Human Movement Science xxx (2011) xxx–xxx

Contents lists available at SciVerse ScienceDirect

Human Movement Science journal homepage: www.elsevier.com/locate/humov

Influence of stimulus amplitude on unintended visuomotor entrainment Manuel Varlet a,b,⇑, Charles A. Coey b, R.C. Schmidt c, Michael J. Richardson b a b c

Movement to Health Laboratory, EuroMov, Montpellier-1 University, Montpellier, France Perceptual-Motor Dynamics Laboratory, Department of Psychology, University of Cincinnati, Cincinnati, OH, USA Department of Psychology, College of the Holy Cross, Worcester, MA, USA

a r t i c l e

i n f o

Article history: Available online xxxx PsycINFO classifications: 2330 2346 2260 3020 Keywords: Visuomotor coordination Eye movements Amplitude Period

a b s t r a c t Rhythmic limb movements have been shown to spontaneously coordinate with rhythmic environmental stimuli. Previous research has demonstrated how such entrainment depends on the difference between the movement periods of the limb and the stimulus, and on the degree to which the actor visually tracks the stimulus. Here we present an experiment that investigated how stimulus amplitude influences unintended visuomotor entrainment. Participants performed rhythmic forearm movements while visually tracking an oscillating stimulus. The amplitude and period of stimulus motion were manipulated. Larger stimulus amplitudes resulted in stronger entrainment irrespective of how participants visually tracked the movements of the stimulus. Visual tracking, however, did result in increased entrainment for large, but not small, stimulus amplitudes. Collectively, the results indicate that the movement amplitude of environmental stimuli plays a significant role in the emergence of unintended visuomotor entrainment. Ó 2011 Elsevier B.V. All rights reserved.

1. Introduction Rhythmic human movements spontaneously coordinate with those of other individuals or environmental stimuli during visual interaction (e.g., Oullier, de Guzman, Jantzen, Lagarde, & Kelso, 2008; Schmidt & O’Brien, 1997; Schmidt, Richardson, Arsenault, & Galantucci, 2007; Varlet, Marin, Lagarde, ⇑ Corresponding author at: Movement to Health Laboratory, EuroMov, Montpellier-1 University, 700 Avenue du Pic Saint Loup, 34090 Montpellier, France. Tel.: +33 467 415 767; fax: +33 467 415 704. E-mail address: [email protected] (M. Varlet). 0167-9457/$ - see front matter Ó 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.humov.2011.08.002

Please cite this article in press as: Varlet, M., et al. Influence of stimulus amplitude on unintended visuomotor entrainment. Human Movement Science (2011), doi:10.1016/j.humov.2011.08.002

2

M. Varlet et al. / Human Movement Science xxx (2011) xxx–xxx

& Bardy, 2011). Such entrainment can occur in everyday life when an actor is walking, dancing, or just talking with another individual (e.g., Richardson, Marsh, & Schmidt, 2005; van Ulzen, Lamoth, Daffertshofer, Semin, & Beek, 2008). Having access to visual information about the movements of an environmental rhythm, however, does not ensure that entrainment will occur (e.g., Shockley, Santana, & Fowler, 2003) and the emergence and stability of spontaneous (or, unintended) coordination can depend on the difference between the natural periods of the movements involved and the degree to which the actor attends to the relevant movement information (e.g., Richardson, Marsh, Isenhower, Goodman, & Schmidt, 2007; Schmidt et al., 2007). The aim of the current study was to investigate whether movement amplitude also influences the occurrence and stability of unintended visuomotor coordination. More specifically, the study examined whether the larger the movement amplitude of a visual stimulus, the greater the occurrence and stability of unintended visuomotor entrainment. Inspired by the dynamical systems theory, previous research has shown that rhythmic visuomotor coordination between the movements of an individual and an environmental stimulus or rhythm is constrained by the dynamical entrainment processes of coupled oscillators (e.g., Byblow, Chua, & Goodman, 1995; Richardson et al., 2005; Schmidt et al., 2007; Wimmers, Beek, & van Wieringen, 1992). In line with the predictions of the Haken, Kelso, and Bunz (1985) coupled oscillator model that captures the dynamics of bimanual rhythmic coordination (see also, Kelso, 1995) and its derivatives for visual coordination perception (e.g., Bingham, 2004; Bingham, Schmidt, & Zaal, 1999; Zaal, Bingham, & Schmidt, 2000), visuomotor limb-to-stimulus movements are constrained (without practice) to in-phase and anti-phase patterns of coordination (relative phase values of 0° and 180°, respectively), with in-phase coordination being more stable than anti-phase coordination (e.g., Richardson et al., 2007; Schmidt & O’Brien, 1997; Wimmers et al., 1992). In addition, the stability of in-phase and anti-phase coordination decreases as movement period decreases (i.e., movement becomes faster) and the difference between the natural periods (i.e., detuning) of movement’s involved increases, with anti-phase coordination becoming unstable at fast movement periods and for large magnitudes of detuning (e.g., Richardson et al., 2007; Schmidt, Carello, & Turvey, 1990; see Schmidt & Richardson (2008) for a review). Rhythmic visuomotor coordination can occur both intentionally and unintentionally (spontaneously and without awareness). Like bimanual coordination, intended visuomotor coordination is typically absolute, meaning that either in-phase or anti-phase coordination are stably maintained for an extended period of time. In contrast, unintended coordination tends to be relative because of the weak strength of the coupling (e.g., Richardson et al., 2007; Schmidt & O’Brien, 1997; von Holst, 1973) and is characterized by an intermittent attraction toward in-phase and anti-phase patterns of coordination (e.g., Issartel, Marin, & Cadopi, 2007; Schmidt & O’Brien, 1997; Tognoli, Lagarde, de Guzman, & Kelso, 2007). Accordingly, unintended visuomotor entrainment is much more affected by differences between the period of the visual stimulus and the preferred period (i.e., comfort mode) of the actor than intended visuomotor coordination, with even small differences in period greatly reducing the chance that entrainment will occur (e.g., Richardson et al., 2007; Schmidt & O’Brien, 1997; Schmidt et al., 2007). Lopresti-Goodman, Richardson, Silva, and Schmidt (2008) provided a clear demonstration of the significant impact period difference has on the occurrence of unintended visuomotor coordination. In this experiment, participants were instructed to oscillate a wrist pendulum at a self-selected comfort tempo while simultaneously reading letters displayed on an oscillating visual stimulus displayed on a projection screen. The period of the visual stimulus was manipulated as a function of the participant’s preferred movement period as measured from a set of pre-trials. The results demonstrated that the magnitude and stability of entrainment decreased when the stimulus period was faster or slower than the participant’s preferred movement period, with no visuomotor entrainment occurring for stimulus periods that were greater or less than 15% of the participant’s preferred movement period. Researchers who have investigated unintended visuomotor entrainment have also shown how the strength of the visual coupling is mediated by the degree to which an actor attends to the displacements of rhythmic stimuli. Using a similar method to the Lopresti-Goodman et al. (2008) study just described, Schmidt et al. (2007) demonstrated the role that visual tracking plays in the emergence of visuomotor entrainment. Participants were instructed to read letters that were displayed at random intervals either on an oscillating visual stimulus (i.e., tracking condition) or just above the middle of Please cite this article in press as: Varlet, M., et al. Influence of stimulus amplitude on unintended visuomotor entrainment. Human Movement Science (2011), doi:10.1016/j.humov.2011.08.002

M. Varlet et al. / Human Movement Science xxx (2011) xxx–xxx

3

the trajectory of an oscillating visual stimulus (i.e., non-tracking condition). Results demonstrated that entrainment occurred for both non-tracking and tracking conditions, but that significantly stronger entrainment occurred for the tracking condition compared to the non-tracking condition (see also Richardson et al., 2007). One reason why stronger entrainment occurs when participants visually track the stimuli could be that the movement of the eyes establish an intrapersonal eye-limb coupling that, when added to the informational coupling, operates to strengthen the entrainment (Schmidt et al., 2007). Different studies support the existence of such coupling between eyes and limb movements. Better visual tracking of an oscillating stimulus has been demonstrated when its displacement was manually tracked by participants at the same time (Koken & Erkelens, 1992; Leist, Freund, & Cohen, 1987). Coupling between limb and eye movements has also been reported in other experimental situations such as pointing and reaching tasks (e.g., Lunenburger, Kutz, & Hoffmann, 2000; Snyder, Calton, Dickinson, & Lawrence, 2002). Previous research has also showed a significant influence of eye movements on the execution of limb movements similar to the findings of Schmidt et al. (2007) (e.g., Henriques & Crawford, 2002; van Donkelaar, 1997). In addition, when tracking visual stimuli, participants have better access to the endpoints of a movement trajectory that could explain stronger entrainment as well. The endpoints of a stimulus trajectory contain important turn-around point information that strengthens visual coupling by anchoring the movements in time and space (e.g., Bingham, 2004; Hajnal, Richardson, Harrison, & Schmidt, 2009; Roerdink, Ophoff, Peper, & Beek, 2008; Roerdink, Peper, & Beek, 2005; Wilson, Collins, & Bingham, 2005). The above-mentioned research has provided clear evidence that both visual tracking and period difference moderate the strength of unintended visuomotor entrainment. Although the influence of the stimulus amplitude on unintended entrainment has never been investigated, different studies have focused on the role of movement amplitude in bimanual rhythmic motor coordination (e.g., Peper & Beek, 1998a, 1999; Post, Peper, & Beek, 2000). The results of these previous studies have been somewhat varied, however. Specifically, some investigations have shown an increase of the coupling strength in bimanual coordination for larger amplitudes of movement in line with the Haken–Kelso– Bunz model predictions, whereas other studies have found no influence of movement amplitude (e.g., Peper & Beek, 1998b; Peper, de Boer, de Poel, & Beek, 2008; Post et al., 2000). It has also been demonstrated that amplitude asymmetry in bimanual coordination produces an asymmetry between the preferred movement periods of the two hands and destabilizes the coordination (de Poel, Peper, & Beek, 2009). For intended visuomotor coordination, manipulations of movement amplitude have been found to have little to no effect on the stability of coordination (de Rugy, Oullier, & Temprado, 2008; Peper & Beek, 1998a). It is possible, however, that the effects of amplitude may only be apparent for weaker states of coordination, that is, for intermittent unintended coordination (Ridderikhoff, Peper, & Beek, 2005). The possibility that stimulus amplitude may influence the strength of unintended visuomotor entrainment is suggested by research that has investigated the spontaneous entrainment that occurs between the postural movements of a standing participant and the movements of a moving room (e.g., Dijkstra, Schöner, & Gielen, 1994a; Dijkstra, Schöner, Giese, & Gielen, 1994b). Although the relation between the visual information and movement performed differed in this postural research, motion of the room with larger amplitudes resulted in stronger entrainment. More generally, previous research that has shown how the effects of visual tracking and period difference on the stability of visual coordination are significantly reduced during intended coordination and only clearly apparent during investigations of unintended coordination (e.g., Richardson et al., 2007; Schmidt et al., 2007). The current study investigated whether stimulus amplitude influences unintended visuomotor entrainment by using a paradigm similar to those previously employed (e.g., Lopresti-Goodman et al., 2008; Schmidt et al., 2007). Participants were instructed to rhythmically oscillate their forearm while viewing an oscillating visual stimulus of various amplitudes. We expected that larger stimulus amplitudes would increase the occurrence and stability of visuomotor entrainment. Alternatively, it was possible that the strongest entrainment would occur when the stimulus amplitude was equal to the preferred movement amplitude of participants, rather than for the largest stimulus amplitude. In fact, stimulus amplitudes larger or smaller than participants’ preferred amplitude could change their movement amplitude and thus their movement period due to the intrinsic frequency–amplitude relation of human movement (Kay, Kelso, Saltzman, & Schöner, 1987; Rosenbaum, Slotta, Vaughan, & Please cite this article in press as: Varlet, M., et al. Influence of stimulus amplitude on unintended visuomotor entrainment. Human Movement Science (2011), doi:10.1016/j.humov.2011.08.002

4

M. Varlet et al. / Human Movement Science xxx (2011) xxx–xxx

Plamondon, 1991). Such a change may decrease entrainment by increasing the stimulus-participant period difference in line with the amplitude asymmetry effect observed in bimanual coordination (de Poel et al., 2009; Lopresti-Goodman et al., 2008). Moreover, we expected in view of previous research that the influence of stimulus amplitude on unintended visuomotor entrainment would depend on the degree to which participants visually tracked the stimulus. Accordingly, stimulus amplitude was manipulated in both tracking and nontracking conditions (Schmidt et al., 2007). For the tracking condition, we anticipated an increase of the intrapersonal eye-limb coupling for larger stimulus amplitudes (due to an increase in the movement amplitude of the eyes) and that this would, in turn, strengthen visuomotor entrainment. For the non-tracking condition, in which participants only focused their attention on the middle of the stimulus trajectory, it was possible that higher stimulus amplitudes could have a negative effect on the magnitude of visuomotor entrainment because larger amplitudes would decrease the peripheral availability of endpoint information (e.g., Bingham, 2004; Hajnal et al., 2009; Richardson et al., 2007; Wilson et al., 2005). Further, it was possible that the stimulus period might also moderate the influence of stimulus amplitude on the strength of unintended visuomotor entrainment. Considering that manipulations of stimulus amplitude could affect both the amplitude and period of participant movements, the unintended entrainment observed could be the result of an interaction between the amplitude and the period of the stimulus. For instance, entrainment observed for stimulus amplitudes greater than the participant’s preferred amplitude could be stronger when the stimulus period is also slower than the participant’s preferred period. Therefore, the stimulus period was also manipulated in the experiment along with stimulus amplitude and visual tracking. 2. Experiment 2.1. Method 2.1.1. Participants Twenty-two undergraduates from the University of Cincinnati participated in the experiment for partial course credit. All participants had normal or corrected-to-normal vision. The experiment was approved by the University of Cincinnati Institutional Review Board. 2.1.2. Materials Participants stood 0.50 m in front of a 1.25  1.70 m projection screen where the color of a presented stimulus changed (‘flashed’) periodically (i.e., Fig. 1A). A 1  1  1.5 cm FASTRAK motion-tracking sensor (Polhemus Ltd., VT) was fixed to the tip of participants’ right index finger. It recorded the rhythmic movements of their right forearm (with index finger extended) in the horizontal plane at a sampling rate of 60 Hz with a 0.01 mm spatial resolution. A computer recorded the movement trajectories of the forearm and controlled the stimulus displays that were projected using an Epson Powerlite 53c projector (Epson America, Long Beach, CA). Participants wore modified safety glasses that prevented them from seeing their forearm movements, but ensured that they could see everything displayed on the screen in front of them. 2.1.3. Task and stimuli Participants were instructed to name the color changes of a stimulus while they performed rhythmic forearm movements in the horizontal plane at a self-chosen frequency and amplitude in three different tracking conditions: control, non-tracking and tracking. For the control condition, the color changes appeared on a stationary dot in the middle of the screen (i.e., Fig. 1B). Although no oscillating stimulus was displayed on the screen during these trials, a time series for a rhythmically moving stimulus was generated as in the other conditions so that these control trials could be used to index chance level entrainment. For the non-tracking condition, the color changes appeared on a stationary dot positioned over the middle of a horizontally oscillating dot stimulus that did not change color. Participants were told to focus their attention on the stationary dot and report the color changes. For the Please cite this article in press as: Varlet, M., et al. Influence of stimulus amplitude on unintended visuomotor entrainment. Human Movement Science (2011), doi:10.1016/j.humov.2011.08.002

M. Varlet et al. / Human Movement Science xxx (2011) xxx–xxx

5

Fig. 1. (A) Experimental setup. (B) Control, non-tracking and tracking displays used for the experiment.

tracking condition, the color changes appeared on a horizontally oscillating dot stimulus that participants were required to track with their eyes so that they could report when the color changes occurred. Both the moving and stationary stimuli had a diameter of 5.75 cm and were displayed at the forearm height of participants. When a stimulus changed color (the stationary stimulus in the control and non-tracking conditions and moving stimulus in the tracking condition), it did so randomly from red to either yellow, blue, green, or white for 200 ms every 2 s plus a random offset between 0 and 0.999 ms. When a stimulus did not change color (moving stimulus in the non-tracking condition), it remained red throughout the trial. Three different moving stimulus periods (0.9, 1.1 and 1.3 s), and amplitudes (20, 50 and 80 cm corresponding to 23°, 53°, and 77° visual angles) were used to form the different stimulus period and amplitude conditions. These values were chosen because they were centered around the average preferred movement period (1.1 s) and amplitude (50°) obtained in a pilot study. 2.1.4. Procedure On arrival, the participants were informed that the experiment was investigating color processing during multitask performance. They were told they would be required to call out as fast as possible color changes that appeared on stimuli on a projection screen. Participants were also instructed to simultaneously perform rhythmic movements of their right-forearm (index finger extended) in the horizontal plane without moving their wrist or finger. They were given a practice period to explore different periods and amplitudes of movement in order to find those that were most comfortable for them. Following this practice period, participants performed three trials for the control condition (i.e., without a visible moving stimulus) prior to completing eighteen (3 amplitudes  2 visual tracking conditions [non-tracking and tracking]  3 stimulus periods) randomized trials of 45 s. 2.1.5. Design and analysis The forearm displacements of participants in the horizontal plane were extracted, centered around zero, and low-pass filtered using a 10 Hz Butterworth filter. The first 5 s of each trial were discarded to eliminate transient behavior. To determine whether the timing of movements was affected by the visual tracking, stimulus period and stimulus amplitude manipulations, we computed the mean movement period as the average time between the points of maximum angular extension as defined Please cite this article in press as: Varlet, M., et al. Influence of stimulus amplitude on unintended visuomotor entrainment. Human Movement Science (2011), doi:10.1016/j.humov.2011.08.002

6

M. Varlet et al. / Human Movement Science xxx (2011) xxx–xxx

by the maxima of the movement time series. To determine whether the movement amplitude was affected by the experimental manipulations, we calculated the angular distance between the points of maximum flexion and extension for each half cycle of the movement time series. Two different measures were employed to determine the degree of the limb-stimulus entrainment that occurred for the different conditions (e.g., Richardson, Campbell, & Schmidt, 2009; Schmidt et al., 2007). We first calculated the cross-spectral coherence, which measures the entrainment between two rhythmic movements on a scale from 0 to 1. A value of 1 reflects a perfect coordination and a value of 0 reflects an absence of coordination (see Schmidt and O’Brien (1997) for details). For the second measure, we calculated the distribution of relative phase angles between the participant and stimulus time series. To determine these distributions, we computed the continuous relative phase of the two time series between 180 and 180 using the Hilbert transform (Pikovsky, Rosenblum, & Kurths, 2001). We then computed the percentage of occurrence of the absolute value of the relative phase angles across nine 20° regions of relative phase from 0° to 180°. Previous research showed that unintended visuomotor entrainment is characterized by a concentration of relative phase angles in the portions of the distribution close to either 0° and 180° (e.g., Richardson et al., 2007, 2009; Schmidt et al., 2007). For the statistical analysis, the values of the different dependent variables for the control condition in the factor tracking (i.e., control, non-tracking and tracking) corresponded to the average of the values obtained for the three control trials with the different stimulus time series created a posteriori. We used 3  3  3 repeated-measures ANOVA with variables of tracking (control, non-tracking and tracking), stimulus period (0.9, 1.1 and 1.3 s) and stimulus amplitude (20, 50 and 80 cm) for the statistical analysis of average movement period, average movement amplitude and average coherence. Newman–Keuls post hoc comparisons were used when it was necessary to determine the nature of the effect. We also used 3  3  3  9 repeated-measures ANOVA with variables of tracking (control, non-tracking and tracking), stimulus period (0.9, 1.1 and 1.3 s), stimulus amplitude (20, 50 and 80 cm) and phase region (0–20°, 20–40°, . . ., 160°–180°) for the statistical analysis of the relative phase distributions. In view of previous research demonstrating that unintended visuomotor phase entrainment occurs around 0° and 180°, in this analysis, we focused only on the interactions involving the factor phase region and only on the phase region 0–20° and 160–180° for the post hoc comparisons to understand the effects of the different factors (e.g., Richardson et al., 2007, 2009; Schmidt et al., 2007). 2.2. Results 2.2.1. Movement period and amplitude The ANOVA performed on the period of movement yielded significant main effects for stimulus period, F(2, 42) = 5.30, p < .05, g2p = 0.20, and for tracking, F(2, 42) = 20.22, p < .05, g2p = 0.49, and a significant interaction between stimulus period and tracking, F(4, 84) = 3.90, p < .05, g2p = 0.16 (see Table 1). Post–hoc comparisons revealed that participants decreased their period while an oscillating stimulus was visible on the screen (i.e., non-tracking and tracking conditions compared to the control condition) (p < .05), and that they tended to match the period of the oscillating stimulus on the screen indicated by a lower movement periods of participants for the stimulus period 0.9 s compared to 1.3 s in non-tracking condition (p < .05), and for the stimulus period 0.9 s compared to 1.1 and 1.3 s in tracking condition (p < .05). This tendency, however, was more pronounced when the stimulus was visually tracked as indicated by a lower movement period of participants in the tracking condition compared to the non-tracking condition for the stimulus period 0.9 s (i.e., closer to the stimulus period) (p < .05) (Schmidt et al., 2007). The ANOVA performed on the movement amplitude yielded a significant main effect of tracking, F(2, 42) = 11.64, p < .05, = g2p 0.36, stimulus period, F(2, 42) = 6.89, p < .05, g2p = 0.25, and stimulus amplitude, F(2, 42) = 6.39, p < .05, g2p = 0.23 (see Table 1). Post–hoc comparisons showed significantly larger movement amplitudes for the control condition compared to the non-tracking and tracking conditions (p < .05), for the stimulus period 1.3 s compared to 0.9 and 1.1 s (p < .05) (see Fig. 2), and for the stimulus amplitudes of 50, 80 cm compared to 20 cm (p < .05). Together, these results indicate that the movement amplitude of participants decreased when viewing the oscillating stimulus (i.e., non-tracking and tracking conditions) and increased for stimuli with larger period and amplitude. Please cite this article in press as: Varlet, M., et al. Influence of stimulus amplitude on unintended visuomotor entrainment. Human Movement Science (2011), doi:10.1016/j.humov.2011.08.002

7

M. Varlet et al. / Human Movement Science xxx (2011) xxx–xxx

Table 1 Mean and standard deviation of the period and amplitude of movement as a function of the visual tracking conditions, the amplitudes and periods of the stimulus. Stimulus

Control

Amplitude (cm)

Period (s)

Amplitude (cm)

0.9

20 50 80 20 50 80 20 50 80 20 50 80 20 50 80 20 50 80 20 50 80 20 50 80 20 50 80

1.27 1.27 1.27 1.27 1.27 1.27 1.27 1.27 1.27 0.99 1.02 1.04 1.03 1.02 1.06 1.08 1.05 1.08 0.99 0.98 0.95 1.05 1.04 1.06 1.04 1.07 1.09

33.03 33.03 33.03 33.03 33.03 33.03 33.03 33.03 33.03 25.08 26.62 27.61 26.27 27.17 28.45 26.76 27.86 29.28 25.65 25.75 25.19 24.56 26.57 26.92 25.76 27.18 28.75

1.1

1.3

Non-tracking

0.9

1.1

1.3

Tracking

Participants

Period (s)

0.9

1.1

1.3

(0.30) (0.30) (0.30) (0.30) (0.30) (0.30) (0.30) (0.30) (0.30) (0.21) (0.28) (0.23) (0.16) (0.19) (0.18) (0.18) (0.24) (0.25) (0.20) (0.17) (0.19) (0.25) (0.15) (0.18) (0.23) (0.24) (0.24)

(10.10) (10.10) (10.10) (10.10) (10.10) (10.10) (10.10) (10.10) (10.10) (9.90) (10.10) (12.40) (11.39) (10.40) (12.70) (9.98) (11.20) (14.10) (10.81) (11.70) (9.49) (8.15) (10.10) (11.10) (11.34) (9.01) (11.20)

Fig. 2. Amplitude of participants as a function of stimulus period and stimulus amplitude.

2.2.2. Entrainment The ANOVA performed on the average cross-spectral coherence yielded a significant main effect for stimulus period, F(2, 42) = 5.18, p < .05, g2p = 0.20. This effect suggested that the coherence was higher when the stimulus oscillated at a period of 1.1 s (the estimated preferred period of oscillation) although post hoc tests revealed that this coherence was only significantly higher than the 0.9 s stimulus (p < .05) but not significantly higher than the 1.3 s stimulus (p > .05). There were also significant effects of tracking, F(2, 42) = 13.86, p < .05, g2p = 0.40, stimulus amplitude, F(2, 42) = 0.64, p < .05, g2p = 0.29, and an interaction between tracking and stimulus amplitude, F(4, 84) = 5.68, p < .05, Please cite this article in press as: Varlet, M., et al. Influence of stimulus amplitude on unintended visuomotor entrainment. Human Movement Science (2011), doi:10.1016/j.humov.2011.08.002

8

M. Varlet et al. / Human Movement Science xxx (2011) xxx–xxx

Fig. 3. Average coherence as a function of tracking conditions, stimulus amplitude and stimulus period.

Fig. 4. The continuous relative phase (RP) trial time series showing the relative phase angles between the movements of the stimulus and the participant over time as a function of tracking conditions, stimulus amplitude for the stimulus period of 1.1 s.

Fig. 5. The distributions of relative phase angles as function of tracking conditions, stimulus amplitude and stimulus period.

Please cite this article in press as: Varlet, M., et al. Influence of stimulus amplitude on unintended visuomotor entrainment. Human Movement Science (2011), doi:10.1016/j.humov.2011.08.002

M. Varlet et al. / Human Movement Science xxx (2011) xxx–xxx

9

g2p = 0.21 (see Fig. 3). As depicted in Fig. 3, the non-tracking and the tracking conditions had greater coherence than the control for the three stimulus amplitudes (p < .05), but tracking had greater coherence than the non-tracking only for the 50 and 80 cm stimulus amplitudes (p < .05). These results demonstrate that entrainment occurred for the three stimulus amplitudes for both non-tracking and tracking conditions, but that visual tracking increases entrainment for the large, but not the small, stimulus amplitudes. Additional post hoc comparisons showed significant differences between the stimulus amplitudes 80 cm and 20, 50 cm for the non-tracking condition (p < .05) and between the stimulus amplitudes 20 cm and 50, 80 cm for the tracking condition (p < .05), further indicating that entrainment increased with greater stimulus amplitudes in both non-tracking and tracking conditions. No other interactions were significant. The ANOVA performed on relative phase yielded a significant main effect for phase region, F(8, 168) = 7.83, p < .05, g2p = 0.27, and a significant interaction between stimulus period and phase region, F(16, 336) = 2.52, p < .05, g2p = 0.11 (see Figs. 4 and 5). Post–hoc comparisons showed stronger in-phase entrainment (phase region 0–20°) for the stimulus period 1.1 s (estimated preferred period of participants) compared to 0.9 and 1.3 s (p < .05). The analysis also revealed a significant interaction between stimulus amplitude and phase region, F(16, 336) = 2.82, p < .05, g2p = 0.12, between tracking and phase region, F(16, 336) = 5.89, p < .05, g2p = 0.22, and between tracking, stimulus amplitude and phase region, F(32, 672) = 3.29, p < .05, g2p = 0.14. These results show that the non-tracking and tracking conditions had stronger in-phase entrainment than the control—higher percentages relative phase angles near 0° for the three stimulus amplitudes in non-tracking condition (p < .05) and for the stimulus amplitudes 50 and 80 cm in tracking condition (p < .05). The tracking condition also resulted in stronger entrainment than the non-tracking condition for the stimulus amplitudes 50 and 80 cm—higher percentages of relative phase angles near 0° (p < .05) and near 180° (p < .05), respectively. In line with the cross-spectral coherence analysis, these results demonstrate that entrainment occurred in both non-tracking and tracking conditions and that visual tracking increased entrainment for the large, but not the small, stimulus amplitudes. No other significant interactions were revealed.

3. Discussion The current study investigated whether the movement amplitude of a visual stimulus influences unintended visuomotor entrainment. We hypothesized that participants would spontaneously coordinate their forearm movements with an oscillating visual stimulus, that larger stimulus amplitudes would increase the occurrence and stability of the visuomotor entrainment, and that this influence would be modulated by visual tracking and stimulus period. Consistent with these expectations, and as a replication of previous research (e.g., Lopresti-Goodman et al., 2008; Schmidt et al., 2007), the cross-spectral coherence and relative phase analyses demonstrate that individuals spontaneously synchronized their limb movements with the rhythmic movements of environmental stimuli in an in-phase and anti-phase manner and that stronger entrainment occurred while participants visually tracked the movement of the stimulus and when the stimulus period was equal to their preferred movement period. The significance of the current study is that it extends the current understanding of what spatial–temporal properties constrain the stability of unintended visuomotor coordination by demonstrating that the strength of the entrainment depends on the movement amplitude of the stimulus. Specifically, the current results demonstrate that increases in stimulus amplitude augment the occurrence and stability of visuomotor entrainment, with stronger entrainment being observed for larger stimulus amplitudes in both tracking and non-tracking conditions. These results corroborate the previous research that indicates that coupling strength is greater for larger movement amplitudes (e.g., Dijkstra et al., 1994a; Peper et al., 2008; Swinnen, Dounskaia, Levin, & Duysens, 2001). The current results do not find support for the proposal that entrainment should be strongest for the stimulus amplitude that corresponds to the preferred movement amplitude (de Poel et al., 2009). Our results also extend previous findings by showing that the influence of visual tracking depends on the stimulus amplitude. In short, no significant difference was obtained between the nontracking and tracking conditions for the small stimulus amplitude, but was evident in the moderate Please cite this article in press as: Varlet, M., et al. Influence of stimulus amplitude on unintended visuomotor entrainment. Human Movement Science (2011), doi:10.1016/j.humov.2011.08.002

10

M. Varlet et al. / Human Movement Science xxx (2011) xxx–xxx

and large stimulus amplitudes. One can explain this finding as follows. First, assuming that visually tracking a stimulus enhances unintended entrainment because an intrapersonal eye-limb coupling is formed, the movement of the eyes may have been too small to create such an eye-limb coupling and enhance entrainment in the tracking conditions compared to the non-tracking conditions. Moreover, for the small stimulus amplitudes, the total kinematics of the stimulus’s trajectory was available for both non-tracking and tracking conditions, and thus participants had the same amount of movement information in both conditions. In contrast, for the moderate to large stimulus amplitudes picking up information about the entire trajectory became difficult without visually tracking the stimulus, and thus the visual coupling was weaker for the non-tracking compared to the tracking condition. One caveat to this latter conclusion is that although stronger entrainment was observed in the tracking compared to the non-tracking condition, there was still a positive relationship between stimulus amplitude and the level of entrainment in the non-tracking condition. That is, for the non-tracking condition entrainment was found to increase as stimulus amplitude increased, even for the largest stimulus amplitudes where the endpoints of the stimulus motion where outside the participant’s attentional focus. This supports previous research showing that although the availability of information about the entire movement trajectory, and in particular endpoint information, might be important, intended visuomotor coordination can be stably maintained while focusing on the middle of the trajectory (e.g., Hajnal et al., 2009; Roerdink et al., 2008), and extends it to unintended visuomotor entrainment. This latter conclusion is supported by the findings of a recent experiment in which participants were instructed to swing a wrist-pendulum while focusing their visual attention either on the middle or on an endpoint of a visual stimulus’s oscillatory motion (Schmidt, Mergeche, Bucci, & Richardson, 2010). The results indicated no difference in the occurrence or stability of unintended visuomotor entrainment when attending to the middle or endpoint of the trajectory, suggesting that entrainment can occur between the limb movements of an individual and a visual environmental rhythm as long as some visual information about the trajectory is available. The results also show a significant influence of the stimulus period on the movement period and amplitude of participants. Supporting previous research, participants produced slower and faster movement periods when observing slower and faster stimulus periods, respectively (Lopresti-Goodman et al., 2008; Schmidt et al., 2007). The movement amplitude of participants also increased with slower stimulus periods, a finding that is consistent with spontaneous amplitude changes observed in intended visuomotor coordination (Peper & Beek, 1998a). The results also demonstrate a significant influence of the stimulus amplitude on the movement amplitude of participants. They produced smaller and larger movement amplitudes with smaller and larger stimulus amplitudes, respectively. Overall, these results show that the period and amplitude of participants’ movement depend on an interaction between the period and amplitude of the oscillating stimulus, and hence, are perhaps constrained by the intrinsic frequency-amplitude relation of human movement (Kay et al., 1987; Rosenbaum et al., 1991). Finally, the increase in movement amplitude of participants observed with larger stimulus amplitudes could provide an additional explanation for the positive relationship between stimulus amplitude and the magnitude of unintended visuomotor entrainment. Stronger entrainment obtained in the current study may not only be a consequence of larger stimulus amplitudes resulting in increased visual activity, but may also be due to larger stimulus amplitudes resulting in an increase in the movement amplitude of an individual’s limb movements. Although the neurophysiological bases of the processes underlying unintended visuomotor entrainment remain largely unknown, actively moving a limb with larger amplitudes may result in stronger afferent—efferent neural activities (Kandel, Schwartz, Jessell, Siegelbaum, & Hudspeth, 1991), which could result in stronger interactions with the neural visual activity and thus in stronger entrainment. This possibility, however, is not supported by previous research, which found that changes in the movement amplitude of participants did not affect the stability of intended visuomotor coordination (Peper & Beek, 1998a). This may yet prove to be different for unintended visuomotor coordination and is an issue for future research. In summary, the study presented here shows that unintended visuomotor entrainment is not only strengthened when an actor visually tracks the environmental stimulus and when the periods of the actor’s limb and the stimulus are close to each other, but also when the movement amplitude of the stimulus increases. Moreover, stimulus amplitude appears to modulate the amplitude of an actor’s Please cite this article in press as: Varlet, M., et al. Influence of stimulus amplitude on unintended visuomotor entrainment. Human Movement Science (2011), doi:10.1016/j.humov.2011.08.002

M. Varlet et al. / Human Movement Science xxx (2011) xxx–xxx

11

limb movements as well as the influence of visual tracking with no effect on unintended visuomotor entrainment for small stimulus amplitudes. Accordingly, our findings suggest that to appropriately understand the patterning and stability of the movement coordination that occurs between an individual and an environmental rhythm requires that research identify the physical, spatial–temporal, and informational properties of the situation being investigated. Acknowledgments This research was supported by the National Science Foundation (BCS Awards: 0750190, 0750187, 0926662), and SKILLS, an Integrated Project (FP6-IST Contract #035005) of the Commission of the European Community. References Bingham, G. P. (2004). Another timing variable composed of state variables: Phase perception and phase driven oscillators. In H. Hecht & G. J. P. Savelsbergh (Eds.), Theories of time-to-contact advances in psychology series (pp. 421–442). Amsterdam: Elsevier. Bingham, G. P., Schmidt, R. C., & Zaal, F. T. (1999). Visual perception of the relative phasing of human limb movements. Attention, Perception, & Psychophysics, 61, 246–258. Byblow, W. D., Chua, R., & Goodman, D. (1995). Asymmetries in coupling dynamics of perception and action. Journal of Motor Behavior, 27, 123–137. de Poel, H. J., Peper, C. E., & Beek, P. J. (2009). Disentangling the effects of attentional and amplitude asymmetries on relative phase dynamics. Journal of Experimental Psychology: Human Perception and Performance, 35, 762–777. de Rugy, A., Oullier, O., & Temprado, J. J. (2008). Stability of rhythmic visuo-motor tracking does not depend on relative velocity. Experimental Brain Research, 184, 269–273. Dijkstra, T. M., Schöner, G., & Gielen, C. C. (1994a). Temporal stability of the action-perception cycle for postural control in a moving visual environment. Experimental Brain Research, 97, 477–486. Dijkstra, T. M., Schöner, G., Giese, M. A., & Gielen, C. C. (1994b). Frequency dependence of the action-perception cycle for postural control in a moving visual environment: Relative phase dynamics. Biological Cybernetics, 71, 489–501. Hajnal, A., Richardson, M. J., Harrison, S. J., & Schmidt, R. C. (2009). Location but not amount of stimulus occlusion influences the stability of visuo-motor coordination. Experimental Brain Research, 199, 89–93. Haken, H., Kelso, J. A. S., & Bunz, H. (1985). A theoretical model of phase transitions in human hand movements. Biological Cybernetics, 51, 347–356. Henriques, D. Y., & Crawford, J. D. (2002). Role of eye, head, and shoulder geometry in the planning of accurate arm movements. Journal of Neurophysiology, 87, 1677–1685. Issartel, J., Marin, L., & Cadopi, M. (2007). Unintended interpersonal co-ordination: ‘‘Can we march to the beat of our own drum?’’. Neuroscience Letters, 411, 174–179. Kandel, E. R., Schwartz, J. H., Jessell, T. M., Siegelbaum, S. A., & Hudspeth, A. J. (1991). Principles of neural science (Vol. 3). Elsevier: New York. Kay, B. A., Kelso, J. A. S., Saltzman, E. L., & Schöner, G. (1987). Space-time behavior of single and bimanual rhythmical movements: Data and limit cycle model. Journal of Experimental Psychology: Human Perception and Performance, 13, 178–192. Kelso, J. A. S. (1995). Dynamic patterns: The self-organization of brain and behavior. Cambridge, MA: MIT Press. Koken, P. W., & Erkelens, C. J. (1992). Influences of hand movements on eye movements in tracking tasks in man. Experimental Brain Research, 88, 657–664. Leist, A., Freund, H. J., & Cohen, B. (1987). Comparative characteristics of eye and hand tracking in humans. Human Neurobiology, 6, 19–26. Lopresti-Goodman, S. M., Richardson, M. J., Silva, P., & Schmidt, R. C. (2008). Period basin of entrainment for unintentional visual coordination. Journal of Motor Behavior, 40, 3–10. Lunenburger, L., Kutz, D. F., & Hoffmann, K. P. (2000). Influence of arm movements on saccades in humans. European Journal of Neuroscience, 12, 4107–4116. Oullier, O., de Guzman, G., Jantzen, K. J., Lagarde, J., & Kelso, J. A. S. (2008). Social coordination dynamics: Visual information exchange mediates spontaneous phase synchrony between people. Social Neuroscience, 3, 178–192. Peper, C. E., & Beek, P. J. (1998a). Are frequency-induced transitions in rhythmic coordination mediated by a drop in amplitude? Biological Cybernetics, 79, 291–300. Peper, C. E., & Beek, P. J. (1998b). Distinguishing between the effects of frequency and amplitude on interlimb coupling in tapping a 2:3 polyrhythm. Experimental Brain Research, 118, 78–92. Peper, C. E., & Beek, P. J. (1999). Modeling rhythmic interlimb coordination: The roles of movement amplitude and time delays. Human Movement Science, 18, 263–280. Peper, C. E., de Boer, B. J., de Poel, H. J., & Beek, P. J. (2008). Interlimb coupling strength scales with movement amplitude. Neuroscience Letters, 437, 10–14. Pikovsky, A., Rosenblum, M., & Kurths, J. (2001). Synchronization: A universal concept in nonlinear science. New York: Cambridge University Press. Post, A. A., Peper, C. E., & Beek, P. J. (2000). Relative phase dynamics in perturbed interlimb coordination: The effects of frequency and amplitude. Biological Cybernetics, 83, 529–542.

Please cite this article in press as: Varlet, M., et al. Influence of stimulus amplitude on unintended visuomotor entrainment. Human Movement Science (2011), doi:10.1016/j.humov.2011.08.002

12

M. Varlet et al. / Human Movement Science xxx (2011) xxx–xxx

Richardson, M. J., Campbell, W., & Schmidt, R. C. (2009). Movement interference during action observation as emergent coordination. Neuroscience Letters, 449, 117–122. Richardson, M. J., Marsh, K. L., Isenhower, R., Goodman, J., & Schmidt, R. C. (2007). Rocking together: Dynamics of intentional and unintentional interpersonal coordination. Human Movement Science, 26, 867–891. Richardson, M. J., Marsh, K. L., & Schmidt, R. C. (2005). Effects of visual and verbal information on unintentional interpersonal coordination. Journal of Experimental Psychology: Human Perception and Performance, 31, 62–79. Ridderikhoff, A., Peper, C. E., & Beek, P. J. (2005). Unraveling interlimb interactions underlying bimanual coordination. Journal of Neurophysiology, 94, 3112. Roerdink, M., Ophoff, E. D., Peper, C. E., & Beek, P. J. (2008). Visual and musculoskeletal underpinnings of anchoring in rhythmic visuo-motor tracking. Experimental Brain Research, 184, 143–156. Roerdink, M., Peper, C. E., & Beek, P. J. (2005). Effects of correct and transformed visual feedback on rhythmic visuo-motor tracking: Tracking performance and visual search behavior. Human Movement Science, 24, 379–402. Rosenbaum, D. A., Slotta, J. D., Vaughan, J., & Plamondon, R. (1991). Optimal movement selection. Psychological Science, 2, 86–91. Schmidt, R. C., Carello, C., & Turvey, M. T. (1990). Phase transitions and critical fluctuations in the visual coordination of rhythmic movements between people. Journal of Experimental Psychology: Human Perception and Performance, 16(2), 227. Schmidt, R. C., Mergeche, J., Bucci, C., & Richardson, M. J. (2010). How important is direction change information for spontaneous entrainment? Poster presented at the Annual North American Meeting of the International Society for Ecological Psychology. IL: Normal. Schmidt, R. C., & O’Brien, B. (1997). Evaluating the dynamics of unintended interpersonal coordination. Ecological Psychology, 9, 189–206. Schmidt, R. C., & Richardson, M. J. (2008). Dynamics of interpersonal coordination. Coordination: Neural, behavioral and social dynamics, 281–308. Schmidt, R. C., Richardson, M. J., Arsenault, C. A., & Galantucci, B. (2007). Visual tracking and entrainment to an environmental rhythm. Journal of Experimental Psychology: Human Perception and Performance, 33, 860–870. Shockley, K. D., Santana, M. V., & Fowler, C. A. (2003). Mutual interpersonal postural constraints are involved in cooperative conversation. Journal of Experimental Psychology: Human Perception and Performance, 29, 326–332. Snyder, L. H., Calton, J. L., Dickinson, A. R., & Lawrence, B. M. (2002). Eye-hand coordination: Saccades are faster when accompanied by a coordinated arm movement. Journal of Neurophysiology, 87, 2279–2286. Swinnen, S. P., Dounskaia, N., Levin, O., & Duysens, J. (2001). Constraints during bimanual coordination: The role of direction in relation to amplitude and force requirements. Behavioral Brain Research, 123, 201–218. Tognoli, E., Lagarde, J., de Guzman, G. C., & Kelso, J. A. S. (2007). The phi complex as a neuromarker of human social coordination. Proceedings of the National Academy of Science of the United States of America, 104, 8190–8195. van Donkelaar, P. (1997). Eye-hand interactions during goal-directed pointing movements. NeuroReport, 8, 2139–2142. van Ulzen, N. R., Lamoth, C. J., Daffertshofer, A., Semin, G. R., & Beek, P. J. (2008). Characteristics of instructed and uninstructed interpersonal coordination while walking side-by-side. Neuroscience Letters, 432, 88–93. Varlet, M., Marin, L., Lagarde, J., & Bardy, B. G. (2011). Social postural coordination. Journal of Experimental Psychology: Human Perception and Performance, 37, 473–483. von Holst, E. (1973). Relative coordination as a phenomenon and as a method of analysis of central nervous functions. In R. Martin (Ed.), The collected papers of Erich von Holst, Vol. 1: The behavioral physiology of animals and man (pp. 33–135). Coral Gables, FL: University of Miami Press. Wilson, A. D., Collins, D. R., & Bingham, G. P. (2005). Perceptual coupling in rhythmic movement coordination: Stable perception leads to stable action. Experimental Brain Research, 164, 517–528. Wimmers, R. H., Beek, P. J., & van Wieringen, P. C. W. (1992). Phase transitions in rhythmic tracking movements: A case of unilateral coupling. Human Movement Science, 11, 217–226. Zaal, F. T., Bingham, G. P., & Schmidt, R. C. (2000). Visual perception of mean relative phase and phase variability. Journal of Experimental Psychology: Human Perception and Performance, 26, 1209–1220.

Please cite this article in press as: Varlet, M., et al. Influence of stimulus amplitude on unintended visuomotor entrainment. Human Movement Science (2011), doi:10.1016/j.humov.2011.08.002