Modulation of Human Muscle Spindle Discharge by Arterial Pulsations - Functional Effects and Consequences

Arterial pulsations are known to modulate muscle spindle firing; however, the physiological significance of such synchronised modulation has not been investigated. Unitary recordings were made from 75 human muscle spindle afferents innervating the pretibial muscles. The modulation of muscle spindle discharge by arterial pulsations was evaluated by R-wave triggered averaging and power spectral analysis. We describe various effects arterial pulsations may have on muscle spindle afferent discharge. Afferents could be “driven” by arterial pulsations, e.g., showing no other spontaneous activity than spikes generated with cardiac rhythmicity. Among afferents showing ongoing discharge that was not primarily related to cardiac rhythmicity we illustrate several mechanisms by which individual spikes may become phase-locked. However, in the majority of afferents the discharge rate was modulated by the pulse wave without spikes being phase locked. Then we assessed whether these influences changed in two physiological conditions in which a sustained increase in muscle sympathetic nerve activity was observed without activation of fusimotor neurones: a maximal inspiratory breath-hold, which causes a fall in systolic pressure, and acute muscle pain, which causes an increase in systolic pressure. The majority of primary muscle spindle afferents displayed pulse-wave modulation, but neither apnoea nor pain had any significant effect on the strength of this modulation, suggesting that the physiological noise injected by the arterial pulsations is robust and relatively insensitive to fluctuations in blood pressure. Within the afferent population there was a similar number of muscle spindles that were inhibited and that were excited by the arterial pulse wave, indicating that after signal integration at the population level, arterial pulsations of opposite polarity would cancel each other out. We speculate that with close-to-threshold stimuli the arterial pulsations may serve as an endogenous noise source that may synchronise the sporadic discharge within the afferent population and thus facilitate the detection of weak stimuli

Classification of texture and frictional condition at initial contact by tactile afferent responses

Adjustments to friction are crucial for precision object handling in both humans and robotic manipulators. The aim of this work was to investigate the ability of machine learning to disentangle concurrent stimulus parameters, such as normal force ramp rate, texture and friction, from the responses of tactile afferents at the point of initial contact with the human finger pad. Three textured stimulation surfaces were tested under two frictional conditions each, with a 4 N normal force applied at three ramp rates. During stimulation, the responses of fourteen afferents (5 SA-I, 2 SA-II, 5 FA-I, 2 FA-II) were recorded. A Parzen window classifier was used to classify ramp rate, texture and frictional condition using spike count, first spike latency or peak frequency from each afferent. This is the first study to show that ramp rate, texture and frictional condition could be classified concurrently with over 90% accuracy using a small number of tactile sensory units

Consistent interindividual increases or decreases in muscle sympathetic nerve activity during experimental muscle pain

We recently showed that long-lasting muscle pain, induced by intramuscular infusion of hypertonic saline, evoked two patterns of cardiovascular responses across subjects: one group showed parallel increases in muscle sympathetic nerve activity (MSNA), blood pressure, and heart rate, while the other group showed parallel decreases. Given that MSNA is consistent day to day, we tested the hypothesis that individuals who show increases in MSNA during experimental muscle pain will show consistent responses over time. MSNA was recorded from the peroneal nerve, together with blood pressure and heart rate, during an intramuscular infusion of hypertonic saline causing pain for an hour in 15 subjects on two occasions, 2-27 weeks apart. Pain intensity ratings were not significantly different between the first (5.8 ± 0.4/10) and second (6.1 ± 0.2) recording sessions. While four subjects showed significant decreases in the first session (46.6 ± 9.2 % of baseline) and significant increases in the second (159.6 ± 8.9 %), in 11 subjects, there was consistency in the changes in MSNA over time: either a sustained decrease (55.6 ± 6.8 %, n = 6) or a sustained increase (143.5 ± 6.1 %, n = 5) occurred in both recording sessions. There were no differences in pain ratings between sessions for any subjects. We conclude that the changes in MSNA during long-lasting muscle pain are consistent over time in the majority of individuals, reflecting the importance of studying interindividual differences in physiology

Slowly adapting mechanoreceptors in the borders of the human fingernail encode fingertip forces

There are clusters of slowly adapting (SA) mechanoreceptors in the skin folds bordering the nail. These “SA-IInail” afferents, which constitute nearly one fifth of the tactile afferents innervating the fingertip, possess the general discharge characteristics of slowly adapting type II (SA-II) tactile afferents located elsewhere in the glabrous skin of the human hand. Little is known about the signals in the SA-IInail afferents when the fingertips interact with objects. Here we show that SA-IInail afferents reliably respond to fingertip forces comparable to those arising in everyday manipulations. Using a flat stimulus surface, we applied forces to the finger pad while recording impulse activity in 17 SA-IInail afferents. Ramp-and-hold forces (amplitude 4 N, rate 10 N/s) were applied normal to the skin, and at 10, 20, or 30° from the normal in eight radial directions with reference to the primary site of contact (25 force directions in total). All afferents responded to the force stimuli, and the responsiveness of all but one afferents was broadly tuned to a preferred direction of force. The preferred directions among afferents were distributed all around the angular space, suggesting that the population of SA-IInail afferents could encode force direction. We conclude that signals in the population of SA-IInail afferents terminating in the nail walls contain vectorial information about fingertip forces. The particular tactile features of contacted surfaces would less influence force-related signals in SA-IInail afferents than force-related signals present in afferents terminating in the volar skin areas that directly contact objects

Pulse-wave driven muscle spindles.

<p>Each panel shows post stimulus time histogram at the bottom and raster sweeps of single cardiac cycles on top. <b>A–C</b>, Afferents typically responded with one single spike phase-locked to the cardiac cycle. <b>D–F</b>, Afferents responding with two spikes at the time corresponding to the pulse wave upbeat. A third spike corresponding to the time of dicrotic notch is generated by afferents depicted in <b>E</b> and <b>F</b> (see also <b>B</b>&<b>D</b>). Each bar indicates total count of spikes falling within corresponding 0.02 s time bin. Each dot in raster plot indicates one spike.</p

Muscle spindles in human tibialis anterior encode muscle fascicle length changes

Muscle spindles provide exquisitely sensitive proprioceptive information regarding joint position and movement. Through passively driven length changes in the muscle-tendon unit (MTU), muscle spindles detect joint rotations because of their in-parallel mechanical linkage to muscle fascicles. In human microneurography studies, muscle fascicles are assumed to follow the MTU and, as such, fascicle length is not measured in such studies. However, under certain mechanical conditions compliant structures can act to decouple the fascicles, and therefore the spindles, from the MTU. Such decoupling may reduce the fidelity by which muscle spindles encode joint position and movement. The aim of the present study was to measure, for the first time, both the changes in firing of single muscle spindle afferents and changes in muscle fascicle length in vivo from the tibialis anterior muscle (TA) during passive rotations about the ankle. Unitary recordings were made from 15 muscle spindle afferents supplying TA via a microelectrode inserted into the common peroneal nerve. Ultrasonography was used to measure the length of an individual fascicle of TA. We saw a strong correlation between fascicle length and firing rate during passive ankle rotations of varying rates (0.1-0.5Hz) and amplitudes (1-9°). In particular, we saw responses observed at relatively small changes in muscle length that highlight the sensitivity of the TA muscle to small length changes. This study is the first to measure spindle firing and fascicle dynamics in vivo and provides an experimental basis for further understanding the link between fascicle length, MTU length and spindle firing patterns

Examples of R-wave triggered discharge rate averages in pulse-wave modulated muscle spindles.

<p>Panels on the left (<b>A</b>–<b>E</b>) illustrate five afferents showing positive peak (excitatory response to the upbeat of pulse wave). Panels on the right (<b>F</b>–<b>J</b>) show five afferents displaying an initial negative peak (inhibitory effect). Discharge rate modulation is expressed as % difference from mean discharge rate. Time elapsed after R-wave is shown on the x-axis. Text box indicates the relative amount of variance explained by arterial pulsations (EV). Black thick lines represent averages. Gray thin lines show overlay of individual discharge rate traces in every cardiac cycle.</p

Comparison of R-wave triggered discharge rate averages between different physiological conditions.

<p>Modulation of discharge rate is normalized to the variance in discharge rate over the whole recording and plotted as a function of time, measured from the R-wave of ECG signal. Afferents are grouped according to whether the initial modulatory peak in response to the upbeat of the pulse wave is positive (graphs in left column) or negative (graphs in right column), as revealed by the sign of the eigenvector coefficient (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0035091#pone-0035091-g006" target="_blank">Fig. 6<b>B</b></a>). <b>A</b> & <b>B</b>, changes in discharge rate modulation during inspiratory-capacity apnoea. <b>C</b> & <b>D</b>, changes in discharge rate modulation during muscle pain. <b>E</b> & <b>F</b>, changes in discharge rate modulation during skin pain. <b>G</b> & <b>H</b>, discharge rate modulation during active voluntary contraction.</p