major ascending kinesthetic sensory pathway.