Coupling between reaching movement direction and hand orientation for grasping

Abstract

In a previous work, we demonstrated that orientation of the hand in the horizontal plane (azimuth) at the time of grasping depends on the direction of the reaching movement in the horizontal plane. Here we report three experiments to further investigate the generality of this coupling. Azimuth of the hand for grasping was studied while subjects were reaching for objects placed at various locations on a horizontal board. Hand movements were recorded with an electromagnetic sensor giving information about hand 3D position and orientation. As expected, hand azimuth for grasping was coupled with movement direction in the central part of the workspace (but reached a limit for rightmost reaching directions). The coupling did not depend on the direction of where the object had to be put after grasping. Various initial positions and azimuths of the hand were compared to the most comfortable initial hand posture. The coupling between hand azimuth and movement direction remained whatever the initial hand azimuth. This demonstrates that reaching movement direction is coupled with azimuth at the time of grasping and not with a rotational hand movement. The coupling between hand azimuth and movement direction subsisted when the initial upper trunk orientation was changed. Thus our results cannot be explained by an invariance of the coupling coded in hand-centered or shoulder-centered coordinates. They rather suggest that the movement is produced in a frame of reference associated with the environment.

Introduction

Prehension movements involve two components: transportation of the hand in vicinity of the object to be grasped (the reaching or transport component) and formation of the finger posture for grasping (the grasping component) [32]. The finger configuration for grasping varies with the intrinsic properties of the object such as size, shape and weight and can be described as an opposition axis along which the fingers exert forces on the object and ensure stable grasp [21], [28]. The orientation of the opposition axis for grasping is known to depend on the shape and orientation of the object [7], [10], [11], [24]. In addition, it has been demonstrated that, when it is not constrained by the shape or orientation of the object, the orientation of the opposition axis varies with the location of the object in the horizontal plane [14], [31]. In a recent study, we confirmed that hand azimuth (i.e. the projection of the hand longitudinal axis in the horizontal plane) for grasping depends on the location of the object in the horizontal plane and we found that it also varied with the initial hand position [33]. We demonstrated that the variations of hand azimuth with either the object location or the initial hand position could be largely explained by a coupling of hand azimuth for grasping to movement direction in the horizontal plane (i.e. the vector joining the initial hand position to the object location). This result confirms that the control of hand orientation for grasping is strongly linked to the control of the reaching component, as proposed by Desmurget et al. [7], [10].

The mechanisms of the control of goal-directed movements are still controversial. For some authors, goal-directed movements are first specified as a vector in the task space, thus defining the trajectory of movement of the end-point of the limb [1], [13], [17]. It is usually assumed that visuomotor coordination is achieved through a sequence of coordinate transformations between the visual space where the target is perceived and the motor space, which is defined in joint and muscle coordinates [30]. In particular, Soechting and Flanders proposed an intermediate coordinate system centered on the shoulder [38], [39]. Other authors proposed that goal-directed movements are planned in joint space as sets of angles representing a desired or a reference posture [7], [10], [11], [18], [34], [35]. Some differences between the results favoring the spatial motor control hypothesis and those favoring the postural motor control hypothesis could be due to different experimental constraints [9]. However, there is at present no agreement on the question of how the central nervous system chooses an upper limb posture that corresponds to a desired hand position and orientation in space. This question is not trivial since the mapping between the desired hand position and orientation in space and the upper limb joint configuration is not unique and since human subjects adopt a regular upper limb configuration for grasping despite anatomical redundancy [18].

The hypothesis is that movements are controlled by means of synergies, which reduce the number of available degrees of freedom [3]. One example was found in the oculomotor system since the orientation of the eyeball during fixation (3 degrees of freedom, df) is uniquely determined by gaze direction (2 df), each eye orientation having its rotation axis in a head fixed plane called Listing’s plane [5], [41]. This behavioral regularity, known as Donder’s law, is probably linked to neural mechanisms. It has been proposed that the straight arm when pointing may be similar to the eye and achieve a constant orientation for a particular target, even if the rotation axes does not follow Listing’s law [20]. However, Donder’s law is not obeyed in more general upper limb movements, in particular when the task involves upper arm–fore arm coordination [26] or when considering movements from different initial positions [8], [16], [33], [40].

Instead, we propose that reaching to grasp movements use the coupling between reaching movement direction and hand orientation as a simplifying synergic principle [33]. Such a coupling, which explains the differences in grasping posture due to both the target and the different initial hand positions, may simplify the planning of prehension and the coordination of reaching and grasping. Here, we report a series of three experiments aimed at further testing the generality of the coupling between movement direction and hand azimuth. In the previous study, subjects had to bring the object in front of them after having grasped it [33]. The first experiment compared this task condition to a lifting task, which imposes no horizontal movement direction after grasping. The second and third experiments were designed to test the hypothesis that the coupling of hand azimuth for grasping to movement direction could be explained by an invariance in hand-centered [17] or in shoulder-centered reference frames [38], [39]. If this were the case, hand azimuth for grasping should vary with a modification of the initial posture with different orientations of the hand or the trunk, respectively. In addition, the workspace was wider than the previous one, in order to test the consequence of a conflict between movement direction and the need to preserve a comfortable posture for grasping [34], [35]. In these three experiments, hand azimuth for grasping was tightly coupled to the reaching movement direction, at least within the central workspace. This coupling was not modified by the initial hand or trunk orientation, suggesting that it was not planned in hand- or shoulder-centered reference frame. The generality and robustness of this relationship suggests that the control of goal-directed gestures is more likely devoted to the orientation of the distal limb segment than to the trajectory of the hand in space.