Research ReportMore precise tracking of horizontal than vertical target motion with both the eyes and hand
Introduction
People direct their gaze at important objects. Doing so presumably helps prevent collisions with them if they are obstacles and helps one to reach them if the goal is for instance to grasp them (Johansson et al., 2001). If such objects or the observer is moving, or both are moving, the eyes move to maintain gaze on the object of interest (Barnes, 2008; Spering et al., 2011). Although it is not evident that it is more important to keep the image of a moving object of interest close to the fovea in the horizontal than in the vertical direction, it has repeatedly been shown that horizontal components of pursuit eye movements are more accurate than vertical ones. This has been demonstrated for children (Grönqvist et al., 2006; Robert et al., 2014; Takeichi et al., 2003), adults (Baloh et al., 1988; Collewijn & Tamminga, 1984; Ke et al., 2013; Lipton et al., 1980; Rottach et al., 1996), and even cats and monkeys (Evinger & Fuchs, 1978; Kettner et al., 1996). More precise horizontal tracking has not only been found when motion of the target is restricted to the vertical or horizontal axis (Baloh et al., 1988; Lipton et al., 1980; Robert et al., 2014), it is also observed for the horizontal and vertical components of pursuit of a target that is moving in both dimensions (Ke et al., 2013; Kettner et al., 1996; Soechting et al., 2010). The possibility of having direction-dependent differences in the precision of pursuit is in line with neurophysiological studies arguing for separate neural substrates for horizontal and vertical eye movements (Chubb et al., 1984; Kettner et al., 1996; Saito & Sugimura, 2020).
Despite all this evidence that horizontal components of pursuit eye movements are more precise than vertical ones, the reason(s) for this directional asymmetry remains largely unknown. It has been suggested that everyday experience may be responsible for this bias, because in daily life objects that are pursued tend to mainly move horizontally (Collewijn & Tamminga, 1984). Even if this is the case, it is not evident whether the asymmetry arises because horizontal target motion is predicted better or because horizontal movements of the eyes are controlled more precisely. To determine which is more likely, we make use of the fact that we know that when tracking a visual target with the hand, the eyes also track the target (Danion & Flanagan, 2018; Niehorster et al., 2015; Xia & Barnes, 1999). We investigate whether the directional asymmetry that has been found during isolated eye movements is also present during manual tracking of a target that moves in a haphazard manner across a frontal plane, and if so, whether the asymmetry in eye movements is accompanied by a similar asymmetry in hand movements. We reason that if tracking is more precise in the horizontal than in the vertical direction for both eye and hand movements, the directional asymmetry is likely to result from better prediction of the target's motion along the horizontal axis, rather than from the control of the movement itself independently being more precise for horizontal movements of both the eye and hand. If the directional asymmetry arises from better prediction we also expect tracking errors to be correlated across the effectors. Although prediction is believed to play an important role in many aspects of human behaviour (Bar, 2007; Bubic et al., 2010; Clark, 2013) its role in guiding movements is still being debated (Fiehler et al., 2019; Zhao & Warren, 2017) as are the neural mechanisms involved (see Hogendoorn, 2020 for a recent overview), or the extent to which these mechanisms are shared across effectors (Binaee & Diaz, 2019).
The possibility that eye and hand movements exhibit a similar directional asymmetry is grounded upon the observation that there is an intricate relationship between eye and hand movements in tasks such as reaching (Crawford et al., 2004; Miall et al., 2001; Neggers & Bekkering, 2000; Prablanc et al., 1979) and intercepting (Binaee & Diaz, 2019; de la Malla et al., 2017; Mrotek & Soechting, 2007; but see Càmara, Lòpez-Moliner, Brenner, & de la Malla, 2020), as well as tracking (Bock, 1987; Danion & Flanagan, 2018; Huang & Hwang, 2012; Koken & Erkelens, 1992; Mather & Putchat, 1983; Miall et al., 2001; Niehorster et al., 2015). In tracking, making eye movements is believed to help guide the hand (Danion & Flanagan, 2018; Gouirand et al., 2019), but making hand movements is also believed to help keep the eyes on the target (Danion & Flanagan, 2018; Huang & Hwang, 2012; Koken & Erkelens, 1992; Mather & Putchat, 1983; Niehorster et al., 2015), in particular by increasing smooth pursuit gain and thereby decreasing the number of catch-up saccades. There is some evidence that horizontal eye movements are more precise than vertical ones in a manual interception task (Mrotek & Soechting, 2007), but in that study the asymmetry was observed before the hand started to move, and there was no comparison between the precision of horizontal and vertical hand movements.
Here, we reanalyse the data of previous studies in which a large set of participants were asked to move a cursor with a joystick so that it tracked a visual target that followed a smooth but unpredictable trajectory in the frontal plane (Gouirand et al., 2019; Mathew et al., 2018, 2019). Having simultaneously recorded both eye and hand movements in our previous studies allows us not only to assess the directional asymmetry in precision for each effector, but also to compare this asymmetry across effectors. Since the motion that participants were asked to track is smooth but not completely predictable, we expect participants to try to anticipate the target's future path, but not to be able to do this so well that tracking is almost perfect. This will allow us to quantify differences between the horizontal and vertical lag and precision of movements of both the eye and hand with respect to the target's motion.
Section snippets
Participants
We made no attempt to estimate the required sample size but simply used all the initial data from three previous studies that all started in the same way, giving us data for sixty-two right-handed volunteers (31 females; 26.8 ± 6.2 years of age; from here on this notation will be used to indicate mean ± standard deviation). The data are from the initial, identical baseline trials of three separate groups of participants, from three separate experiments (Gouirand et al., 2019; Mathew et al., 2018
Representative trial
Fig. 3 shows one representative trial. In this example, vertical tracking looks somewhat poorer than horizontal tracking both for the eye and the hand. In the next sections this observation will be analysed in more detail.
Eye tracking performance
Eye tracking of the target was typically more accurate in the horizontal direction than in the vertical one. The mean absolute distance between gaze and target was .84 cm in the horizontal direction and .99 cm in the vertical direction [F(1,61) = 18.42; p < .001; repeated
Discussion
Our main objective was to investigate the possible asymmetry between vertical and horizontal tracking with the hand and eyes during manual tracking. Our results can be summarized with the following key findings. First, we observed that both the eye and hand consistently tracked the target more precisely along the horizontal axis than along the vertical one. Second, significantly smaller residual errors were obtained when considering separate lags for horizontal and vertical tracking than when
Contributions
FRD and EB initiated the study that is based on data originally collected by FRD, NG and JM. All authors analysed data. FRD and EB drafted the manuscript and the figures.
Open practices
The study in this article earned Open Materials and Open Data badges for transparent practices. Materials and data for the study are available at https://doi.org/10.5281/zenodo.3923579.
Declaration of competing interest
The authors state they have no conflict of interest.
Acknowledgement
We thank Cédric Goulon and Franck Buloup for technical support and providing respectively their ICE and Docometre software (courtesy of Institut des Sciences du Mouvement, Marseille, France). This work was part of Innovative Training Network ‘Perception and Action in Complex Environment’ (PACE) that has received funding from the European Union’s Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant agreement N° 642961. This paper reflects only the authors' view and
References (61)
The proactive brain : Using analogies and associations to generate predictions
Trends in cognitive sciences
(2007)Cognitive processes involved in smooth pursuit eye movements
Brain and Cognition
(2008)Coordination of arm and eye movements in tracking of sinusoidally moving targets
Behavioural Brain Research
(1987)Eye-hand coordination : Eye to hand or hand to eye?
Current Biology: CB
(2000)- et al.
Coupling of hand and foot voluntary oscillations in patients suffering cerebellar ataxia : Different effect of lateral or medial lesions on coordination
- et al.
Developmental asymmetries between horizontal and vertical tracking
Vision Research
(2006) - et al.
Orientational asymmetries in small-field optokinetic nystagmus in human infants
Behavioural Brain Research
(1984) - et al.
Horizontal and vertical pursuit eye movements, the oculocephalic reflex, and the functional psychoses
Psychiatry Research
(1980) - et al.
Comparison of horizontal, vertical and diagonal smooth pursuit eye movements in normal human subjects
Vision Research
(1996) - et al.
Intercepting a moving target : On-line or model-based control?
Journal of Vision
(2017)
A comparison of the dynamics of horizontal and vertical smooth pursuit in normal human subjects
Aviation, Space, and Environmental Medicine
Movements of the eyes and hands are coordinated by a common predictive strategy
Journal of Vision
Fast responses of the human hand to changes in target position
Journal of Motor Behavior
Prediction, cognition and the brain
Frontiers in Human Neuroscience
Looking away from a moving target does not disrupt the way in which the movement toward the target is guided
Journal of Vision
Neuron activity in monkey vestibular nuclei during vertical vestibular stimulation and eye movements
Journal of Neurophysiology
Whatever next? Predictive brains, situated agents, and the future of cognitive science
The Behavioral and Brain Sciences
Human smooth and saccadic eye movements during voluntary pursuit of different target motions on different backgrounds
The Journal of Physiology
Spatial transformations for eye-hand coordination
Journal of Neurophysiology
Optimal integration of gravity in trajectory planning of vertical pointing movements
Journal of Neurophysiology
Visuomotor feedback gains are modulated by gaze position
Journal of Neurophysiology
Potential systematic interception errors are avoided when tracking the target with one's eyes
Scientific Reports
Different gaze strategies during eye versus hand tracking of a moving target
Scientific Reports
Saccadic, smooth pursuit, and optokinetic eye movements of the trained cat
The Journal of Physiology
Prediction in goal-directed action
Journal of Vision
The inertial anisotropy of the arm is accurately predicted during movement planning
The Journal of Neuroscience: the Official Journal of the Society for Neuroscience
Oculo-manual tracking of visual targets : Control learning, coordination control and coordination model
Experimental Brain Research
Eye movements do not play an important role in the adaptation of hand tracking to a visuomotor rotation
Journal of Neurophysiology
Independent selection of eye and hand targets suggests effector-specific attentional mechanisms
Scientific Reports
Motion extrapolation in visual Processing : Lessons from 25 Years of flash-lag debate
The Journal of Neuroscience: the Official Journal of the Society for Neuroscience
Cited by (2)
- 1
Current affiliation: Institute of Neuroscience, Institute of Communication & Information Technologies, Electronics & Applied Mathematics, Université Catholique de Louvain, Belgium.