Periodic Modulation of Motor-Unit Activity in Extrinsic Hand Muscles During Multidigit Grasping

Abstract

We recently examined the extent to which motor units of digit flexor muscles receive common input during multidigit grasping. This task elicited moderate to strong motor-unit synchrony (common input strength, CIS) across muscles (flexor digitorum profundus, FDP, and flexor pollicis longus, FPL) and across FDP muscle compartments, although the strength of this common input was not uniform across digit pairs. To further characterize the neural mechanisms underlying the control of multidigit grasping, we analyzed the relationship between firing of single motor units from these hand muscles in the frequency domain by computing coherence. We report three primary findings. First, in contrast to what has been reported in intrinsic hand muscles, motor units belonging to different muscles and muscle compartments of extrinsic digit flexors exhibited significant coherence in the 0- to 5- and 5- to 10-Hz frequency ranges and much weaker coherence in the higher 10–20 Hz range (maximum 0.0025 and 0.0008, respectively, pooled across all FDP compartment pairs). Second, the strength and incidence of coherence differed considerably across digit pairs. Third, contrary to what has been reported in the literature, across-muscle coherence can be stronger and more prevalent than within-muscle coherence, as FPL–FDP2 (thumb-index digit pair) exhibited the strongest and most prevalent coherence in our data (0.010 and 43% at 3 Hz, respectively). The heterogeneous organization of common input to these muscles and muscle compartments is discussed in relation to the functional role of individual digit pairs in the coordination of multiple digit forces in grasping.

Neuromuscular mechanisms and neural strategies in the control of time-varying muscle contractions

“…These features are in accord with the concept of a common, frequency-modulated neural input to the MN population (De Luca and Erim 1994;see also DeLuca and Contessa 2012;De Luca and Erim 2002;Farina et al 2013;Farmer et al 1993;Johnston et al 2005Johnston et al , 2009Laine and Bailey 2011;Marsden et al 1999;Rose and Knight 2011;Semmler et al 1997;Winges et al 2008). As indicated by our analyses, the strength of the modulation synchrony is not related to the force level and the frequency of the force variations or, equivalently, to the level and frequency of the oscillatory common input.…”

Limits to the Control of the Human Thumb and Fingers in Flexion and Extension

“…They include the divergence of corticospinal axons to reach more than one motoneuron pool (e.g., Cheney 1978, 1980;Shinoda et al 1981; for review, see Lemon 2008) and the major overlapping and intermingling of cortical output zones to individual upper limb muscles documented in nonhuman primates (e.g., Landgren et al 1962;Rathelot and Strick 2006;Schieber and Hibbard 1993). As a result of such factors, there is short-term synchronization of motor unit discharge of functionally linked hand muscles or across muscle compartments of the multitendoned extrinsic hand muscles (Hockensmith et al 2005;Johnston et al 2005;Nordstrom et al 1992;Reilly et al 2004;Santello and Fuglevand 2004;Winges and Santello 2004). There is also evidence for coherence between cortical activity and forearm EMG (e.g., Baker et al 1997;Brown 2000;Conway et al 1995;Gross et al 2000;Salenius and Hari 2003) and coherent forces across different digits during voluntary tasks (e.g., Kilbreath et al 2002;Li 2002;Rearick and Santello 2002;Santello and Soechting 2000;Yu et al 2007).…”

Muscle-Pair Specific Distribution and Grip-Type Modulation of Neural Common Input to Extrinsic Digit Flexors

“…Motor-unit synchrony is considered to be the result of branched presynaptic input to the motor neurons originating from a common source (Farmer et al 1993;Sears and Stagg 1976;Semmler et al 2002), whereas coherence is thought to reflect the frequency content of the common synaptic input (Farmer et al 1993;Halliday 2000;Rosenberg et al 1998; but see Taylor and Enoka 2004a,b). Significant motor-unit coherence has been observed in the absence of motor-unit synchrony and vice versa (Johnston et al 2005), suggesting that different mechanisms may underlie these two measures of correlated motor-unit activity (Semmler et al 2003).…”

“…We previously reported a heterogeneous organization of common input across motor neurons supplying muscles and muscle compartments of the extrinsic digit flexors during object hold with five digits (Johnston et al 2005;Winges and Santello 2004). Specifically, we found greater motor-unit synchrony and coherence across an extrinsic thumb flexor muscle (m. flexor pollicis longus, FPL) and the index finger compartment of the muscle flexor digitorum profundus (FDP2) than across FPL and FDP3,4 and 5 (middle,ring,and little finger FDP compartments,respectively).…”

“…Specifically, during object hold with two digits, a single digit must counteract thumb forces and torques to prevent object slip, whereas in a five-digit object hold all fingers must be coordinated such that the sum of their forces and torques counteract those exerted by the thumb. The strength and periodicity of common neural input during two-digit object hold was compared with that measured during five-digit grasp (Johnston et al 2005;Winges and Santello 2004).…”