From Single Motor Unit Activity to Multiple Grip Forces: Mini-review of Multi-digit Grasping1

Integrative and Comparative Biology, Sep 2005 by Winges, Sara A, Santello, Marco

SYNOPSIS.

This paper is a mini review of kinetic and kinematic evidence on the control of the hand with emphasis on grasping. It is not meant to be an exhaustive review, rather it summarizes current research examining the mechanisms through which specific patterns of coordination are elicited and observed during reach to grasp movements and static grasping. These coordination patterns include the spatial and temporal covariation of the rotation at multiple joints during reach to grasp movements. A basic coordination between grip forces produced by multiple digits also occurs during whole hand grasping such that normal forces tend to be produced in a synchronous fashion across pairs of digits. Finally, we address current research that suggests that motor unit synchrony across hand muscles and muscle compartments might be one of the neural mechanisms underlying the control of grasping.

INTRODUCTION

Grasping with the entire hand requires coordination among multiple joints and muscles. The control required to produce a successful grasp may be complex due to the large number of muscle and joints involved. When an object is grasped and held against gravity, the control becomes more complex in order to hold the object against gravity and prevent slippage. The question arises as to what strategies the central nervous system (CNS) uses to control the large number of degrees of freedom of the hand, i.e., muscles, joints. The mechanism(s) through which this control may act is not yet well understood. This mini review examines research that has addressed this question using tasks requiring the control of individual and multiple digits. A more extensive review has recently been published (Schieber and Santello, 2004).

PATTERNS OF COORDINATION IN GRASPING

Kinematics

The temporal coordination of joint motion has been studied extensively during reach to grasp tasks. The maximum opening of the hand occurs at hand peak velocity and is linearly related to object size (Connolly and Goodale, 1999; Jeannerod, 1981, 1984). During the reach to grasp objects of different shapes, the whole hand is shaped in a continuous fashion during the reach as a function of object geometry (Santello and Soechting, 1998; Santello et al., 1998, 2002; Winges et al., 2003). This behavior is characterized by consistent covariations in the angular excursion of the metacarpal and proximal interphalangeal joints (Santello et al., 1998, 2002). Principal components analysis of hand kinematics revealed the existence of a few coordination patterns describing the pre-shaping of the entire hand during the reach. The first pattern consisted of a common extension and flexion of the joints, which determined the maximum hand opening, while the second pattern was related to finger span near the end of the reach. Additionally, these patterns of pre-shaping of the hand to object shape occur without the need for continuous visual feedback (Santello et al., 2002; Schettino et al., 2003; Winges et al., 2003). These consistent kinematic patterns are the net result of biomechanical constraints (e.g., flexor and extensor muscles crossing several joints) and neural control (e.g., muscle activation patterns; see below).

Kinetics

The magnitude of normal forces produced by each digit used to grasp and hold an object varies with the object's weight and center of mass position and are dependent on surface texture (Edin et al., 1992; Santello and Soechting, 2000; Zatsiorsky et al., 2002). In any static grasping task, the sum of the forces and moments applied to the object must be equal to zero (Jenmalm and Johansson, 1997). In a two-digit precision grip task, this requires a symmetrical partition of grip (normal) forces between the thumb and one of the fingers involved in the grasp. When additional fingers are used to oppose the thumb force, i.e., three to five digit grasp, the total force produced by the fingers must equal that of the thumb. How the total force exerted by all fingers is shared among each finger (i.e., force sharing pattern), however, is indeterminate (Santello and Soechting, 2000). Nevertheless, when subjects lift and hold an object with five digits, a characteristic force-sharing pattern typically emerges where the index finger produces the largest amount of force followed by the middle, ring and little fingers (Santello and Soechting, 2000). This pattern is established early in the lift (Rearick and Santello, 2002; Reilmann et al., 2001), is modulated according to the object's center of mass also when this is not predictable on a trial-to-trial basis, and is preserved when grasping is performed by the non-preferred hand (Rearick et al., 2003; Salimi et al., 2000). Although general patterns of grip force magnitude exist based on object properties during multi-digit grasping, the grip forces exerted by each digit tend to fluctuate and must be controlled and coordinated in the temporal domain.

In everyday grasping the normal forces produced by each digit are selected based on the properties of the object and the context in which the grasp is taking place. When the entire hand is used to grasp an object the magnitude and temporal relationship between the forces must be adjusted to prevent object slip and maintain its desired position in space. Recent studies have demonstrated that a default strategy may exist where forces between pairs of digits are produced in a synchronous fashion while holding an object against gravity (Santello and Soechting, 2000; Rearick and Santello, 2002; Rearick, et al., 2003). This observation appears to be independent of the amount of force produced by a finger, i.e., force scaling due to changes in the center of mass position (Santello and Soechting, 2000) and the predictability of changes in center of mass as well as handedness (Rearick and Santello, 2002). This consistent tendency of forces to be produced synchronously appears to be specific to grasping and holding an object against gravity. When subjects are asked to produce the same total force without lifting the object, the tendency of forces to be produced synchronously is dramatically reduced (Rearick et al., 2003). These results suggest that the production of synchronous grip forces may serve a functional purpose such as acting as a safety mechanism to ensure grasp stability, i.e., to prevent object slip. This finding also suggests that the central nervous system uses task specific control strategies to coordinate multiple grip forces. One way in which the central nervous system may elicit this behavior is through common neural input to multiple motoneuron pools (see below).