Identified proprioceptive afferents and motor rhythm entrainment in the crayfish walking system

R. C. Elson*, K. T. Sillar, B. M.H. Bush

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

20 Citations (Scopus)

Abstract

1. In crayfish, Pacifastacus leniusculus, remotion of a walking leg stretches the thoraco-coxal (TC) muscle receptor organ (TCMRO), located at the leg's articulation with the thorax. In vitro, alternate stretch and release of the fourth leg's TCMRO entrained the centrally generated rhythmic motor output to that leg, with the remotor phase of the rhythm entraining to TCMRO stretch, the promotor phase to release. This coordination of motor bursts to afferent input corresponds to that of active, rhythmic movements in vivo. 2. Entrainment was rapid in onset (stable coordination resulting within the first or second stimulus cycle) and was relatively phase-constant (whatever the stimulus frequency, during 1:1 entrainment, remotor bursts began near the onset of stretch and promotor bursts began near the onset of release). Outside the range of 1:1 entrainment, 2:1, 1:2, and 1:3 coordination ratios (rhythm:stimulus) were encountered. Resetting by phasic stimulation of the TCMRO was complete and probabilistic: effective stimuli triggered rapid transitions between the two burst phases. 3. The TCMRO is innervated by two afferents, the nonspiking S and T fibers, which generate graded depolarizing receptor potentials in response to stretch. During proprioceptive entrainment, the more phasic T fiber depolarized and hyperpolarized more rapidly or in advance of the more tonic S fiber. These receptor potentials were modified differently in the two afferents by interaction with central synaptic inputs that were phase-locked to the entrained motor rhythm. 4. Injecting slow sinusoidal current into either afferent alone could entrain motor rhythms: promotor phase bursts were entrained to depolarization of the S fiber or hyperpolarization of the T fiber, whereas the converse response was obtained for remotor phase bursts. 5. During proprioceptive entrainment, tonic hyperpolarization of the S fiber weakened entrained promotor bursts and allowed remotor burst durations to increase. Hyperpolarizing the T fiber weakened entrained remotor bursts and allowed promotor bursts to occur during stretch. These results suggest that the staggered receptor potentials of the two afferents alternately excite opposite burst phases of the rhythm during proprioceptive entrainment. 6. Injecting brief current pulses into either afferent perturbed the timing of entrained bursts in opposite ways, suggesting that, during proprioceptive entrainment, the membrane potential trajectories of the two afferents have reciprocal triggering effects on burst transitions. 7. We infer that entrainment results from 1) complete resetting of burst transitions in a two- phase central oscillator, 2) opposing feedback pathways mediated by a phasic and a tonic afferent, 3) temporally staggered afferent receptor potentials, and 4) the ability of afferent receptor potentials to trigger burst transitions.

Original languageEnglish
Pages (from-to)530-546
Number of pages17
JournalJournal of Neurophysiology
Volume67
Issue number3
DOIs
Publication statusPublished - 1 Mar 1992

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