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

Abstract

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.

Active information sampling varies across the cardiac cycle

“…Formulated in terms of the interoceptive predictive coding framework (Barrett & Simmons, 2015;Seth, 2013), which extends the free-energy principle (Friston, 2010) to interoceptive processes and connects them to consciousness and emotion, this periodic-and thus predictable-ascending baroreceptor input to central structures is anticipatorily cancelled out by top-down interoceptive predictions, thereby minimizing its influence on perception (Critchley & Garfinkel, 2018;Salomon et al, 2016). Besides modulating arterial baroreceptor discharge, heartbeat-related pressure fluctuations generate periodic sensory influences throughout the body-affecting, for example, the discharge of tactile (Macefield, 2003) or muscle spindle afferents (Birznieks, Boonstra, & Macefield, 2012)-which are predicted and normally do not enter perceptual awareness. In our constant attempt to minimize sensory uncertainty (Peters, McEwen, & Friston, 2017), inhibition of such predictable cardiac-induced sensory effects has been argued to reducepotentially distracting-self-related sensory noise (Salomon et al, 2016) at the benefit of our processing of the outside world, for example, by increasing the signal-to-noise ratio of external stimuli.…”

Active sampling in visual search is coupled to the cardiac cycle

“…In addition, as they also suggested a more parsimonious explanation: cardioballistic fluctuations of the ejected blood may 13 exert a direct effect in the muscle activity (Fallon, 2004). Interestingly, the afferent discharge of muscle spindles is modulated by arterial pulsations (Birznieks, Boonstra, & Macefield, 2012)…”

Visceral Signals Shape Brain Dynamics and Cognition

“…In addition to cardiac and blood vessel receptors, the occurrence of cardiac contractions is also signaled through other, less well known pathways. The pulse modulates the neural activity of tactile [53] and proprioceptive [54,55] receptors, showing that information about cardiac activity is already present at the most peripheral level in the somatosensory modality. Another intriguing possibility is direct vasculoneuronal coupling in the CNS [56], an effect recently observed in rodent slices [57], where a change in pressure in the vessels modulates neural firing.…”

“…Why does baroreceptor activation sometimes facilitate stimulus processing, as for somatosensory detection or threat, and sometimes inhibit it, as for pain? Should all results be interpreted as reflecting baroreceptor activation, or does pulse-related information mediated by tactile [53] and proprioceptive [54,55] receptors also play a role, with potentially a direct influence on muscle activity?…”