Exp Brain Res (2014) 232:575–586 DOI 10.1007/s00221-013-3766-z

Research Article

Preferred directions of arm movements are independent of visual perception of spatial directions Natalia Dounskaia · Wanyue Wang · Robert L. Sainburg · Andrzej Przybyla 

Received: 14 May 2013 / Accepted: 1 November 2013 / Published online: 21 November 2013 © Springer-Verlag Berlin Heidelberg 2013

Abstract Directional preferences have previously been demonstrated during horizontal arm movements. These preferences were characterized by a tendency to exploit interaction torques for movement production at the shoulder or elbow, indicating that the preferred directions depend on biomechanical, and not on visual perception-based factors. We directly tested this hypothesis by systematically dissociating visual information from arm biomechanics. Sixteen subjects performed a free-stroke drawing task that required performance of fast strokes from the circle center toward the perimeter, while selecting stroke directions in a random order. Hand position was represented by a cursor displayed in the movement plane. The free-stroke drawing was performed twice, before and after visuomotor adaptation to a 30° clockwise rotation of the perceived hand path. The adaptation was achieved during practicing pointing movements to eight center-out targets. Directional preferences during performance of the free-stroke drawing task were revealed in ten out of the sixteen subjects. The orientation and strength of these preferences were largely the same in both conditions, showing no significant effect of the visuomotor adaptation. In both conditions, the major

N. Dounskaia (*) · W. Wang  Kinesiology Program, School of Nutrition and Health Promotion, Arizona State University, Phoenix, AZ 85004, USA e-mail: [email protected] R. L. Sainburg · A. Przybyla  Department of Kinesiology, The Pennsylvania State University, University Park, PA 16802, USA R. L. Sainburg · A. Przybyla  Department of Neurology, The Pennsylvania State University, Hershey, PA 17033, USA

preferred directions were characterized by higher contribution of interaction torque to net torque at the shoulder as well as by relatively low inertial resistance and the sum of squared shoulder and elbow muscle torques. These results support the hypothesis that directional preferences are largely determined by biomechanical factors. However, this biomechanical effect can decrease or even disappear in some subjects when movements are performed in special conditions, such as the virtual environment used here. Keywords Arm movements · Multi-joint · Interaction torque · Visuomotor adaptation · Movement direction · Variability

Introduction Our previous studies revealed directional preferences of horizontal arm movements (Dounskaia and Goble 2011; Dounskaia et al. 2011; Goble et al. 2007; Wang and Dounskaia 2012; Wang et al. 2012). This was achieved by using a free-stroke drawing task that provided freedom in the selection of movement direction of the arm and, thus, enabled subjects to demonstrate directional preferences. Subjects produced center-out strokes, moving the arm in the horizontal plane. The instruction was to produce strokes in as many directions as possible while selecting the directions in a random order. Although this instruction encouraged the uniform distribution of movement directions around the circle, actual distribution was anisotropic, revealing systematic directional preferences. We previously employed both computational and experimental approaches to investigate the factors that

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might contribute to these directional preferences. The computational approach consisted of quantifying a number of kinetic and kinematic factors, or costs, that seemed likely to be optimized during arm movements and comparing the optimal directions for each cost to the preferred directions revealed with the free-stroke drawing task. Up to eight different costs of arm movements were examined. The results consistently pointed to a single criterion as the best predictor of the preferred directions. This criterion represented the prediction of the leading joint hypothesis (LJH, see for review Dounskaia 2005, 2010) that there is a preference to perform arm movements by rotating either the shoulder or elbow (leading joint) actively, by muscle torque (MT), and by using interaction torque (IT) produced by the leading joint motion as the dominant mover of the other (subordinate) joint. In other words, the preference is to limit active control to a single joint and let the rest of the arm be pulled predominantly passively. This finding was further supported experimentally by testing how various movement conditions influenced the directional preferences and the ability of the various optimization criteria to account for these preferences. Movement speed, availability of visual feedback, attention, and load attached to the wrist were manipulated. All these studies consistently supported the preference to organize joint control according to the prediction of the LJH, i.e., to actively generate motion at one joint only and allow passive inter-segmental dynamics to be the primary source of motion of the other joint. Although our previous studies point to biomechanical factors as the cause of the directional preferences, it remains unclear whether a propensity to move in specific spatial directions contributes to these preferences. Dounskaia and Goble (2011) investigated this contribution by comparing the free-stroke production with and without visual feedback. Removal of visual feedback during movement resulted in moderate increases in the strength of directional preferences, but it did not change the preferred directions. This result does not support the influence of perception of spatial directions on the preferred directions, rather suggesting that this perception is used to overcome the directional preferences and improve stroke direction randomization. However, memory of visual information about the initial arm position obtained prior to withdrawing visual information could be sufficient to successfully perform movements in desired spatial directions (Ghez et al. 1995). Thus, the role of perceived spatial directions in the emergence of directional preferences remains unclear. The goal of the present study was to clarify this role. This was achieved by using a virtual environment. The visually perceived movement directions were systematically

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dissociated from arm biomechanics by applying a clockwise 30° rotation of the perceived hand position. The preferred directions were compared before and after adaptation to this visuomotor rotation. When the rotation of the perceived hand path was applied, motion of the cursor in a certain direction required motion of the hand in a different direction that compensated for the visual rotation. As previous studies have demonstrated, a novel association between the directions of the cursor and hand motions (visuomotor adaptation) emerges as a result of practice of pointing movements to center-out targets in this paradigm (Cunningham 1989; Roby-Brami and Burnod 1995; Pine et al. 1996). The practice of pointing movements also changes the association between the cursor motion direction and inter-segmental dynamics because the pattern of interaction torques at the joints is unique in each movement direction (Dounskaia et al. 2002; Galloway and Koshland 2002). Two alternative predictions were tested. If the directional preferences represent biases toward specific visually represented directions, adaptation to the clockwise 30° rotation of the perceived hand path will result in the counterclockwise 30° rotation of the preferred directions of actual hand movements. However, if the directional preferences are caused by biomechanical factors, as predicted by the LJH, the visuomotor adaptation will have no effect on the preferred directions.

Materials and methods Subjects Sixteen neurologically intact right-handed adults (nine males and seven females, 21.6 ± 0.9 years of age) were recruited from the community of Pennsylvania State University to participate in this study. Handedness was assessed using a questionnaire that was adapted from Hull (1936) and that included 35 questions. All subjects signed an informed consent form approved by the Pennsylvania State University Institutional Review Board. The experiment was conducted in accordance with ethical guidelines set forth in the Declaration of Helsinki. Experimental apparatus A schematic representation of the experimental setup is shown in Fig. 1a. Subjects were seated in front of a table with the right arm supported horizontally over a frictionless air jet system the height of which was just below the shoulder level. A circle, its center, targets, and a cursor representing the index finger position were projected on a horizontal back-projection screen positioned above the arm. A mirror positioned parallel and below the screen reflected

Exp Brain Res (2014) 232:575–586

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Fig. 1  Experimental setup and results of visuomotor adaptation. a Lateral and b top view of the experimental apparatus. The initial position of the endpoint was defined by shoulder and elbow joint angles of ϕ = 40° and θ = 100°, respectively. Positive values of ϕ and θ corresponded to joint flexion

the visual display, so as to give the illusion that the display was in the same horizontal plane as the fingertip. Movements were restricted to the shoulder and elbow joint. The joints distal to the elbow were immobilized using a splint. Trunk motion was limited using a four-point trunk restraint system. Position and orientation of each limb segment were recorded at 130 Hz sampling frequency using a Flock of Birds (FOB) electromagnetic 6-DOF movement tracking system (Ascension-Technology, USA). Two sensors were firmly attached to the upper arm and the wrist, respectively, at approximately the center of each segment. The position of the following three bony landmarks was digitized and remained at a constant distance offset from the sensors throughout the experimental session: (1) index fingertip, (2) the lateral epicondyle of the humerus, and (3) the acromion, directly posterior to the acromioclavicular joint. Experimental design The initial position of the arm during all movements performed in the experiment was defined by the shoulder and elbow joint angles of ϕ = 40° and θ = 100°, respectively (Fig. 1b). The usage of the same initial joint angles assured similar inter-segmental dynamics conditions across subjects. The initial joint angles were chosen to minimize passive effects that arise when motion approaches anatomical limits of joint rotations. The experiment included four sessions. In the first (baseline) session, no rotation (NR) of the perceived hand path was applied. Subjects were presented a circle of 15 cm radius and its center. The center-out free-stroke drawing task was performed that required subjects to produce straight strokes from the center to the perimeter of the circle by sliding the tip of the right index finger along the table surface. Accuracy of reaching the perimeter was deemphasized. Fingertip motion was represented by displacement of the cursor. No other feedback on produced strokes was

provided. Upon completing each stroke, subjects moved the fingertip along the table surface back to the circle center to initiate a subsequent stroke. The instruction was to produce strokes in as many directions across the circle as possible while selecting directions in a random order. Clockwise or counterclockwise stroke sequences and repetitive movements in the same directions were not allowed. These instructions encouraged the uniform distribution of movement directions. Deviations from the uniform distribution consistent across subjects would indicate inherent directional preferences. The production of strokes was paced by a metronome at 1 Hz frequency with a stroke and a movement back to the center performed at each beat. Twentytwo trials of the free-stroke drawing task were performed, each of 15-s duration. The first two trials were practice trials that were not included in the analysis. In the second (training) session, subjects performed center-out reaching movements with clockwise rotation of the cursor motion representing the perceived hand path. Eight targets equally distributed around the initial position at the 15 cm distance from it were used. Eighteen blocks of eight reaching movements to all targets were performed, resulting 144 movements in total. The amount of rotation of the perceived hand path gradually increased from 0° to 30° with an increment of 3° during the first 11 movement blocks, and it was maintained at 30° during the remaining seven blocks. The gradual rotation was used because it has been shown that this design avoids explicit knowledge of the rotation that may interfere with adaptation (Malfait and Ostry 2004). The third (testing) session included the free-stroke drawing task performed with the 30° clockwise rotation (WR) of the perceived hand path. The task and instructions given to subjects were identical to those in the first session. Again, 20 trials of 15 s duration were performed. The fourth (aftereffect) session was conducted similarly to the training session, although the rotation of the

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perceived hand path was not applied. Subjects performed four blocks of reaching movements toward the eight targets. This was done to verify whether adaptation to the visuomotor rotation persisted throughout the previous testing session. Analysis of directional preferences The positional data were filtered with a 7 Hz low-pass 4thorder Butterworth digital filter. To establish directional preferences, movements produced during the free-stroke drawing task in both the NR and WR conditions were analyzed. Center-out strokes were identified with the use of minima of fingertip velocity. The beginning and end of each stroke were defined by two consecutive minima the first of which occurred at a  0.1). The main effect of block was significant [F(2, 26) = 27.5, P 

Preferred directions of arm movements are independent of visual perception of spatial directions.

Directional preferences have previously been demonstrated during horizontal arm movements. These preferences were characterized by a tendency to explo...
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