Skeletal muscle function underpins muscle spindle abundance

Abstract

Muscle spindle abundance is highly variable within and across species, but we currently lack any clear picture of the mechanistic causes or consequences of this variation. Previous use of spindle abundance as a correlate for muscle function implies a mechanical underpinning to this variation, but these ideas have not been tested. Herein, we use integrated medical imaging and subject-specific musculoskeletal models to investigate the relationship between spindle abundance, muscle architecture and in vivo muscle behaviour in the human locomotor system. These analyses indicate that muscle spindle number is tightly correlated with muscle fascicle length, absolute fascicle length change, velocity of fibre lengthening and active muscle forces during walking. Novel correlations between functional indices and spindle abundance are also recovered, where muscles with a high abundance predominantly function as springs, compared to those with a lower abundance mostly functioning as brakes during walking. These data demonstrate that muscle fibre length, lengthening velocity and fibre force are key physiological signals to the central nervous system and its modulation of locomotion, and that muscle spindle abundance may be tightly correlated to how a muscle generates work. These insights may be combined with neuromechanics and robotic studies of motor control to help further tease apart the functional drivers of muscle spindle composition.

The association between muscle architecture and muscle spindle abundance

“…Instead, any inference of spindle provision should be based on a suitably transformed linear relationship 12 . Subsequently, the residual value of the linear regression of the log-transformed spindle number and muscle mass as an unbiased measure has become the prevailing descriptor of spindle abundance 10 , 11 , 13 . Residual values are homogenously distributed, allow for back-transformation calculations of spindle number, and provide the most unbiased comparative measure of relative spindle abundance 10 , 11 .…”

Not solely a motor: the role of muscles in sensory mechanisms and integrative control

“…The model analysis included a total of 23 individual muscles, spanning a range of estimated muscle spindle abundance. The authors found that the absolute number of muscle spindles was related to muscle fibre length, and predictive of total muscle length, its velocity profile, and to a certain extent to the force-generating capacity of muscles during walking [2]. Their findings suggest an intriguing correlation between muscle mechanical roles and spindle abundance.…”

“…The findings from Kissane et al . [2] suggest an important hypothesis about the relationship between a muscle's mechanics and spindle sensory organ abundance and highlight the importance of considering the relationships between muscle sensing and mechanics.…”

“…The study by Kissane et al . [2] estimated muscle spindle abundance because this could not be measured directly. Additionally, they focused solely on steady-state walking, which allows the simulation of muscle–tendon dynamics based upon non-invasive measures of anatomy and movement dynamics.…”

“…Versatile switching among mechanical roles requires precisely timed modulation of neural control, yet a large gap remains in understanding how sensing and control dynamics are integrated to achieve mechanical function. The findings from Kissane et al [2] suggest an important hypothesis about the relationship between a muscle's mechanics and spindle sensory organ abundance and highlight the importance of considering the relationships between muscle sensing and mechanics.…”