Synergistic muscle activation impacts muscle spindles projecting to mouse trigeminal mesencephalic nucleus

Muscle spindles (MSs) are essential for conveying sensory information about changes in muscle fiber lengths. Epimuscular myofascial force transmission (EMFT) occurs through mechanical connections between muscular and connective tissues and yields strain variability along muscle fibers. As those connective tissues also surround the MSs, EMFT effects imply a direct interaction of motor action and mechanoreceptor response. However, the sensory implications of EMFT remain poorly understood, limiting our understanding of muscle control. We investigated the impact of synergistic muscle activity on MS feedback by recording neuronal activity from the trigeminal mesencephalic nucleus (Me5) in mice. Using a modernized protocol, we applied mechanical stimuli to identify MS afferents while preserving epimuscular connections between mastication muscles. For the first time in vivo, we identified MS afferents from the masseter and temporalis muscles projecting to Me5 in mice using electrophysiological recordings, partly confirmed by histological analysis. Their firing properties were comparable to those in larger animals. We then assessed how MSs respond to local length changes induced by intramuscular electrical stimulation of a synergistic muscle. Our results showed that activating the temporalis muscle significantly influenced MS activity in the masseter MSs (n = 44), while activating the masseter led to a non-significant change in the firing rate of temporalis MSs (n = 7). The findings suggest that synergistic muscle activity impacts MS feedback through a combination of neural and mechanical mechanisms, with mechanical factors likely dominant. We conclude that EMFT contributes to sensorimotor integration, making synergistic muscle activity an important determinant for MS feedback.