Physiological tremor increases when skeletal muscle is shortened: implications for fusimotor control

Abstract

The involuntary force fluctuations associated with physiological (as distinct from pathological) tremor are an unavoidable component of human motor control. While the origins of physiological tremor are known to depend on muscle afferentation, it is possible that the mechanical properties of muscle-tendon systems also affect its generation, amplification and maintenance. In this paper, we investigated the dependence of physiological tremor on muscle length in healthy individuals. We measured physiological tremor during tonic, isometric plantarflexion torque at 30% of maximum at three ankle angles. The amplitude of physiological tremor increased as calf muscles shortened in contrast to the stretch reflex whose amplitude decreases as muscle shortens. We used a published closed-loop simulation model of afferented muscle to explore the mechanisms responsible for this behaviour. We demonstrate that changing muscle lengths does not suffice to explain our experimental findings. Rather, the model consistently required the modulation of γ-static fusimotor drive to produce increases in physiological tremor with muscle shortening - while successfully replicating the concomitant reduction in stretch reflex amplitude. This need to control γ-static fusimotor drive explicitly as a function of muscle length has important implications. First, it permits the amplitudes of physiological tremor and stretch reflex to be decoupled. Second, it postulates neuromechanical interactions that require length-dependent γ drive modulation to be independent from α drive to the parent muscle. Lastly, it suggests that physiological tremor can be used as a simple, non-invasive measure of the afferent mechanisms underlying healthy motor function, and their disruption in neurological conditions.

Distribution Heterogeneity of Muscle Spindles Across Skeletal Muscles of Lower Extremities in C57BL/6 Mice

“…Two parts of the pole of regions were rarely equal in the majority of cases, indicating the absence of correlation with the location of the spindle in its muscle. Since the 1980s, the muscle spindle has been assumed to be asymmetrical, although after reconstructing the profile of the muscle spindle and based on morphological research on efferent fibers, the spindle has been accepted to be symmetrical ( Jalaleddini et al, 2017 ). Considering the absence of related research, muscle spindle dissymmetry needs to be further explored.…”

Modulation of spinal circuits following phase-dependent electrical stimulation of afferent pathways

“…Alternatively, the PSD of the 30 s plateau was estimated using Welch's periodogram method. The power of the force exerted corresponding to the frequency band related to the frequency band of the mimicked pathological tremor and physiological tremor was estimated by averaging the PSD in the [3][4][5][6] Hz and [5][6][7][8][9][10][11][12] Hz frequency bands, respectively [34]. The goal of this analysis was to explore the potential effects of the phase-dependent stimulation in the specific frequency bands of motor control related to the stimulation applied and the physiological tremor.…”

Methodological advances for studying gamma motor neurons

“…Only superficial nerves can be recorded, limiting the muscles that can be studied [ 10 ], although recently a group has published methods to record from spindle afferents in the foot during standing [ 34 • ]. Coupling experimental recordings of muscle or spindle afferent activity with computer modeling is a promising approach to test hypotheses about fusimotor control [ 35 • , 36 ]. For instance, EMG recordings of physiological tremor at different muscle lengths were used to determine that shorter muscle lengths were accompanied by larger tremor amplitudes in human subjects.…”

“…For instance, EMG recordings of physiological tremor at different muscle lengths were used to determine that shorter muscle lengths were accompanied by larger tremor amplitudes in human subjects. Using a closed-loop model of an afferented gastrocnemius muscle, increased static γ motor neuron drive was identified as the likely causal factor [ 36 ]. A similar computer model of the proprioceptive circuit was coupled with servo motor control of a cadaver finger to test hypotheses about altering γ motor neuron drive on the stretch reflex using realistic muscle and tendon forces [ 37 , 38 ].…”