Effects of fatigue on synergies in a hierarchical system

Abstract

We investigated the effect of fatigue produced by timed maximal voluntary contraction (MVC) of the index finger of one of the hands on performance in MVC and accurate cyclic force production tasks in right-handed subjects. Based on earlier studies, we hypothesized that fatigue would produce an increase in the indices of force-stabilizing synergies in both hands as well as between the hands in two-hand tasks. Synergies were defined as co-varied adjustments of commands to fingers (modes) across cycles that stabilized total force. Fatigue caused a significant reduction in the MVC of the exercised as well as the non-exercised hand. Indices of finger enslaving (lack of individuation) increased with fatigue in both hands, although the increase was significant in the exercised hand only. In contrast to the significant effects of fatigue on MVC forces performed by the non-exercised hand, there were no comparable transfer effects on the root mean square errors during accurate force production. During one-hand tasks, both hands showed high indices of force-stabilizing synergies. These indices were larger in the left hand. Fatigue led to a general increase in synergy indices. Exercise by the left hand had stronger effects on synergy indices seen in both hands. Exercise by the right hand showed ipsilateral effects only. Smaller effects of fatigue were observed on accuracy of performance of the force-down segments of the force cycles compared to the force-up segments. For the bimanual tasks, synergies were analyzed at two hierarchical levels, two-hand (four-finger) and within-a-hand (two-finger). An increase in the synergy index with fatigue was observed at the lower (two-finger) level of the hierarchy only. We interpret the lack of effects of fatigue at the upper (two-hand) level as a consequence of a trade-off between synergies at different levels of the hierarchy. The differences between the hands are discussed within the dynamic dominance hypothesis.

Introduction

Exercise-induced fatigue impairs the motor function and has detrimental effects on contractile muscle properties (reviewed in Barry and Enoka, 2007, Gandevia, 2001, Gandevia et al., 1996). Despite the changes in the neuromotor apparatus, goal-relevant features of performance by redundant motor systems are relatively preserved during fatigue of one (or a few) of the elements involved in the task (Forestier and Nougier, 1998, Fuller et al., 2009, Gates and Dingwell, 2010, Huffenus et al., 2006, Missenard et al., 2009, Rodacki et al., 2001). Large sets of elements (multiple muscles crossing a joint, multiple joints within an extremity, or multiple extremities) are traditionally viewed as redundant (Bernstein, 1967, Latash, 1996, Turvey, 1990) and posing computational problems for the central nervous system (CNS). Alternatively, they may be viewed as abundant (Gelfand & Latash, 1998) and organized by the neural controller into synergies that ensure stable performance in a variety of motor tasks.

By the term “synergy” we imply neural organizations that ensure co-varied (across trials) adjustments of elemental variables (output variables of individual elements) that reduce variance of an important performance variable produced by all the elements together (reviewed in Latash, 2008, Latash et al., 2007). The framework of the uncontrolled manifold hypothesis (Scholz & Schöner, 1999) has been used to quantify synergies. The UCM hypothesis implies that the central nervous system (CNS) acts in a space of elemental variables, creates in this space a subspace (UCM) corresponding to a desired value of a performance variable, and then limits variance of the elemental variables to that subspace. Variance of elemental variables may be viewed as the sum of two components, “good variance” along the UCM (V_UCM) that does not affect performance, and “bad variance” orthogonal to the UCM (V_ORT) that does. If V_UCM > V_ORT (both variance indices quantified per degree-of-freedom), a conclusion is drawn that a synergy stabilizes the performance variable. If V_UCM ⩽ V_ORT, we conclude that there is no synergy stabilizing the performance variable. The relative difference (ΔV) between V_UCM and V_ORT has been used as a quantitative index of synergy. Our previous studies of exercise-induced fatigue have shown an increase in the index of synergy for accurate multi-digit force production tasks as well as in multi-muscle postural tasks (Park et al., 2012, Singh and Latash, 2011, Singh et al., 2010a, Singh et al., 2010b).

Our earlier studies of the effects of fatigue on multi-finger synergies were limited to performance by the dominant arm. It has been shown, however, that the two arms are specialized for different aspects of coordinated behavior (Sainburg, 2002, Wang and Sainburg, 2007). The dynamic dominance hypothesis (Sainburg, 2005) states that the dominant arm is specialized for trajectory control while the non-dominant hand is better for the control of postural states. In the current study, the main task involved sinusoidal rhythmic force production and, hence, our first hypothesis was that, in the right-handers, the right hand would have higher indices of force stabilizing synergy than the left hand.

The previous studies have shown an increase in the index of force-stabilizing synergy for the exercised limb (Singh et al., 2010a, Singh et al., 2010b) but whether these effects transfer to the non-exercised limb is unknown. Several studies have documented fatigue-induced decline in the maximal voluntary contraction force (MVC) (Martin and Rattey, 2007, Rattey et al., 2006, Todd et al., 2003, Zijdewind et al., 1998) and increased motor-unit synchronization (Boonstra et al., 2007, Boonstra et al., 2008) not only within the exercised limb but also in the non-exercised limb. Thus, our second hypothesis was that the non-exercised hand would show effects on the two variance components (V_UCM and V_ORT) and synergy index (ΔV) similar to those in the exercised hand, but possibly of smaller magnitude.

Bimanual tasks have been viewed as being controlled in a hierarchical fashion (Dounskaia et al., 2005; Gorniak et al., 2007a, Gorniak et al., 2007b; Tseng, Scholz, & Galloway, 2009). At the upper level of the hierarchy the task is distributed between the two arms, while at the lower level the action of each arm is distributed amongst the elements (joints or digits). A trade-off between synergy indices at different levels within a hierarchically organized system has been demonstrated (Gorniak et al., 2007a, Gorniak et al., 2009): There were strong force-stabilizing synergies at the higher level of the hierarchy (between-hands) but not at the lower level (within-a-hand). Hence, we expected to see force-stabilizing synergies between the hands (ΔV > 0) but not within-a-hand (ΔV < 0) in two-hand tasks. We also investigated whether adjustments of multi-digit synergies to fatigue of a single finger were seen at both within-a-hand and between-hands levels. We hypothesized that during fatigue synergy indices would show an increase at both levels of the hierarchy.