Significantly Delayed Medium-Latency Response of the Stretch Reflex in Delayed-Onset Muscle Soreness of the Quadriceps Femoris Muscles Is Indicative of Sensory Neuronal Microdamage

Abstract

Unaccustomed or strenuous eccentric exercise is known to cause delayed-onset muscle soreness. A recent hypothesis postulated that mechano-energetic microinjury of the primary afferent sensory neuron terminals in the muscle spindles, namely a transient Piezo2 channelopathy, could be the critical cause of delayed-onset muscle soreness in the form of a bi-phasic non-contact injury mechanism. This theory includes that this microlesion could delay the medium-latency response of the stretch reflex. Our aim with this study was to investigate this hypothesis. According to our knowledge, no study has examined the effect of delayed-onset muscle soreness on the medium-latency response of the stretch reflex. Our findings demonstrated that a significant delay in the medium-latency stretch reflex could be observed right after a multi-stage fitness test in the quadriceps femoris muscles of Hungarian professional handball players who consequently experienced delayed-onset muscle soreness. The long-latency stretch reflex and most likely short-latency stretch reflex were unaffected by delayed-onset muscle soreness in our study, which is in line with earlier findings. We translate these findings as indicative of proprioceptive Type Ia terminal microdamage in the muscle spindle in line with the aforementioned new acute non-contact compression axonopathy theory of delayed-onset muscles soreness.

Delayed Onset Muscle Soreness and Critical Neural Microdamage-Derived Neuroinflammation

“…Furthermore, Alvarez et al and Bullinger et al showed permanent central synaptic disconnection of proprioceptors from motoneurons after nerve injury, and this phenomenon is associated with the loss of vesicular glutamate transporter (VGLUT) 1/Ia synapses on motoneurons [ 20 , 21 ]. Sonkodi et al suggested that the muscle spindle origin of increased M-wave latency on motoneurons after eccentric exercise-induced muscle damage should not be excluded [ 22 ] and even proposed that the transiently impaired muscle spindle-derived proprioceptors and the resultant synaptic disconnection on motoneurons are responsible for the increased M-wave latency in DOMS, in line with the findings of Vincent, Alvarez and Bullinger et al [ 19 , 20 , 21 , 22 ].…”

“…Finally, Alvarez et al showed that in the case of peripheral nerve injury, the VGLUT1 synapses of Type Ia central terminals are lost permanently on motoneurons, leading to a loss of proprioceptive feedback from the muscle spindles [ 21 ]. Sonkodi et al proposed a similar disruption, however acutely or transiently, in VGLUT1 transmission on motoneurons in DOMS when transient Piezo2 channelopathy is present [ 22 ]. As a result of the lost VGLUT1 synapses, the NMDA receptors at the axonal endings of the same pseudounipolar proprioceptive neurons could be activated, namely, at the presynaptic central terminal on the spinal dorsal horn [ 31 , 60 , 61 ].…”

“…Correspondingly, it has been suggested that Piezo2 could transiently transform from a physiological state to a pathophysiological state in hyperexcited proprioceptive terminals under an induced ASR when unaccustomed or strenuous eccentric contractions should be sustained, which could be the aforementioned “leakiness” to Piezo currents and even to glutamate when it should not be [ 9 ]. Correspondingly, Sonkodi et al suggested that proprioceptive Piezo2 microdamage and the loss of the VGLUT1 connection could involve NMDA receptor activation [ 9 , 22 ].…”

“…The signs of the suggested silent proprioceptive terminal Piezo2 microinjury could be impaired proprioception and transient autonomic disbalance [ 9 , 31 ]. The grounds of proprioceptive impairment were suggested and lately demonstrated to be a minor alteration of the stretch reflex in the affected striated muscles [ 22 , 31 , 53 ]. This impairment is attributed to the aforementioned compromised static phase firing sensory encoding of the stretch reflex [ 22 , 31 , 32 , 53 ].…”

Osteoporosis in Light of a New Mechanism Theory of Delayed Onset Muscle Soreness and Non-Contact Anterior Cruciate Ligament Injury

“…The proprioceptive signalling of MSs and Golgi tendon organs (GTOs) is essential for the non-autonomous morphologic restoration of microfractured bones or remodelling [ 15 , 16 ]. Moreover, it is suggested that the primary transient proprioceptive terminal Piezo2 microinjury concomitant with microfractures impairs the static phase firing encoding of the stretch reflex [ 7 , 10 , 17 , 18 ] and correspondingly, this impairment could be realigned by the dynamic encoding of MSs and GTOs [ 19 , 20 ]. Hence, proprioceptive sensory neurons are proposed to have a role not only in the guidance of growth and regeneration, but also remodelling [ 6 , 9 , 10 ].…”