Exp Brain Res DOI 10.1007/s00221-009-1982-3

RESEARCH NOTE

Location but not amount of stimulus occlusion influences the stability of visuomotor coordination Alen Hajnal Æ Michael J. Richardson Æ Steven J. Harrison Æ R. C. Schmidt

Received: 1 June 2009 / Accepted: 20 July 2009 ! Springer-Verlag 2009

Abstract The current study examined whether the amount and location of available movement information influenced the stability of visuomotor coordination. Participants coordinated a handheld pendulum with an oscillating visual stimulus in an inphase and antiphase manner. The effects of occluding different amounts of phase at different phase locations were examined. Occluding the 0"/ 180" phase locations (end-points) significantly increased the variability of the visuomotor coordination. The amount of occlusion had little or no affect on the stability of the coordination. We concluded that the end-points of a visual rhythm are privileged and provide access to movement information that ensures stable coordination. The results are discussed with respect to the proposal of Bingham (Ecol Psychol 16:45–43, 2004) and Wilson et al. (Exp Brain Res 165:351–361, 2005) that the relevant information for rhythmic visual coordination is relative direction information. Keywords

Coordination ! Coupling ! Perception

A. Hajnal (&) Department of Psychology, University of Southern Mississippi, 118 College Dr. #5025, Hattiesburg, MS 39406, USA e-mail: [email protected] M. J. Richardson Colby College, Waterville, USA S. J. Harrison University of Connecticut, Storrs, USA R. C. Schmidt College of the Holy Cross, Worcester, USA

Introduction Rhythmic coordination of limb movements of an individual has received considerable amount of attention over the past several decades. Adopting a dynamical systems framework, much of the research has been aimed at understanding and modeling the patterns and stabilities of interlimb coordination (Haken et al. 1985; Kelso et al. 1990; Schmidt et al. 1993; Scho¨ner et al. 1986). Discovering that the same patterns and stabilities occur between the limbs of two individuals, or an individual and an environmental rhythm, has led some researchers to argue that the coupling that constrains rhythmic coordination is informational (Bingham 2004a; Kugler and Turvey 1987; Mechsner et al. 2001; Schmidt et al. 1990; Schmidt et al. 2007; Schmidt and Turvey 1994; Wilson et al. 2005a). Most notable is the research on visually mediated rhythmic limb coordination, which has demonstrated that coordination of limb movements with an oscillating visual stimulus (Byblow et al. 1995; Ceux et al. 2003; Liao and Jagacinski 2000; Peper and Beek 1998; Roerdink et al. 2005; Russell et al. 2004), or the movements of another individual (Amazeen et al. 1995; de Rugy et al. 2006; Schmidt et al. 1990, 1998; Schmidt and Turvey 1994; Temprado et al. 2003; Temprado and Laurent 2004) are constrained to inphase and antiphase patterns of coordination, that inphase is more stable than antiphase coordination, and that the stability of such coordination decreases with increases in movement frequency. Considering the coupling for rhythmic coordination as informational leads one to investigate what movement information needs to be detected for stable rhythmic coordination, and in addition, as to how the pick-up of this information constrains the patterning and stabilities of visuomotor coordination. Bingham and colleagues have

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argued that the stability of visuomotor coordination might depend on the perception of relative phase or, more specifically, on the detection of information that specifies relative phase (Bingham 1995; Bingham and Zaal 1999; Bingham et al. 2001; Zaal et al. 2000). This argument stems from findings that demonstrate how perceptual judgments of relative phase stability mirror the relative phase stabilities observed for interlimb coordination. Specifically, individuals judged the relative phase of two visually displayed dots as being maximally stable when the dots oscillated inphase (08), moderately stable when the dots oscillated antiphase (1808), and completely unstable when the dots oscillated at a 908 relative phase relation. Judgments of stability were also found to decrease with increases in movement frequency, and relative phase variability was better discriminated for 08 compared to 1808, and not at all for a 908 relative phase relation. Based on the above findings and subsequent experimental work, Bingham (2004a, b) and Wilson et al. (2005a, b) have proposed that the visual information relevant for visuomotor coordination is the relative direction of movement along parallel orientations and that the detection of this information is dependent upon the relative speed of movement (relative direction is more difficult to discriminate as relative speed increases). Pertinent to this hypothesis is the degree to which specific kinematic locations of a movement are particularly important for the production of stable visual coordination and whether the amount of available movement information influences the stability of visual rhythmic coordination. The current study investigates these questions by occluding different amounts of an oscillating visual stimulus’ motion at different locations and measuring the influence that these manipulations had on the stability of 1:1 frequency locked visuomotor coordination. In short, occluding regions of the visual stimulus’ motion at which relative direction information is most salient should decrease the stability of the visual coordination. Thus, increased occlusion of the lower relative speed portions (i.e., the endpoints) of the stimulus’ trajectory should increase the variability of the coordination, whereas occluding higher relative speed portions (i.e., the mid-point) should have little or no effect on the stability (variability) of the visual coordination.

A pendulum was constructed from a 46-cm-long aluminum rod with a 12-cm wooden handle attached to the rod’s top and a 150-g lead weight attached to the rod’s base. The eigenfrequency of the pendulum was 0.90 Hz. Wrist-pendulum movement trajectories were recorded at 100 Hz using electrogoniometers (Biometrics, Gwent, UK) attached to the back of the participants’ right hand and 12–14 cm up on his/ her forearm. A Dell Optiplex Pentium-4 PC computer was programmed to record the movements of the wrist as well as generate the oscillating visual stimulus and the regions of occlusion on the projection screen (Dell LCD Projector 2300MP). The experimental setup is shown in Fig. 1a.

Materials and methods Ten students from the University of Connecticut participated in partial fulfillment of a course requirement. All were right-handed and had normal or corrected-to-normal vision. All procedures were approved by the university’s Institutional Review Board.

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Fig. 1 a The experimental setup. b An illustration of the motion and phase (hs) of the visual stimulus. c The motion and phase (hw) of a pendulum swung about the wrist

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The oscillatory stimulus was a round dot 4 cm in diameter, which oscillated horizontally in a sinusoidal motion at 0.90 Hz with amplitude of 85 cm (see Fig. 1b). Participants were required to coordinate their movements with the oscillating stimulus. The stimulus was occluded (hidden from view) by rectangles that were projected over different parts of the stimulus trajectory. The design of the experiment was a 2 9 3 9 3 withinsubjects design with variables of relative phase mode (w: inphase [/ = 0"], antiphase [/ = 180"]), amount of occluded phase (80", 120", 160"), and location of occluded phase (0"/180", 90"/270", 45"/135"/225"/315"). Upon arrival, participants were informed that they would be required to coordinate the rhythmic movements of a handheld pendulum with the movements of a visually projected oscillating stimulus. Participants sat in a chair positioned 1.6 m from a projection screen. The chair had a forearm support parallel to the ground on the right-hand side so that a handheld pendulum could be oscillated in the sagittal plane using ulnar-radial deviation of the wrist joint (see Fig. 1a, c). They were handed the 0.9 Hz pendulum and instructed to grasp it such that the top of the pendulum’s handle was flush with the top of the fist. The experimenter then showed the participants the visual stimulus and demonstrated how to successfully coordinate their wrist movements with the stimulus in inphase and antiphase manners. They were told that inphase coordination refers to the situation in which the pendulum and the stimulus are in the same position and moving in the same direction at any point in time. Conversely, they were told that antiphase refers to situations when the pendulum and the stimulus are in opposite positions and move in opposite directions at any point in time. Participants were also told that portions of the visual stimulus would be occluded in some trials and that although coordination might be difficult during these occlusion trials, they should try their best to maintain the specified mode of coordination. The experiment consisted of thirty-six 35-s trials (two trials for each of the 18 different conditions), with condition order randomized across the trials.

points of minimum angular deviation (valleys) of the movement time series. To examine the patterning and stability of the coordination across the different conditions, the relative phase between the movement time series of the wrist and the oscillating stimulus was examined for each trial. This was done by first differentiating the wrist and stimulus movement time series for each trial to obtain two velocity time series. These velocity time series were then normalized by frequency and the movement phase angles (h") calculated for the wrist and stimulus time series as hi ¼ arctanðx_i =xi Þ;

ð1Þ

where x_ i is the normalized angular velocity at the ith sample (normalized in terms of the mean angular frequency for the trial) and xi is the angular displacement of the ith sample. The difference between the phase angles of the wrist and stimulus was then computed (/ = hw - hs), and the dependent variable of SD/ was calculated from the resulting relative phase time series. The first 5 s of each movement time series was removed to eliminate transients. For 11 trials, an additional 5 s (a total of 10 s) of the movement time series was removed from the beginning of the trial to eliminate transients. Eight trials were dropped from the analysis due to the participant’s inability to maintain the intended phase mode.

Results Period and amplitude The 2 (phase mode) 9 3 (amount of phase occlusion) 9 3 (location of phase occlusion) repeated-measures analysis of variance (ANOVA) conducted on mean period yielded no significant results, with participants producing the intended frequency of 0.9 Hz for each condition. The analysis of amplitude also yielded no significant effects with the mean amplitude being consistent (overall mean of 53.61") across the different conditions.1 We concluded that any potential effect of occlusion on the variability of relative phase was not moderated by changes in period or amplitude.

Data reduction and analysis Relative phase The motion time series were normalized around zero and low-pass filtered (Butterworth filter) with a cutoff frequency of 10 Hz before calculating the dependent measures. The mean period in seconds was calculated for each trial as the mean time between the points of maximum angular extension of the movement time series. The mean movement amplitude in degrees was also calculated for each trial as the mean difference between the points of maximum angular extension (peaks) and the corresponding

The 2 9 3 9 3 repeated-measures ANOVA conducted on SD/ yielded a significant main effect of phase mode, F(1, 9) = 11.61, p \ 0.01, with participants exhibiting a higher magnitude of relative phase fluctuations for 1

Compared to the small magnitude difference in amplitude measured in the present study, in a related experiment by de Rugy et al. (2008) even a threefold increase in stimulus amplitude had no influence on the stability of visuo-motor coordination.

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Exp Brain Res Fig. 2 SD/ as a function of amount and location of phase occlusion

antiphase coordination (14.28") compared to inphase coordination (12.35"). More importantly, there was a significant effect for location of phase occlusion, F(2, 18) = 31.99, p \ 0.01. The SD/ was greater for the 0"/180" (14.625") occlusion condition compared to the 90"/270" (12.49") and 45"/135" (12.82") occlusion conditions (see Fig. 2).2 There was no phase mode 9 location interaction (p [ 0.28), but a (planned) simple effects analysis revealed that when the endpoints were occluded antiphase was less stable than inphase coordination, F(1,9) = 6.06, p \ 0.05. Interestingly, there was no main effect for amount of phase occlusion F(2, 18) = 2.45, p [ 0.11, nor any interaction effects (all p [ 0.88), with the amount of phase occlusion having no influence on the variability of the coordination. The same SD/ was observed for all three occlusion amounts.

Discussion The present results are consistent with Bingham’s relative direction proposal. Coordination became less stable whenever detection of relative direction was diminished by increased relative speed, occlusion, or both. In the case of antiphase movements this happened to coincide with endpoints of the trajectory being occluded, where relative speed is slower (allowing relative direction to be perceived more easily) than in other parts of the trajectory. In the case of inphase movements, occlusion of the end-points also resulted in increase of SD/, as compared to other occlusion locations. This may have been due to the larger absolute speed of the oscillating stimulus away from the end-points. Also consistent with the relative direction model, antiphase was less stable than inphase when detection of relative direction was compromised by end-point occlusion. 2

The results of a pilot experiment that included manipulation of the location of occlusion at a fixed occlusion amount of 80" revealed that the variability of relative phase was equal to control (no occlusion) in all but the end-point occlusion location condition.

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It is particularly interesting to note that participants could still perform the task even when the end-points were occluded with the largest amount of occlusion (160"), which shows that there is information throughout the trajectory that enables the task to be performed and that this information is more difficult, but not impossible to discriminate in some cases (e.g., in antiphase pattern). As such, the perception-action system involved in visuomotor coordination with an environmental stimulus exhibits remarkable resilience against complete breakdown of coordination. What would happen if information about relative direction was not continuously available for visual perception, but only suggested? The possibility that the endpoints of a visual rhythm ‘anchor’ the movements of an individual during visuomotor coordination would lead to the question of whether the coordination that occurs between the movements of an individual and a discrete metronomic visual stimulus is as or more stable than the visuomotor coordination that occurs between the movements of an individual and a continuously oscillating stimulus. Future research examining this question might help in understanding whether visuomotor coordination can be constrained by a discrete or a continuous informational coupling, and whether end-points play an essential instead of an accidental role in visuomotor coordination (Roerdink, et al. 2005, 2008). An unintentional visuomotor coordination paradigm (Richardson et al. 2005; Schmidt et al. 2007) might prove useful for identifying the potential benefits of end-point information, as well as differences between discrete and continuous informational couplings. Because the coordination dynamic is much weaker for spontaneous, unintentional compared to intentional visual coordination, manipulations that identify important sources of information, such as that detected at the end-points of a visual rhythm, could potentially result in the complete absence of visuomotor coordination (Richardson et al. 2007). It is an empirical question whether the present results are general enough to hold up in other coordination tasks, such as bimanual coordination driven by a periodic visual

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stimulus (e.g., Mechsner et al. 2001), or interpersonal coordination tasks in which participants track and coordinate with one another’s movements, effectively behaving as animate metronomes. It is plausible to assume that the intrinsically larger variability of human metronomes has the potential to cause a complete breakdown of coordination. In any case, the discovery of information that underwrites visuomotor coordination may help us understand how synchrony in skillful individual or collective behavior (such as dance, sports, and music) emerges in an environment that may include both animate and inanimate periodic stimuli. Acknowledgments The authors would like to thank Justin Goodman for his help with data collection and Bruce Kay, Kerry Marsh, and Michael Turvey for their helpful comments. This work was funded by National Science Foundation Grants BSC-0240277, BCS0240266, and BCS-0750190.

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