Receptor potentials of isolated frog muscle spindle evoked by sinusoidal stimulation

Abstract

Receptor potentials in response to sinusoidal stimulation have been recorded from isolated muscle spindles of the frog. Sinusoidal displacements of different amplitudes (20-120 micron) and frequencies (0.1-100 Hz) were used. The mean static stretch level was adjusted between resting length (L0) and L0 + 400 micron, so that the amplitude and phase-response characteristics were measured at different operating points. Depending on the amount of static prestretch, there is a well-defined dynamic range, which limits the receptor potential by nonlinear compression of either its positive or negative half-cycle. For each point on the static operating curve there exists a dynamic operating curve with a sigmoidal shape. The range of each dynamic curve is approximately 80 micron, independent of the static displacement, and the maxima of all dynamic curves are the same. Therefore the dynamic curves are not symmetrical about their static operating point. The slope of the steepest portion is 10% of the maximum elicitable receptor potential per 10-micron dynamic displacement. For stimulus frequencies greater than 2 Hz the receptor potential deviates from a sinusoidal waveform, exhibiting a fast depolarization transient during stretch and a prolonged repolarization transient during release of stretch. The steepness of the depolarization transient increases with increasing stimulus frequency, amplitude, and prestretch level. As a result, the interval from trough to peak of the receptor potential shortens to less than 90 degrees instead of half a cycle. The repolarization transient has an exponential decay with a time constant of approximately 40 ms that remains constant during the various stimulus conditions. As a result of this slow decay time, individual receptor potentials summate, so that the response divides into a modulated receptor potential (AC component) and a maintained depolarization (DC component). The amplitude response characteristic of the stationary AC component increases with increasing stimulus frequencies up to a peak at 2 Hz, after which it declines with a slope of -3 dB/octave. Provided large sinusoidal stretches and/or extended prestretch levels are used, this high-frequency decline of the AC component is compensated for by the proportional increase of the DC component, so that the peak depolarization values remain constant from 2 to 100 Hz. Stimulus and response are in phase for stimulus frequencies less than 2 Hz and reverse to phase lag at higher stimulus frequencies.(ABSTRACT TRUNCATED AT 400 WORDS)

Dendritic excitability and localization of GABA‐mediated inhibition in spider mechanoreceptor neurons

“…Although this difference was not statistically significant it is important because, if the action potentials had propagated antidromically from the soma to the dendrite, the dendritic delay would have been longer. Evidence for dendritic excitability has also been provided from insect mechanosensory neurons (Guillet et al ., 1980; Erler & Thurm, 1981; Field & Matheson, 1998), mammalian Pacinian corpuscles (Pawson & Bolanowski, 2002) and muscle spindles (Querfurth, 1985). Initiation of action potentials in the dendrite presumably allows fast detection of rapidly occurring mechanical stimuli, such as vibration.…”

Active Signal Conduction through the Sensory Dendrite of a Spider Mechanoreceptor Neuron

“…In the Pacinian corpuscle, action potentials are assumed to arise at the first node of Ranvier within the corpuscle (Diamond et al, 1956;Loewenstein, 1971), but there is also evidence that voltage-activated sodium channels, and regenerative activity, occur earlier in the sensory neurite (Pawson and Bolanowski, 2002). Action potentials are also thought to start at the first node of Ranvier in muscle spindles, but there is evidence of regenerative processes in the sensory dendrites (Querfurth, 1985). In crustacean stretch receptors, transduction occurs at dendrite tips, electrically distant from the soma, but there is evidence of active currents in the dendrites that contribute to the receptor potential (Swerup and Rydqvist, 1992).…”

Action‐potential initiation and maintained activity of the isolated frog muscle spindle

“…There was no reset to the resting membrane potential, and during the entire hyperpolarizing afterpotential, the receptor was still capable of processing external stimuli (Querfurth, 1985b). (2) Even large stimulus‐evoked receptor potentials were considerably smaller than the resting receptor potential (Querfurth, 1985a, 1986a), so that the stimulus‐evoked receptor potential just controlled the resting receptor potential. (3) The resting receptor potential provided a powerful enhancement of the transducer signal and therefore increased the sensitivity of the receptor organ: even small receptor potentials in response to subtle mechanical disturbances provoked suprathreshold excitation, which would have failed if the receptor potential started from the far lower voltage of the resting membrane potential.…”

“…Likewise, small subthreshold depolarizations have been recorded in the isolated muscle spindle preparation in response to stimulus‐evoked receptor potentials that just reached the threshold condition (Querfurth, 1986b). (v) Because small subthreshold depolarizations as well as local responses and action potentials were blocked by procain (Katz, 1950b; Stämpfli, 1952) or tetrodotoxin (Querfurth, 1985a, 1986a), one might conclude that these potentials were generated by the same fast sodium channel. (vi) The small subthreshold depolarizations differ from the transducer responses because the stimulus‐evoked receptor potentials have been shown to be unaffected by procain or tetrodotoxin (Ottoson & Shepherd, 1971).…”

“…Methods and experimental procedures are described elsewhere (Querfurth, 1985a, b). Briefly, the muscle spindle receptor was isolated from M. extensor digitorum longus IV of Rana esculenta immediately after decapitation (according to the Directive 86/609EEC) and consisted of the encapsulated sensory region together with the afferent nerve.…”