Tonic muscle pain does not increase fusimotor drive to human leg muscles: implications for chronic muscle pain

Abstract

New Findings r What is the central question of this study?Based on data obtained from experimental animals, muscle pain is believed to cause a reflex activation of fusimotor neurones and thereby increase the sensitivity of muscle spindles to stretch. Using a model of long-lasting muscle pain, we asked the question: does tonic muscle pain increase the resting discharge of muscle spindles in human subjects? r What is the main finding and its importance?Microelectrode recordings from single muscle spindle afferents revealed no net change in the discharge of spontaneously active spindle endings during moderate-strong pain lasting ∼1 h. We conclude that, unlike the situation in anaesthetized animals, muscle pain does not cause a reflex increase in fusimotor drive and spindle discharge.Experimental pain induced in animals has shown that noxious stimulation of group III and IV afferents increases the firing of muscle spindles via a reflex excitation of fusimotor (γ) motoneurones. Chronic muscle pain has been hypothesized to develop as a result of a vicious cycle involving this mechanism. In order to explore the effects of long-lasting muscle pain on the fusimotor system, single unit muscle spindle afferents were recorded from 15 subjects. Afferent activity was recorded from foot and ankle extensor muscles whilst infusing hypertonic saline into the tibialis anterior muscle of the ipsilateral leg, producing moderate-strong pain lasting for ∼60 min. A change in fusimotor drive was inferred by observing changes in the mean discharge rate of spontaneously active muscle spindle afferents. Homonymous and heteronymous muscles remained relaxed and showed no increase in activity, arguing against any fusimotor-driven increase in motor activity, and there was no net change in the firing of muscle spindle afferents. We conclude that long-lasting stimulation of group III and IV afferents fails to excite fusimotor neurones and increase muscle spindle discharge. Accordingly, the vicious cycle theory has no functional basis for the development of myalgia in human subjects.

Lower hamstring extensibility in men compared to women is explained by differences in stretch tolerance

“…The physiological link between pain and increased spindle output has also been questioned. Recent evidence using experimentally induced muscle pain reported that muscle spindle output was not increased, suggesting that stimulation of group III and IV afferents fails to excite fusimotor neurons and increase muscle spindle discharge [31]. Therefore the causation for termination of the test and thus the relationship between pain and extensibility, evident only in men, is probably mediated by behavioural interpretation of the pain elicited during stretch.…”

Sensing the body in chronic pain: A review of psychophysical studies implicating altered body representation

“…Indeed, there is evidence that large-diameter afferents are responsible for the pain commonly experienced after exercise, implicating access to the pain pathway by spindle afferents (Weerakkody et al, 2001(Weerakkody et al, , 2003b. However, recordings of afferents in healthy human subjects during stimulation of group III and IV afferents, via hypertonic saline, does not alter fusimotor excitability or muscle spindle discharge (Birznieks et al, 2008;Fazalbhoy et al, 2013). In light of such observations, the associated changes in chronic pain patients regarding proprioception more likely involves upstream disturbances, such as the neural processing of proprioceptive signals (Brumagne et al, 2004;Popa et al, 2007;McCabe and Blake, 2008).…”

Functional properties of human muscle spindles

“…A model for chronic musculoskeletal pain syndromes was established in anesthetized animals based on the reflex activation of fusimotor neurons by nociceptor response (Johansson and Sojka 1991). Unfortunately, following the same trend as other candidates for independent control, when this potential reflex excitation of fusimotor drive was investigated in awake human subjects, during the deep pain produced by injection or infusion of hypertonic saline into the tibialis anterior muscle, no net change in the spindle firing was seen (Birznieks et al 2008;Fazalbhoy et al 2013).…”