Elsevier

Human Movement Science

Volume 41, June 2015, Pages 265-281
Human Movement Science

Informational constraints on spontaneous visuomotor entrainment

https://doi.org/10.1016/j.humov.2015.03.011Get rights and content

Highlights

  • Limb movements spontaneously entrain to environmental visual rhythms.

  • Stronger entrainment occurs to visual rhythms tracked with the eyes.

  • Enhanced entrainment seems not to be supported by eye–limb neuromuscular synergies.

  • Eye-tracking strengthens entrainment by allowing the pick-up of more information.

  • Informational constraints modulate motor coordination dynamics.

Abstract

Past research has revealed that an individual’s rhythmic limb movements become spontaneously entrained to an environmental rhythm if visual information about the rhythm is available and its frequency is near that of the individual’s movements. Research has also demonstrated that if the eyes track an environmental stimulus, the spontaneous entrainment to the rhythm is strengthened. One hypothesis explaining this enhancement of spontaneous entrainment is that the limb movements and eye movements are linked through a neuromuscular coupling or synergy. Another is that eye-tracking facilitates the pick up of important coordinating information. Experiment 1 investigated the first hypothesis by evaluating whether any rhythmic movement of the eyes would facilitate spontaneous entrainment. Experiments 2 and 3 (respectively) explored whether eye-tracking strengthens spontaneous entrainment by allowing the pickup of trajectory direction change information or allowing an increase in the amount of information to be picked-up. Results suggest that the eye-tracking enhancement of spontaneous entrainment is a consequence of increasing the amount of information available to be picked-up.

Introduction

The movements of people are often entrained to external or environmental visual rhythms. Such coordination occurs for example when juggling with three or more balls, when the hands of a juggler become coordinated in time and space with the movements of the balls (Beek, 1989, Beek and Turvey, 1992). The movements of an individual are also often coordinated to the rhythmic movements produced by other people (Schmidt & Richardson, 2008). The postural or limb movements of two or more people tend to spontaneously synchronize when talking, walking or acting together for instance (Néda et al., 2000, Ramenzoni et al., 2011, Schmidt and O’Brien, 1997, Shockley et al., 2003, Tognoli et al., 2007, van Ulzen et al., 2008, Varlet et al., 2011). Such interpersonal visuomotor coordination has received a growing amount of attention from researchers because there is evidence that it modulates the success of everyday social interactions (Marsh et al., 2009, Wiltermuth and Heath, 2009). Coordinated movements in a dyad or group of people can enhance for example feelings such as social connectedness, affiliation and even the efficiency of their communication (Bernieri, 1988, Chartrand and Bargh, 1999, Hove and Risen, 2009, Miles et al., 2011, Richardson et al., 2007, Shockley et al., 2009, Wiltermuth and Heath, 2009).

Previous research has found that the dynamics of visuomotor coordination is modulated by how the actor visually attends to the movements of the external or environmental stimulus (Huys and Beek, 2002, Richardson et al., 2007, Roerdink et al., 2013, Roerdink et al., 2008, Roerdink et al., 2005, Schmidt et al., 2007). In particular, it has been shown that the occurrence of spontaneous visuomotor entrainment depends on whether or not the actor visually tracked the movements of the stimulus with the eyes (Romero et al., 2012, Schmidt et al., 2007, Varlet et al., 2012a). Specifically, tracking a stimulus with the eyes has been found to enhance entrainment. The origin of this effect, however, remains largely unknown. Here we present three experiments that were aimed at gaining a better understanding of the influence of eye movements on the occurrence of spontaneous visuomotor entrainment.

Numerous studies have demonstrated that the dynamics of rhythmic visuomotor coordination can be understood as constrained by the dynamical entrainment processes of interacting oscillators (Byblow et al., 1995, Coey et al., 2011, de Rugy et al., 2008, Peper and Beek, 1998, Richardson et al., 2007, Schmidt et al., 1990, Schmidt and O’Brien, 1997, Snapp-Childs et al., 2011, Tognoli et al., 2007, Wimmers et al., 1992). These processes have been found to underlie the organization and stability of a wide range of oscillatory systems involving a variety of components (Pikovsky et al., 2001, Strogatz, 2003). This includes for instance the emergence of coordinated behavior in groups of planets, neurons or humans. Previous studies that investigated rhythmic bimanual coordination provided the first evidence of dynamical entrainment processes in human movement systems (Haken et al., 1985, Kelso, 1984, Kelso, 1995, Schöner et al., 1986). Coupled by neuromuscular information, the movements of two hands of an individual become spontaneously synchronized (Kelso, Southard, & Goodman, 1979). Such synchronization occurs in one of two possible modes: an in-phase pattern of coordination where the hands move at the same time in the same direction or an anti-phase pattern of coordination where the hands move at the same time in opposite direction (Kelso, 1984, Kelso, 1995). In addition, previous research has shown that anti-phase coordination is less stable than in-phase coordination as indicated by greater variability and can only be maintained for slow to moderate movement frequencies (Kelso, 1984, Kelso, 1995). Typical of coupled oscillators systems, the occurrence and stability of rhythmic bimanual coordination has also been found to depend on the difference between the preferred or natural movement frequencies of each hand (Fuchs et al., 1996, Sternad et al., 1992). This effect has been largely illustrated in previous research using a wrist pendulum paradigm (Schmidt et al., 1993, Sternad et al., 1992, Treffner and Turvey, 1995). In these studies, participants are instructed to swing and coordinate hand-held pendulums about the wrist that either have the same or different natural frequencies (manipulated by changing the position of the mass attached). The results demonstrate that the most stable coordination occurs when participants are instructed to coordinate identical pendulums (Schmidt et al., 1993, Sternad et al., 1992, Treffner and Turvey, 1995). Furthermore, the stability of the coordination progressively decreased, the greater the difference between the pendulums’ natural frequencies.

Of particular relevance for the current study is that such dynamical entrainment processes have not only been found between the limb movements of a single individual (i.e., intrapersonal coordination), but also between the limb movements of an individual and external visual rhythms, including the rhythmic movements produced by other people (i.e., interpersonal coordination) (Issartel et al., 2007, Lopresti-Goodman et al., 2008, Peper and Beek, 1998, Schmidt and O’Brien, 1997, Tognoli et al., 2007, van Ulzen et al., 2008, Varlet et al., 2012a, Wimmers et al., 1992). That is, when an individual is visually coupled to a stimulus movement or rhythm, the movements of the individual can become spontaneously synchronized toward an in-phase or anti-phase pattern of coordination. As with interpersonal interlimb coordination, in-phase is more stable than anti-phase and tends to be observed more often. Moreover, the stability of such visuomotor coordination is similarly modulated by the difference between preferred movement frequencies of the actor and the observed stimulus rhythm (Lopresti-Goodman et al., 2008, Richardson et al., 2005, Schmidt and O’Brien, 1997).

Visuomotor coordination, however, is typically weaker and less stable than intrapersonal coordination (i.e., coordination between or within limbs’ movements of an individual) (Richardson et al., 2008, Schmidt et al., 1998). The decreased stability of visuomotor coordination is due in part to the nature of the visual coupling, which is weaker than the neuromuscular coupling that characterizes intrapersonal interlimb coordination. The movement intention of the actor when viewing stimulus rhythm also plays a significant role in shaping the stability and intermittency of visuomotor coordination. Although still more variable than intrapersonal interlimb coordination, when an actor intends to coordinate with a visual rhythm the coordination can be maintained absolutely, in that movements of the actor become phase locked with the visual rhythm in either an in-phase and anti-phase pattern over time. When an actor has no specific intention to coordinate with an observed stimulus rhythm, coordination can still occur, however tends to be relative (instead of absolute) or intermittent (von Holst, 1973) with the actor spontaneously falling in and out of coordination over time. For such unintentional or spontaneous coordination the difference between the participant preferred movement frequency and stimulus frequency has to be small enough to be compensated by a weak visual coupling (Lopresti-Goodman et al., 2008). Otherwise, the limb of the participant moves in time and space totally independent of the stimulus’ movements and no spontaneous entrainment or coordination appears. However, there is evidence that the strength of such a visual coupling is mediated by the degree to which an actor attends to the displacements of the external or environmental rhythm (Richardson et al., 2007, Schmidt et al., 2007).

More specifically, previous research has shown that the stability of the coordination depends on whether the actor visually tracked stimulus displacements with eye movements (Romero et al., 2012, Schmidt et al., 2007, Varlet et al., 2012a). Schmidt et al. (2007) investigated the spontaneous entrainment between the pendulum swinging of participants and a visual stimulus that oscillated horizontally on a projection screen. Participants were instructed to oscillate their pendulum at their preferred tempo and maintain this tempo while reading letters that were displayed at random intervals on the screen. The letters occurred either just above the middle of the trajectory of the oscillating visual stimulus (i.e., non-tracking condition) or on the oscillating stimulus itself (tracking condition). Although participants were only instructed to maintain their preferred tempo, the results demonstrated that their movements became spontaneously and intermittently synchronized with the stimulus movements in both the tracking and non-tracking conditions. More importantly, the results revealed that synchronization was stronger in the tracking condition (i.e., when participants tracked the stimulus displacements with their eyes) as indicated by more occurrence of in-phase or anti-phase coordination.

Although these results have been replicated in other studies (Romero et al., 2012, Varlet et al., 2012a), the origin of this constructive eye-tacking effect on spontaneous visuomotor entrainment is still an open question. Specifically, why does tracking a stimulus movement with the eyes increase the occurrence of spontaneous visuomotor entrainment? A possible explanation is that the movements of the eyes establish an intrapersonal eye–limb neuromuscular coupling or synergy that when added to the visual coupling increases the entrainment. Numerous studies have found mutual influences between eye and limbs’ movements and support the existence of such a neuromuscular coupling (Engel et al., 2000, Falciati et al., 2013, Gauthier et al., 1988, Koken and Erkelens, 1992, Lünenburger et al., 2000, Maioli et al., 2007, van Donkelaar et al., 2000). First, there is evidence that the movements of a limb can influence the dynamics of eye movements. Saccadic eye movements are faster when they are accompanied by arm movements, for instance (Lünenburger et al., 2000, Snyder et al., 2002). The movements of a limb also modulate the dynamics of smooth pursuit eye movements. For example, the efficiency of smooth visual pursuit can be enhanced when an actor also tracks the moving target with his or her arm (Gauthier et al., 1988, Koken and Erkelens, 1992, Leist et al., 1987, van Donkelaar and Lee, 1994). Changes in smooth visual pursuit have also been found during manual tracking when perturbations were applied to the actors’ moving arm (Scarchilli & Vercher, 1999). Inversely, there is also evidence that eye movements can influence the dynamics of limbs’ movements (Henriques and Crawford, 2002, van Donkelaar, 1997). Previous research has shown for example that saccadic eye movements can increase the accuracy of limb movements when performed simultaneously (Abrams, Meyer, & Kornblum, 1990). The execution of arm movements has been found to be faster when accompanied by saccade eye movements (Gueugneau, Crognier, & Papaxanthis, 2008). The limbs movements of an individual are also influenced by smooth pursuit eye movements (Hiraoka et al., 2013, Maioli et al., 2007). Maioli et al. (2007), for example, has demonstrated changes in corticospinal excitability of arm and hand muscles during smooth pursuit eye movements. Together, these results provide evidence of a synergistic relation between eye and limb movements and support the assumption that enhancement of visuomotor entrainment with eye tracking might originate from an intrapersonal eye–limb neuromuscular coupling.

Another possibility for the constructive effects of visual tracking on visuomotor synchronization is that visual tracking increases the ability of an actor to detect the kinematic information that best supports such coordination. Previous studies on intentional visuomotor coordination have demonstrated that certain locations of the movement trajectory of an oscillating visual stimulus contain particularly pertinent movement information for stable coordination making it possible for visual tracking to facilitate the pick up of this information. In particular, this research has shown that when an actor intentionally coordinates the movement of a limb with a stimulus oscillating horizontally, he or she tends to preferentially pick up information about stimulus displacements by gazing at the endpoints of its trajectory (Roerdink et al., 2005). Such gaze behaviors principally occur for stimuli oscillating at fast frequencies — when eye-tracking, and thus the pick up of the entire stimulus trajectory, become inefficient due to physiological limitations of smooth pursuit eye movements (Roerdink et al., 2005). Consistent with these findings, other research has shown that fixations on the turn-around points of the stimulus trajectory result in participants’ movements being locally more anchored in time and space, which favors stable coordination (Beek, 1989, Byblow et al., 1994, Fink et al., 2000, Roerdink et al., 2005, Roerdink et al., 2008, Roerdink et al., 2013). Also confirming the importance of the turn-around points of the stimulus trajectory is previous research that occluded different locations of the movement trajectory of an oscillating stimulus when participants performed an intended in-phase or anti-phase coordination (Hajnal et al., 2009, Huys et al., 2005). Results revealed that the least stable coordination occurred when the turn-around points or endpoints of the stimulus trajectory were occluded, which further demonstrates that they are the privileged parts of the trajectory providing critical movement information. The importance of the turn-around points of oscillating stimuli might be explained by the slowness of this part of the trajectory, which would facilitate the detection of critical movement information (Bingham, 2004, Bingham et al., 2001, Hajnal et al., 2009, Wilson et al., 2005, Koken and Erkelens, 1992, Zaal et al., 2000). Supporting this latter assumption is recent study that investigated visuomotor coordination with different stimulus velocity profiles, which demonstrated that greater slowdown to the endpoints of the stimulus trajectory enhanced entrainment (Varlet et al., 2014).

The past research outlined above, therefore, suggests two hypotheses for why eye tracking increases spontaneous or unintentional visuomotor entrainment. One hypothesis is that the limb movements entrain to the moving eyes through a neuromuscular coupling or synergy linking the eyes and limb and when added to visual coupling reinforces the entrainment. Another hypothesis is that entrainment is strengthened because eye tracking allows for the pick up of important movement information at the endpoints or turn-around points of the movement trajectory of the stimulus. The following three experiments were aimed at investigating these two hypotheses.

Section snippets

Experiment 1

The current experiment investigated whether the eye-tracking enhancement of spontaneous visuomotor entrainment is due to a neuromuscular eye–limb coupling in which the movement of the eyes entrains the movement of the limbs. This hypothesis predicts that any rhythmic movement of the eyes at the same tempo of a stimulus should be sufficient to enhance the occurrence and magnitude of spontaneous entrainment between an individual’s rhythmic limb movements and an oscillating visual stimulus.

Experiment 2

One explanation for the eye-tracking enhancement of spontaneous visuomotor entrainment is that eye tracking allows information about the trajectory endpoints, which contains important direction-change information, to be picked, hence, enhancing coordination. As explained in the introduction, evidence supporting the importance of trajectory endpoints or turn-around points comes from a number of different studies. Hajnal et al. (2009) occluded different parts of the trajectory of an oscillating

Experiment 3

Although the previous experiment discounts the possibility that eye-tracking enhances spontaneous entrainment because it allows coordination relevant information at the turn-around points of the trajectory to be picked-up, the possibility remains that eye-tracking enhances spontaneous entrainment because it allows a greater amount of information to be picked-up. Accordingly, this last experiment manipulated the amount of information available about a rhythmic stimulus while controlling eye

General discussion

Previous research has shown that the limb movements of an actor become spontaneously coordinated with the movements of external or environmental visual rhythms and that such entrainment is stronger when the actor visually tracked the movements of the stimulus with the movements of the eye. The aim of the present study was to understand why this is. Across three experiments, we addressed two possible explanations of this phenomenon. The first is that a neuromuscular coupling or synergy between

Acknowledgments

This research was supported by National Science Foundation Awards BCS-0750187 and BCS-0750190, Agence Nationale de la Recherche grant (Project SCAD # NT09_457350) and National Institutes of Health Grant R01GM105045. The authors thank Samantha Morr for her help with the figures.

References (94)

  • N.R. van Ulzen et al.

    Characteristics of instructed and uninstructed interpersonal coordination while walking side-by-side

    Neuroscience Letters

    (2008)
  • M. Varlet et al.

    Influence of stimulus amplitude on unintended visuomotor entrainment

    Human Movement Science

    (2012)
  • R.H. Wimmers et al.

    Phase transitions in rhythmic tracking movements: A case of unilateral coupling

    Human Movement Science

    (1992)
  • R.A. Abrams et al.

    Eye–hand coordination: Oculomotor control in rapid aimed limb movements

    Journal of Experimental Psychology: Human Perception and Performance

    (1990)
  • P.J. Beek

    Juggling dynamics

    (1989)
  • P.J. Beek et al.

    Temporal patterning in cascade juggling

    Journal of Experimental Psychology: Human Perception and Performance

    (1992)
  • F.J. Bernieri

    Coordinated movement and rapport in teacher–student interactions

    Journal of Nonverbal Behavior

    (1988)
  • G.P. Bingham

    A perceptually driven dynamical model of bimanual rhythmic movement (and phase perception)

    Ecological Psychology

    (2004)
  • G.P. Bingham et al.

    The effect of frequency on the visual perception of relative phase and phase variability of two oscillating objects

    Experimental Brain Research

    (2001)
  • W.D. Byblow et al.

    Asymmetries in coupling dynamics of perception and action

    Journal of Motor Behavior

    (1995)
  • T.L. Chartrand et al.

    The chameleon effect: The perception–behavior link and social interaction

    Journal of Personality and Social Psychology

    (1999)
  • C. Coey et al.

    Effects of movement stability and congruency on the emergence of spontaneous interpersonal coordination

    Experimental Brain Research

    (2011)
  • K.M. Dalton et al.

    Gaze fixation and the neural circuitry of face processing in autism

    Nature Neuroscience

    (2005)
  • A.J. de Brouwer et al.

    Don’t rock the boat: How antiphase crew coordination affects rowing

    PLoS One

    (2013)
  • A. de Rugy et al.

    Stability of rhythmic visuo-motor tracking does not depend on relative velocity

    Experimental Brain Research

    (2008)
  • K.C. Engel et al.

    Similarity in the response of smooth pursuit and manual tracking to a change in the direction of target motion

    Journal of Neurophysiology

    (2000)
  • L. Falciati et al.

    Covert oculo-manual coupling induced by visually guided saccades

    Frontiers in Human Neuroscience

    (2013)
  • P.W. Fink et al.

    Local and global stabilization of coordination by sensory information

    Experimental Brain Research

    (2000)
  • P. Fitzpatrick et al.

    Dynamical methods for evaluating the time-dependent unfolding of social coordination in children with autism

    Frontiers in Integrative Neuroscience

    (2013)
  • A. Fuchs et al.

    Extending the HKB model of coordinated movement to oscillators with different eigenfrequencies

    Biological Cybernetics

    (1996)
  • G.M. Gauthier et al.

    Oculo-manual tracking of visual targets: Control learning, coordination control and coordination model

    Experimental Brain Research

    (1988)
  • J.J. Gibson

    Visually controlled locomotion and visual orientation in animals

    British Journal of Psychology

    (1958)
  • J.J. Gibson

    The senses considered as perceptual systems

    (1966)
  • J.J. Gibson

    The ecological approach to visual perception

    (1979)
  • A. Hajnal et al.

    Location but not amount of stimulus occlusion influences the stability of visuo-motor coordination

    Experimental Brain Research

    (2009)
  • H. Haken et al.

    A theoretical model of phase transitions in human hand movements

    Biological Cybernetics

    (1985)
  • D.Y.P. Henriques et al.

    Role of eye, head, and shoulder geometry in the planning of accurate arm movements

    Journal of Neurophysiology

    (2002)
  • K. Hiraoka et al.

    Interaction between the premotor processes of eye and hand movements: Possible mechanism underlying eye–hand coordination

    Somatosensory and Motor Research

    (2013)
  • P.S. Holzman et al.

    Eye-tracking patterns in schizophrenia

    Science

    (1973)
  • P.S. Holzman et al.

    Eye-tracking dysfunctions in schizophrenic patients and their relatives

    Archives of General Psychiatry

    (1974)
  • M.J. Hove et al.

    It’s all in the timing: Interpersonal synchrony increases affiliation

    Social Cognition

    (2009)
  • R. Huys et al.

    The coupling between point-of-gaze and ball movements in three-ball cascade juggling: The effects of expertise, pattern and tempo

    Journal of Sports Sciences

    (2002)
  • S. Kawase

    Gazing behavior and coordination during piano duo performance

    Attention, Perception, & Psychophysics

    (2014)
  • J.A. Kelso

    Phase transitions and critical behavior in human bimanual coordination

    American Journal of Physiology – Regulatory, Integrative and Comparative Physiology

    (1984)
  • J.A. Kelso

    Dynamic patterns: The self organization of brain and behaviour

    (1995)
  • J.A. Kelso et al.

    On the nature of human interlimb coordination

    Science

    (1979)
  • P.W. Koken et al.

    Influences of hand movements on eye movements in tracking tasks in man

    Experimental Brain Research

    (1992)
  • Cited by (17)

    • The influence of a conductor and co-performer on auditory-motor synchronisation, temporal prediction, and ancillary entrainment in a musical drumming task

      2020, Human Movement Science
      Citation Excerpt :

      In other words, partners will increase ancillary coherence most strongly when they have each other in view, but observing the same moving visual cue without seeing each other also increases ancillary coherence relative to the permuted pairs, albeit to a lesser degree. This is consistent with general findings that visual rhythms, even in the periphery, facilitate movement coordination, sometimes unintentionally (Clayton, 2007; Richardson et al., 2005; Schmidt et al., 2007; Varlet et al., 2015). It is also consistent with the finding that dyads show lower relative phase and lower standard deviation of relative phase when facing each other, but only on downward movements in a synchronisation dancing task (Miyata et al., 2017).

    • The dual influence of pacer continuity and pacer pattern for visuomotor synchronisation

      2018, Neuroscience Letters
      Citation Excerpt :

      The task required motion (maximal forearm flexions and extensions) triggered by the pacer dynamic, which could call on mechanisms similar to those involved when synchronising discrete movements. Experiment 1 showed a facilitation of VMS with a continuous pacer with a pattern of movement matching the pattern of the forearm movements of tracking, a conclusion that is consistent with previous research [5,17–21,45]. Our results suggest that both the continuity of the pacer and whether the pacer/movement patterns match contribute to this facilitation and that the former might have greater influence than the latter.

    • Investigation of the effects of transcranial alternating current stimulation (tACS) on self-paced rhythmic movements

      2017, Neuroscience
      Citation Excerpt :

      In these situations, body sway, arm or leg movements of interaction partners become entrained when there is an exchange of visual and/or auditory information. Human rhythmic movements also entrain to non-human external rhythms in the environment such as computer-generated sequences of visual and auditory stimulus (Repp and Penel, 2004; Schmidt et al., 2007; Varlet et al., 2015, 2016). Previous research has shown that spontaneous entrainment of human rhythmic movement preferentially occurs when the frequency of the external rhythm is close to the individual’s preferred movement frequency (Schmidt and O’Brien, 1997; Richardson et al., 2007; Varlet et al., 2015).

    • Neural tracking of visual periodic motion

      2023, European Journal of Neuroscience
    View all citing articles on Scopus
    View full text