Journal of Neurophysiology, Vol 67, Issue 3 530-546, Copyright © 1992 by APS
Identified proprioceptive afferents and motor rhythm entrainment in the crayfish walking system
R. C. Elson, K. T. Sillar and B. M. Bush
Department of Physiology, School of Veterinary Science, Bristol, United Kingdom.
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 promoter 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: promoter 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.
