In-parallel and in-series behavior of human muscle spindle endings

D. Burke, A. M. Aniss and S. C. Gandevia Department of Neurology, Prince Henry Hospital, University of New South Wales, Sydney, Australia. 1. The responses of 62 putative muscle spindle afferents innervating the pretibial flexor muscles of normal human subjects were studied during graded twitch contractions of the receptor-bearing muscle to search for possible in-series coupling between spindle endings and motor units. 2. The majority of afferents (n = 57) responded unequivocally in an in-parallel manner to the twitch contractions, regardless of contraction strength. There were two patterns of in-parallel response: afferents without background activity discharged during the relaxation phase of the twitch; afferents with a background discharge were transiently silenced during the contraction phase and resumed their discharge on the relaxation phase. 3. Evidence of in-series coupling was found for five afferents during submaximal twitch contractions, to which each afferent responded in a mixed "biphasic" manner, with increases in discharge during both the contraction and relaxation phases of the twitch. Background discharge, response to stretch, and response during isometric voluntary contractions suggested that four of the afferents innervated primary spindle endings and the fifth a secondary spindle ending. 4. It is argued that the five atypical spindle endings responded in an ambiguous manner during twitch contractions of the receptor-bearing muscle because there was an in-series mechanical coupling between motor units and the spindle. The incidence of demonstrable in-series responses has serious implications for the mechanisms of spindle activation during normal motor behavior, but has only minor implications for the use of the twitch test to identify muscle spindle endings.