Neuroscience Letters 588 (2015) 83–87
Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Regular article
Visuo-locomotor coordination for direction changes in a manual wheelchair as compared to biped locomotion in healthy subjects Caroline Charette a,b , Franc¸ois Routhier a,b , Bradford J. McFadyen a,b,∗ a b
Centre for Interdisciplinary Research in Rehabilitation and Social Integration (CIRRIS), Quebec City Rehabilitation Institute, Quebec, Canada Faculty of Medicine, Department of Rehabilitation, Laval University, Quebec, Canada
h i g h l i g h t s • Anticipatory head movement found for both wheelchair and biped locomotor modes. • Specific gaze behavior depends predominantly on the environmental demands. • Manual wheelchair navigation combines both biped and vehicular-based control.
a r t i c l e
i n f o
Article history: Received 30 September 2014 Received in revised form 19 December 2014 Accepted 2 January 2015 Available online 3 January 2015 Keywords: Gait Eye movements Steering Gaze behavior Wheelchair
a b s t r a c t The visual system during walking provides travel path and environmental information. Although the manual wheelchair (MWC) is also a frequent mode of locomotion, its underlying visuo-locomotor control is not well understood. This study begins to understand the visuo-locomotor coordination for MWC navigation in relation to biped gait during direction changes in healthy subjects. Eight healthy male subjects (26.9 ± 6.4 years) were asked to walk as well as to propel a MWC straight ahead and while changing direction by 45◦ to the right guided by a vertical pole. Body and MWC movement (speed, minimal clearance, point of deviation, temporal body coordination, relative timing of body rotations) and gaze behavior were analysed. There was a main speed effect for direction and a direction by mode interaction with slower speeds for MWC direction change. Point of deviation was later for MWC direction change and always involved a counter movement (seen for vehicular control) with greater minimal distance from the vertical pole as compared to biped gait. In straight ahead locomotion, subjects predominantly fixed their gaze on the end target for both locomotor modes while there was a clear trend for subjects to fixate on the vertical pole more for MWC direction change. When changing direction, head movement always preceded gaze changes, which was followed by trunk movement for both modes. Yet while subjects turned the trunk at the same time during approach regardless of locomotor mode, head movement was earlier for MWC locomotion. These results suggest that MWC navigation combines both biped locomotor and vehicularbased movement control. Head movement to anticipate path deviations and lead steering for locomotion appears to be stereotypic across locomotor modes, while specific gaze behavior predominantly depends on the environmental demands. © 2015 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Steering or changing direction towards a new intended travel path while walking requires sensory-motor coordination to reorient the body while still maintaining balance [1]. The visual system is a crucial part of steering because it provides spatio-temporal information about the desired travel path and general move-
∗ Corresponding author at: CIRRIS, 525 Boul. Wilfrid-Hamel, G1M 2S8, Québec, Canada. Tel.: +1 418 529 9141x6584; fax: +1 418 529 3548. E-mail address: [email protected] (B.J. McFadyen). http://dx.doi.org/10.1016/j.neulet.2015.01.002 0304-3940/© 2015 Elsevier Ireland Ltd. All rights reserved.
ment within the environment. There are many other ways to locomote through the environment including wheeled mobility (e.g., bicycles, scooters, wheelchairs and motorized vehicles). Yet while biped locomotion has been studied for a variety of navigational tasks (e.g., stepping over or circumventing obstacles, changing direction), there is less research on the strategies used for other locomotor modes and very little for manual wheelchair (MWC) locomotion. The MWC is a mode of self-propelled wheeled locomotion that is used frequently [2] but its underlying visuolocomotor control which involves very different head movement as compared to biped or other seated locomotion is still not well understood. In this study, we will focus on navigating
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to a new direction for comparing biped and MWC locomotor modes. For biped gait, steering involves a top-down sequence of body reorientation, starting with a rotation of the eyes and head towards the new travel path followed by the trunk and then the feet [1,3–5]. The anticipatory head movements are considered important to prepare and pre-programme adaptations within two steps prior to path deviations [6]. Specifically, it is suggested that these head movements provide an allocentric reference frame to re-orient the body [3] and steer towards the new direction of travel [7]. During adaptive locomotion, common characteristics of gaze behavior show that the majority of fixations are either directed towards a desired future path or an object of interest [4,8]. Moreover, prior to a direction change, individuals invariably make saccadic eye movements towards the end-point of the travel path, which allows the identification and extraction of information concerning the future path [4]. There are surprisingly few studies to understand the visuolocomotor coordination underlying MWC navigation, specifically during direction changes. However, Higuchi et al. [9] did compare biped and MWC locomotion, with respect to aperture perception in order to pass through doorways. They showed that able-bodied subjects underestimated their extended spatial requirements in a MWC, even after some practice, whereas they overestimated it when walking. The authors concluded that adaptation to altered body dimension is likely to occur very quickly under a familiar form of locomotion [9]. Higuchi et al. [10] also showed that while propelling a WC, able-bodied subjects tended to fixate more frequently on door edges, compared to walking. The authors suggested that the novelty of the locomotion mode caused participants to be more concerned about avoiding a collision with the door [10]. Although a MWC is not a car and does not have the constraints of a road environment in a high-speed context, it is a wheeled vehicle and may involve similar visually based navigational behavior. Land [11] likened the control of making right angle turns in a car to walking in that there is an anticipatory orienting head movement followed by the compensation for the head turning on the body within the car. It was also suggested that when turning a car along a curved road, drivers appear to focus on a tangent point on the inside of the curve of the road 1–2 s before turning [12]. Wilkie et al. [13], however, suggested the use of the tangent point was speed related and proposed a general strategy of «looking where you want to go» through gaze fixations onto points of the road at 1–2 s ahead. This is part of an active gaze theory proposed by Wilkie and Wann [14]. Finally, Land et al. [11] clearly showed that the car makes a countermovement in the opposite direction before turning along a curved road. MWC locomotion involves speeds that are more comparable to walking and thus allow us to compare the visuo-locomotor control between these two modes of locomotion. However, the MWC implies very different propulsion means with the involvement of upper body movement. Given that the MWC is also a common mode of locomotion for many people, it will be interesting to understand the relation to premorbid bipedal behavior for those now using a MWC. As a first important step, the goal of this study was to begin to understand the visuo-locomotor coordination for MWC navigation in relation to biped gait when changing direction in healthy subjects.
2. Material and methods 2.1. Participants Eight able-bodied adult male participants (mean age: 26.9 ± 6.4 years; height: 1.8 ± 0.1 m; mass: 76.5 ± 12.7 kg) were recruited.
Ethics approval was obtained from the Quebec City Rehabilitation Institute and all participants provided written informed consent. Subjects with any self-reported neurological or musculoskeletal problems or a score below 20/20 on the Snellen visual acuity test were excluded.
2.2. Data collection A motion analysis system (four Optotrak Certus motion sensors, NDI, 120 Hz) and seven triads of non-colinear infra-red markers (head, sternal notch, wrists, feet and on the MWC frame) were used to assess body and MWC movements. Gaze behavior data were collected using a commercial eye tracker (Mobile XG from Applied Sciences Laboratories, 30 Hz) that was synchronized with the Optotrak system.
2.3. Protocol Participants were trained for up to 20 min in the MWC (Quickie Q7 from Sunrise Medical) using some tasks of the Wheelchair Skills Training Program (www.wheelchairskillsprogram.ca). Subjects had to roll forwards (100 m), roll backwards (5 m), turn 90◦ (right and left) while moving forwards and backwards, turn in place (180◦ ) as well as ascend and descend a 5◦ and 10◦ incline. Then participants were asked to perform two experimental conditions, walking first and then propelling the MWC, both at comfortable self-selected speeds: (1) straight ahead along an 8.75 m path (SA condition) and (2) changing direction (CD condition) 45◦ to the right off the original straight ahead pathway at a specific point four metres from the start position as indicated by a black vertical pole (VP; 1.86 m height, 3.5 cm diameter). A round target was placed at the end of both paths and subjects were instructed to walk or propel the MWC to it. A corridor (0.92 m wide, 1.85 m long) was placed at the starting point to indicate an initial straight propulsion zone (see below). The vertical pole used for the CD condition was aligned with the right boarder of this corridor.
2.4. Data analysis Five trials were analysed per condition. Dependent variables analyzed during the approach phase (end of corridor to the midpoint of VP crossing) were: (1) average forward speed of the trunk (walking) or centre of the MWC axel, (2) minimal clearance (distance between the wrist and the VP), (3) point of path deviation of the centre of mass of the trunk (walking) or MWC trajectory, (4) temporal coordination of angular deviations for the eye, head, trunk and MWC towards the new direction in relation to the SA condition and (5) relative timing between segments as the difference in temporal coordination between eye-head, head-trunk, and trunkWC. Video data were coded using software (PhysMo Video motion analysis) that allowed a frame-by-frame analysis of gaze behavior (location and duration at every frame for each trial; 30 Hz.). Gaze behavior (see Hollands et al., 2002) was categorized as: a) fixations on a location or object within the scene (≥3 frames) specifically: the vertical pole (VP); the target; and other environmental features (OEF) b) travel fixation which is defined as a gaze that stabilizes at a constant distance in front of the participant and moves with the subject (≥3 frames) or (c) other non-fixations (ONF), which include saccades as rapid eye movements causing a shift in gaze between two locations (≥1 frame), head initiated gaze shift where the eye and head turn together, blinks or undetermined data. The proportions of each gaze behavior as a percent of total behavior was then calculated and mean values reported.
C. Charette et al. / Neuroscience Letters 588 (2015) 83–87
Fig. 1. Example of straight ahead (thin lines) and direction change (thicker) trajectories during biped (dashed lines) and manual wheelchair (solid lines) conditions from random trials of one subject during walking for both conditions. Crosshair indicates approximate position of the vertical pole in the direction change conditions.
2.5. Statistical analysis Two-way (mode by condition) repeated measure ANOVAs were used to analyse speed and gaze behavior with paired t-tests for post-hoc analyses when significant interaction effects were found. Paired t-tests were also used for simple comparisons between modes for clearance, point of deviation and temporal coordination when changing direction.
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For gaze behavior (Fig. 3), participants focused mostly on the target while walking and propelling the MWC straight ahead. During the CD condition, subjects were less likely to focus on the target and shifted gaze between different elements in their environment for both modes of locomotion. For each gaze fixation type, subjects looked more at the vertical pole while changing direction while in the MWC than during biped gait (p = 0.037), were more focused on the target for straight ahead walking (main condition effect of p < 0.001) and were fixed more on other environmental features during CD (main condition effect of p = 0.008 and a condition by mode interaction of p = 0.04). For the travel fixation behavior, there was only a main effect for mode of locomotion (p = 0.004), where subjects engaged more travel fixation during MWC locomotion. There was no main effect reported for the other non-fixation behavior. For the walking SA and CD conditions, there were, respectively, 20.8% and 22% of undetermined and missing data. The same respective numbers for MWC were 15.1% and 12.9%.
4. Discussion 3. Results Example trajectories for each condition are presented in Fig. 1. There were no main mode effects for speed of locomotion during SA (gait: 1.43 ± 0.16 m/s, WC: 1.34 ± 0.21 m/s) or CD (gait: 1.42 ± 0.17 m/s, WC: 1.24 ± 0.22 m/s) conditions, but there was a main effect for condition (p < 0.001) and a condition by mode interaction (p = 0.004) with slower speeds for MWC for CD in comparison with the SA condition (p < 0.001). There was a greater clearance (p = 0.007) during CD in MWC (24.1 ± 9.3 cm) than during biped gait (14.8 ± 4.9 cm). The point of path deviation also tended to be timed closer to the VP while propelling the MWC (0.6 ± 0.2 s) than during gait (0.9 ± 0.1 s), although not statistically significant (p = 0.057). A counter-movement to the left prior to the direction change was observed in 7 out of 8 subjects for MWC only. As shown in Fig. 2a, body reorientation occurred before the VP indicating direction change, starting with a rotation of the head, which always preceded gaze changes, and was then followed by trunk movement for both modes of locomotion (trunk and MWC turned together). For 30% of trials, the rotation of the head started, and then slowed for a short period, but on all trials always continued towards the target. Yet while the relative timing between the onset of rotation of the eye and the head was similar for both modes of locomotion (p = 0.251), the relative timing between head and trunk was different (p = 0.005) (Fig. 2b).
The objective of this study was to begin to understand the visuo-locomotor coordination for MWC navigation in relation to biped gait when changing direction in healthy subjects. The results showed similar SA speeds for MWC and biped gait, allowing us to compare these two modes of locomotion. The slower speed observed in MWC during CD compared to the SA condition may reflect a safer behavior in a more complex environment for these novice MWC users. The counter-movement observed in 7 of the 8 subjects when changing direction during MWC may explain the greater clearances observed since this navigational behavior takes the subjects further from the VP. A study by Land and colleagues [11] clearly showed that before turning, cars also make a counter-movement in the opposite direction. Thus, this counter-movement while propelling the MWC may be related to the vehicular navigational control. However, it also remains to be seen if this behavior is maintained in experienced MWC users. Since the subjects were novice in MWC navigation, this behavior may have been a safer way to navigate, reducing the risk of a potential collision. It has been demonstrated that people tend to maintain a greater safety margin for locomotion in novel situations [15]. While it has been shown that able-bodied persons inexperienced with WC locomotion adapt over minutes and maintain learned skills over weeks [16], they are certainly not experts in MWC locomotion.
Fig. 2. (A) Averages and standard deviations for temporal coordination during direction change to the right while walking and in MWC. Zero crossing represents the time at which subjects crossed the vertical pole. (B) Averages and standard deviations of the relative timing between the eye and head and head and trunk for both modes of locomotion, and trunk and WC for MWC locomotion. Horizontal lines indicate a significant (p < 0.05) differences. Abbreviations: MWC: manual wheelchair.
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The head movement to anticipate path deviation and lead steering for locomotion appears to be stereotypic across locomotor modes. This result is supported by many other studies for biped gait [1,3–5] and it has been suggested that pre-aligning the head towards the new direction provides an allocentric reference frame that can be used for the control of the rest of the body [3]. While the trunk and MWC turned together as might be expected, the absolute timing for trunk yaw was the same for both modes despite their differences in path deviation behavior. This may suggest that there is a constant temporal body shift to the target regardless of locomotor mode for changes in lateral deviations. Interestingly, however, head rotation to the target appeared earlier than gaze shift for both modes of locomotion, which appears to contradict the literature for anticipatory gaze during walking [3–5]. Several factors may explain this result. Foremost, the environmental features of the CD condition may have influenced this behavior. Participants were instructed to use the intermediate vertical pole as a guide for changing direction. Although not an obstacle to the path per se, it still also needed to be avoided when changing direction. The saliency of the VP and its position will thus naturally attract visual attention. Moreover, both the static VP and the target were well known prior to each trial, which allows pre-planning. This differs from other steering studies that used visual cues [1,3,4,17–20] to indicate onset and direction of the turn. In fact, the use of a light cue may provide drive for visual redirection during walking [20]. Not initially knowing where to go also invokes a reactive strategy, that it is minimized in our protocol. Our task is also different from that of turning a 90-degree corner with a wall where the end path is not perceptible from the beginning, and therefore, an anticipatory strategy may be different. Perhaps the VP in our work is a “waypoint” for intermediate steering. A study by Wilkie et al. [21] demonstrated that subjects who performed slalom on a fixed bike switched their gaze from the current slalom gate to the next gate around 1–1.5 s before the first gate was reached. The authors proposed that the strategy used by the participants was to fixate the most proximal waypoint to establish an accurate steering course and then switch gaze towards the next waypoint in the series [21]. In our study, subjects looked at their most immediate environment, which was the VP, and then directed their gaze towards the next point of interest, the target. It may be that when the participants felt confident in clearing the VP, their gaze switched to the target. These specific differences between the onset times of eye rotation ahead of crossing the VP for walking (0.5 ± 0.3 s) and MWC (1.0 ± 0.3 s) may be due to the different navigational trajectories used for the two locomotor modes. The earlier anticipation by the eyes for the MWC mode may be initially to maintain visual contact (even if peripheral) simultaneously on the final target and VP. However, the relative timing between eye and head rotations is the same between these two modes, indicating that the same strategy is used, even though the absolute time of the onset of rotations was not. Similar behavior was also seen for other environmental demands, such as during stepping over an obstacle (within a few steps prior the obstacle) [6] and while driving (individuals looking 1–2 s ahead on the predicted curve before turning) [11,13]. Thus, the observed visuo-locomotor coordination here is most likely due to task predictability and environmental saliency (VP), and may be related to a “waypoint” strategy [21]. Even though there was great intra- and inter-subject variability for the gaze behavior, participants clearly aligned their gaze with environmental features of the steering path differently between conditions. There was a clear trend for subjects to fixate the vertical pole more during direction change in MWC as compared to biped walking. This might be likened to the intermediate collection of information of a tangent-like point [12]. However, statistical analysis demonstrated that only condition had a main effect on the fixation on the target and fixation on other environmental
Fig. 3. Averages and standard deviations for proportion (in percentage) of different visual behaviors for SA and CD conditions for both modes of locomotion. Horizontal lines indicate a significant (p < 0.05) differences from post-hoc analyses on interactions. Abbreviations: W: walking, MWC: manual wheelchair, SA: straight ahead, CD: changing direction, VP: vertical pole, OEF: other environmental features, ONF: other non-fixation.
features behavior. Subjects tended to look more at different elements in the environment and less on the target during CD for both locomotor modes. It is understandable that subjects need to gather more immediate information about path evolution during the direction change as compared to the simple SA task. However, subjects appear to rely slightly more on travel fixation for the SA condition while propelling a MWC. 5. Conclusions MWC navigation appears to combine both biped locomotor and vehicular-based movement control. The results suggest that head movement to anticipate path deviations and lead steering for locomotion is stereotypic across locomotor modes despite different path behavior. Specific gaze behavior depends predominantly on the environmental demands. These results generalize visuo-locomotor coordination strategies while also providing new knowledge on MWC locomotion specifically. Such information could eventually be useful to evaluating and training people in MWC. Further work is needed to compare the strategies used in novice MWC users with more experienced ones (e.g., following a spinal cord injury). Declaration of interest The authors report no conflict of interest. The authors alone are responsible for the content and writing of the paper. Acknowledgements We thank Guy St-Vincent and Olivier Doyle for their technical assistance. This study was supported in part by the Center for Interdisciplinary Research in Rehabilitation and Social Integration (CIRRIS), by the Natural Sciences and Engineering Research Council of Canada (McFadyen; bursaries to Charette) and from a Research Career Award of the Fonds de recherche du Québec - Santé (Routhier). References
C. Charette et al. / Neuroscience Letters 588 (2015) 83–87 [1] A.E. Patla, A. Adkin, T. Ballard, Online steering: coordination and control of body center of mass, head and body reorientation, Exp. Brain Res. 129 (1999) 629–634. [2] M. Shield, Use of wheelchairs and other mobility support devices, Health Rep. 15 (2004) 37–41. [3] M.A. Hollands, K.L. Sorensen, A.E. Patla, Effects of head immobilization on the coordination and control of head and body reorientation and translation during steering, Exp. Brain Res. 140 (2001) 223–233. [4] M.A. Hollands, A.E. Patla, J.N. Vickers, Look where you’re going!: gaze behavior associated with maintaining and changing the direction of locomotion, Exp. Brain Res. 143 (2002) 221–230. [5] T. Imai, S.T. Moore, T. Raphan, B. Cohen, Interaction of the body head and eyes during walking and turning, Exp. Brain Res. 136 (2001) 1–18. [6] A.E. Patla, S.D. Prentice, C. Robinson, J. Neufeld, Visual control of locomotion: strategies for changing direction and for going over obstacles, J. Exp. Psychol. Hum. Percept. Perform. 17 (1991) 603–634. [7] H. Hicheur, S. Vieilledent, M.J.E. Richardson, T. Flash, A. Berthoz, Velocity and curvature in human locomotion along complex curved paths: a comparison with hand movements, Exp. Brain Res. 162 (2005) 145–154. [8] T. Higuchi, Visuomotor control of human adaptative locomotion: understanding the anticipatory nature, Front. Psychol. 277 (2013) 1–9. [9] T. Higuchi, H. Takada, Y. Matsuura, K. Imanaka, Visual estimation of spatial requirements for locomotion in novice wheelchair users, J. Exp. Psychol. Appl. 10 (2004) 55–66. [10] T. Higuchi, M.E. Cinelli, A.E. Patla, Gaze behavior during locomotion trough apertures: the effect of locomotion forms, Hum. Mov. Sci. 28 (2009) 760–771. [11] M.F. Land, Eye movements and the control of actions in everyday life, Prog. Retin. Eye Res. 25 (2006) 296–324.
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[12] M.F. Land, D.N. Lee, Where we look when we steer, Nature 369 (1994) 742–744. [13] R.M. Wilkie, G.K. Kountouriotis, N. Merat, J.P. Wann, Using vision to control locomotion: looking where you want to go, Exp. Brain Res. 204 (2010) 539–547. [14] R.M. Wilkie, J.P. Wann, Eye-movements aid the control of locomotion, J. Vision 3 (2003) 677–684. [15] A.E. Patla, E. Niechwiej, V. Racco, M.A. Goodale, Understanding the contribution of binocular vision to the control of adaptive locomotion, Exp. Brain Res. 142 (2002) 551–561. [16] S. de Groot, H.E.J. Veeger, A.P. Hollander, L.H.V. van der Woude, Adaptations in physiology and propulsion techniques during the initial phase of learning manual wheelchair propulsion, Am. J. Phys. Med. Rehabil. 82 (2003) 504–510. [17] M. Cinelli, A.E. Patla, B. Stuart, Involvement of the head and trunk during gaze reorientation during standing and treadmill walking, Exp. Brain Res. 181 (2007) 183–191. [18] M. Cinelli, A.E. Patla, B. Stuart, Age-related differences during a gaze reorientation task while standing or walking on a treadmill, Exp. Brain Res. 185 (2008) 157–164. [19] M.K.Y. Mak, A.E. Patla, C. Hui-Chan, Sudden turn during walking is impaired in people with Parkinson’s disease, Exp. Brain Res. 190 (2008) 43–51. [20] V.N. Pradeep Ambati, N.G. Murray, F. Saucedo, D.W. Powell, R.J. Reed-Jones, Constraining eye movement when redirecting walking trajectories alters turning control in healthy young adults, Exp. Brain Res. 226 (2013) 549–556. [21] R.M. Wilkie, J.P. Wann, R.S. Allison, Active gaze, Visual look-ahead and locomotor control, J. Exp. Psychol. Hum. Percept. Perform. 34 (2008) 1150–1164.
Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Regular article
Visuo-locomotor coordination for direction changes in a manual wheelchair as compared to biped locomotion in healthy subjects Caroline Charette a,b , Franc¸ois Routhier a,b , Bradford J. McFadyen a,b,∗ a b
Centre for Interdisciplinary Research in Rehabilitation and Social Integration (CIRRIS), Quebec City Rehabilitation Institute, Quebec, Canada Faculty of Medicine, Department of Rehabilitation, Laval University, Quebec, Canada
h i g h l i g h t s • Anticipatory head movement found for both wheelchair and biped locomotor modes. • Specific gaze behavior depends predominantly on the environmental demands. • Manual wheelchair navigation combines both biped and vehicular-based control.
a r t i c l e
i n f o
Article history: Received 30 September 2014 Received in revised form 19 December 2014 Accepted 2 January 2015 Available online 3 January 2015 Keywords: Gait Eye movements Steering Gaze behavior Wheelchair
a b s t r a c t The visual system during walking provides travel path and environmental information. Although the manual wheelchair (MWC) is also a frequent mode of locomotion, its underlying visuo-locomotor control is not well understood. This study begins to understand the visuo-locomotor coordination for MWC navigation in relation to biped gait during direction changes in healthy subjects. Eight healthy male subjects (26.9 ± 6.4 years) were asked to walk as well as to propel a MWC straight ahead and while changing direction by 45◦ to the right guided by a vertical pole. Body and MWC movement (speed, minimal clearance, point of deviation, temporal body coordination, relative timing of body rotations) and gaze behavior were analysed. There was a main speed effect for direction and a direction by mode interaction with slower speeds for MWC direction change. Point of deviation was later for MWC direction change and always involved a counter movement (seen for vehicular control) with greater minimal distance from the vertical pole as compared to biped gait. In straight ahead locomotion, subjects predominantly fixed their gaze on the end target for both locomotor modes while there was a clear trend for subjects to fixate on the vertical pole more for MWC direction change. When changing direction, head movement always preceded gaze changes, which was followed by trunk movement for both modes. Yet while subjects turned the trunk at the same time during approach regardless of locomotor mode, head movement was earlier for MWC locomotion. These results suggest that MWC navigation combines both biped locomotor and vehicularbased movement control. Head movement to anticipate path deviations and lead steering for locomotion appears to be stereotypic across locomotor modes, while specific gaze behavior predominantly depends on the environmental demands. © 2015 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Steering or changing direction towards a new intended travel path while walking requires sensory-motor coordination to reorient the body while still maintaining balance [1]. The visual system is a crucial part of steering because it provides spatio-temporal information about the desired travel path and general move-
∗ Corresponding author at: CIRRIS, 525 Boul. Wilfrid-Hamel, G1M 2S8, Québec, Canada. Tel.: +1 418 529 9141x6584; fax: +1 418 529 3548. E-mail address: [email protected] (B.J. McFadyen). http://dx.doi.org/10.1016/j.neulet.2015.01.002 0304-3940/© 2015 Elsevier Ireland Ltd. All rights reserved.
ment within the environment. There are many other ways to locomote through the environment including wheeled mobility (e.g., bicycles, scooters, wheelchairs and motorized vehicles). Yet while biped locomotion has been studied for a variety of navigational tasks (e.g., stepping over or circumventing obstacles, changing direction), there is less research on the strategies used for other locomotor modes and very little for manual wheelchair (MWC) locomotion. The MWC is a mode of self-propelled wheeled locomotion that is used frequently [2] but its underlying visuolocomotor control which involves very different head movement as compared to biped or other seated locomotion is still not well understood. In this study, we will focus on navigating
84
C. Charette et al. / Neuroscience Letters 588 (2015) 83–87
to a new direction for comparing biped and MWC locomotor modes. For biped gait, steering involves a top-down sequence of body reorientation, starting with a rotation of the eyes and head towards the new travel path followed by the trunk and then the feet [1,3–5]. The anticipatory head movements are considered important to prepare and pre-programme adaptations within two steps prior to path deviations [6]. Specifically, it is suggested that these head movements provide an allocentric reference frame to re-orient the body [3] and steer towards the new direction of travel [7]. During adaptive locomotion, common characteristics of gaze behavior show that the majority of fixations are either directed towards a desired future path or an object of interest [4,8]. Moreover, prior to a direction change, individuals invariably make saccadic eye movements towards the end-point of the travel path, which allows the identification and extraction of information concerning the future path [4]. There are surprisingly few studies to understand the visuolocomotor coordination underlying MWC navigation, specifically during direction changes. However, Higuchi et al. [9] did compare biped and MWC locomotion, with respect to aperture perception in order to pass through doorways. They showed that able-bodied subjects underestimated their extended spatial requirements in a MWC, even after some practice, whereas they overestimated it when walking. The authors concluded that adaptation to altered body dimension is likely to occur very quickly under a familiar form of locomotion [9]. Higuchi et al. [10] also showed that while propelling a WC, able-bodied subjects tended to fixate more frequently on door edges, compared to walking. The authors suggested that the novelty of the locomotion mode caused participants to be more concerned about avoiding a collision with the door [10]. Although a MWC is not a car and does not have the constraints of a road environment in a high-speed context, it is a wheeled vehicle and may involve similar visually based navigational behavior. Land [11] likened the control of making right angle turns in a car to walking in that there is an anticipatory orienting head movement followed by the compensation for the head turning on the body within the car. It was also suggested that when turning a car along a curved road, drivers appear to focus on a tangent point on the inside of the curve of the road 1–2 s before turning [12]. Wilkie et al. [13], however, suggested the use of the tangent point was speed related and proposed a general strategy of «looking where you want to go» through gaze fixations onto points of the road at 1–2 s ahead. This is part of an active gaze theory proposed by Wilkie and Wann [14]. Finally, Land et al. [11] clearly showed that the car makes a countermovement in the opposite direction before turning along a curved road. MWC locomotion involves speeds that are more comparable to walking and thus allow us to compare the visuo-locomotor control between these two modes of locomotion. However, the MWC implies very different propulsion means with the involvement of upper body movement. Given that the MWC is also a common mode of locomotion for many people, it will be interesting to understand the relation to premorbid bipedal behavior for those now using a MWC. As a first important step, the goal of this study was to begin to understand the visuo-locomotor coordination for MWC navigation in relation to biped gait when changing direction in healthy subjects.
2. Material and methods 2.1. Participants Eight able-bodied adult male participants (mean age: 26.9 ± 6.4 years; height: 1.8 ± 0.1 m; mass: 76.5 ± 12.7 kg) were recruited.
Ethics approval was obtained from the Quebec City Rehabilitation Institute and all participants provided written informed consent. Subjects with any self-reported neurological or musculoskeletal problems or a score below 20/20 on the Snellen visual acuity test were excluded.
2.2. Data collection A motion analysis system (four Optotrak Certus motion sensors, NDI, 120 Hz) and seven triads of non-colinear infra-red markers (head, sternal notch, wrists, feet and on the MWC frame) were used to assess body and MWC movements. Gaze behavior data were collected using a commercial eye tracker (Mobile XG from Applied Sciences Laboratories, 30 Hz) that was synchronized with the Optotrak system.
2.3. Protocol Participants were trained for up to 20 min in the MWC (Quickie Q7 from Sunrise Medical) using some tasks of the Wheelchair Skills Training Program (www.wheelchairskillsprogram.ca). Subjects had to roll forwards (100 m), roll backwards (5 m), turn 90◦ (right and left) while moving forwards and backwards, turn in place (180◦ ) as well as ascend and descend a 5◦ and 10◦ incline. Then participants were asked to perform two experimental conditions, walking first and then propelling the MWC, both at comfortable self-selected speeds: (1) straight ahead along an 8.75 m path (SA condition) and (2) changing direction (CD condition) 45◦ to the right off the original straight ahead pathway at a specific point four metres from the start position as indicated by a black vertical pole (VP; 1.86 m height, 3.5 cm diameter). A round target was placed at the end of both paths and subjects were instructed to walk or propel the MWC to it. A corridor (0.92 m wide, 1.85 m long) was placed at the starting point to indicate an initial straight propulsion zone (see below). The vertical pole used for the CD condition was aligned with the right boarder of this corridor.
2.4. Data analysis Five trials were analysed per condition. Dependent variables analyzed during the approach phase (end of corridor to the midpoint of VP crossing) were: (1) average forward speed of the trunk (walking) or centre of the MWC axel, (2) minimal clearance (distance between the wrist and the VP), (3) point of path deviation of the centre of mass of the trunk (walking) or MWC trajectory, (4) temporal coordination of angular deviations for the eye, head, trunk and MWC towards the new direction in relation to the SA condition and (5) relative timing between segments as the difference in temporal coordination between eye-head, head-trunk, and trunkWC. Video data were coded using software (PhysMo Video motion analysis) that allowed a frame-by-frame analysis of gaze behavior (location and duration at every frame for each trial; 30 Hz.). Gaze behavior (see Hollands et al., 2002) was categorized as: a) fixations on a location or object within the scene (≥3 frames) specifically: the vertical pole (VP); the target; and other environmental features (OEF) b) travel fixation which is defined as a gaze that stabilizes at a constant distance in front of the participant and moves with the subject (≥3 frames) or (c) other non-fixations (ONF), which include saccades as rapid eye movements causing a shift in gaze between two locations (≥1 frame), head initiated gaze shift where the eye and head turn together, blinks or undetermined data. The proportions of each gaze behavior as a percent of total behavior was then calculated and mean values reported.
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Fig. 1. Example of straight ahead (thin lines) and direction change (thicker) trajectories during biped (dashed lines) and manual wheelchair (solid lines) conditions from random trials of one subject during walking for both conditions. Crosshair indicates approximate position of the vertical pole in the direction change conditions.
2.5. Statistical analysis Two-way (mode by condition) repeated measure ANOVAs were used to analyse speed and gaze behavior with paired t-tests for post-hoc analyses when significant interaction effects were found. Paired t-tests were also used for simple comparisons between modes for clearance, point of deviation and temporal coordination when changing direction.
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For gaze behavior (Fig. 3), participants focused mostly on the target while walking and propelling the MWC straight ahead. During the CD condition, subjects were less likely to focus on the target and shifted gaze between different elements in their environment for both modes of locomotion. For each gaze fixation type, subjects looked more at the vertical pole while changing direction while in the MWC than during biped gait (p = 0.037), were more focused on the target for straight ahead walking (main condition effect of p < 0.001) and were fixed more on other environmental features during CD (main condition effect of p = 0.008 and a condition by mode interaction of p = 0.04). For the travel fixation behavior, there was only a main effect for mode of locomotion (p = 0.004), where subjects engaged more travel fixation during MWC locomotion. There was no main effect reported for the other non-fixation behavior. For the walking SA and CD conditions, there were, respectively, 20.8% and 22% of undetermined and missing data. The same respective numbers for MWC were 15.1% and 12.9%.
4. Discussion 3. Results Example trajectories for each condition are presented in Fig. 1. There were no main mode effects for speed of locomotion during SA (gait: 1.43 ± 0.16 m/s, WC: 1.34 ± 0.21 m/s) or CD (gait: 1.42 ± 0.17 m/s, WC: 1.24 ± 0.22 m/s) conditions, but there was a main effect for condition (p < 0.001) and a condition by mode interaction (p = 0.004) with slower speeds for MWC for CD in comparison with the SA condition (p < 0.001). There was a greater clearance (p = 0.007) during CD in MWC (24.1 ± 9.3 cm) than during biped gait (14.8 ± 4.9 cm). The point of path deviation also tended to be timed closer to the VP while propelling the MWC (0.6 ± 0.2 s) than during gait (0.9 ± 0.1 s), although not statistically significant (p = 0.057). A counter-movement to the left prior to the direction change was observed in 7 out of 8 subjects for MWC only. As shown in Fig. 2a, body reorientation occurred before the VP indicating direction change, starting with a rotation of the head, which always preceded gaze changes, and was then followed by trunk movement for both modes of locomotion (trunk and MWC turned together). For 30% of trials, the rotation of the head started, and then slowed for a short period, but on all trials always continued towards the target. Yet while the relative timing between the onset of rotation of the eye and the head was similar for both modes of locomotion (p = 0.251), the relative timing between head and trunk was different (p = 0.005) (Fig. 2b).
The objective of this study was to begin to understand the visuo-locomotor coordination for MWC navigation in relation to biped gait when changing direction in healthy subjects. The results showed similar SA speeds for MWC and biped gait, allowing us to compare these two modes of locomotion. The slower speed observed in MWC during CD compared to the SA condition may reflect a safer behavior in a more complex environment for these novice MWC users. The counter-movement observed in 7 of the 8 subjects when changing direction during MWC may explain the greater clearances observed since this navigational behavior takes the subjects further from the VP. A study by Land and colleagues [11] clearly showed that before turning, cars also make a counter-movement in the opposite direction. Thus, this counter-movement while propelling the MWC may be related to the vehicular navigational control. However, it also remains to be seen if this behavior is maintained in experienced MWC users. Since the subjects were novice in MWC navigation, this behavior may have been a safer way to navigate, reducing the risk of a potential collision. It has been demonstrated that people tend to maintain a greater safety margin for locomotion in novel situations [15]. While it has been shown that able-bodied persons inexperienced with WC locomotion adapt over minutes and maintain learned skills over weeks [16], they are certainly not experts in MWC locomotion.
Fig. 2. (A) Averages and standard deviations for temporal coordination during direction change to the right while walking and in MWC. Zero crossing represents the time at which subjects crossed the vertical pole. (B) Averages and standard deviations of the relative timing between the eye and head and head and trunk for both modes of locomotion, and trunk and WC for MWC locomotion. Horizontal lines indicate a significant (p < 0.05) differences. Abbreviations: MWC: manual wheelchair.
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The head movement to anticipate path deviation and lead steering for locomotion appears to be stereotypic across locomotor modes. This result is supported by many other studies for biped gait [1,3–5] and it has been suggested that pre-aligning the head towards the new direction provides an allocentric reference frame that can be used for the control of the rest of the body [3]. While the trunk and MWC turned together as might be expected, the absolute timing for trunk yaw was the same for both modes despite their differences in path deviation behavior. This may suggest that there is a constant temporal body shift to the target regardless of locomotor mode for changes in lateral deviations. Interestingly, however, head rotation to the target appeared earlier than gaze shift for both modes of locomotion, which appears to contradict the literature for anticipatory gaze during walking [3–5]. Several factors may explain this result. Foremost, the environmental features of the CD condition may have influenced this behavior. Participants were instructed to use the intermediate vertical pole as a guide for changing direction. Although not an obstacle to the path per se, it still also needed to be avoided when changing direction. The saliency of the VP and its position will thus naturally attract visual attention. Moreover, both the static VP and the target were well known prior to each trial, which allows pre-planning. This differs from other steering studies that used visual cues [1,3,4,17–20] to indicate onset and direction of the turn. In fact, the use of a light cue may provide drive for visual redirection during walking [20]. Not initially knowing where to go also invokes a reactive strategy, that it is minimized in our protocol. Our task is also different from that of turning a 90-degree corner with a wall where the end path is not perceptible from the beginning, and therefore, an anticipatory strategy may be different. Perhaps the VP in our work is a “waypoint” for intermediate steering. A study by Wilkie et al. [21] demonstrated that subjects who performed slalom on a fixed bike switched their gaze from the current slalom gate to the next gate around 1–1.5 s before the first gate was reached. The authors proposed that the strategy used by the participants was to fixate the most proximal waypoint to establish an accurate steering course and then switch gaze towards the next waypoint in the series [21]. In our study, subjects looked at their most immediate environment, which was the VP, and then directed their gaze towards the next point of interest, the target. It may be that when the participants felt confident in clearing the VP, their gaze switched to the target. These specific differences between the onset times of eye rotation ahead of crossing the VP for walking (0.5 ± 0.3 s) and MWC (1.0 ± 0.3 s) may be due to the different navigational trajectories used for the two locomotor modes. The earlier anticipation by the eyes for the MWC mode may be initially to maintain visual contact (even if peripheral) simultaneously on the final target and VP. However, the relative timing between eye and head rotations is the same between these two modes, indicating that the same strategy is used, even though the absolute time of the onset of rotations was not. Similar behavior was also seen for other environmental demands, such as during stepping over an obstacle (within a few steps prior the obstacle) [6] and while driving (individuals looking 1–2 s ahead on the predicted curve before turning) [11,13]. Thus, the observed visuo-locomotor coordination here is most likely due to task predictability and environmental saliency (VP), and may be related to a “waypoint” strategy [21]. Even though there was great intra- and inter-subject variability for the gaze behavior, participants clearly aligned their gaze with environmental features of the steering path differently between conditions. There was a clear trend for subjects to fixate the vertical pole more during direction change in MWC as compared to biped walking. This might be likened to the intermediate collection of information of a tangent-like point [12]. However, statistical analysis demonstrated that only condition had a main effect on the fixation on the target and fixation on other environmental
Fig. 3. Averages and standard deviations for proportion (in percentage) of different visual behaviors for SA and CD conditions for both modes of locomotion. Horizontal lines indicate a significant (p < 0.05) differences from post-hoc analyses on interactions. Abbreviations: W: walking, MWC: manual wheelchair, SA: straight ahead, CD: changing direction, VP: vertical pole, OEF: other environmental features, ONF: other non-fixation.
features behavior. Subjects tended to look more at different elements in the environment and less on the target during CD for both locomotor modes. It is understandable that subjects need to gather more immediate information about path evolution during the direction change as compared to the simple SA task. However, subjects appear to rely slightly more on travel fixation for the SA condition while propelling a MWC. 5. Conclusions MWC navigation appears to combine both biped locomotor and vehicular-based movement control. The results suggest that head movement to anticipate path deviations and lead steering for locomotion is stereotypic across locomotor modes despite different path behavior. Specific gaze behavior depends predominantly on the environmental demands. These results generalize visuo-locomotor coordination strategies while also providing new knowledge on MWC locomotion specifically. Such information could eventually be useful to evaluating and training people in MWC. Further work is needed to compare the strategies used in novice MWC users with more experienced ones (e.g., following a spinal cord injury). Declaration of interest The authors report no conflict of interest. The authors alone are responsible for the content and writing of the paper. Acknowledgements We thank Guy St-Vincent and Olivier Doyle for their technical assistance. This study was supported in part by the Center for Interdisciplinary Research in Rehabilitation and Social Integration (CIRRIS), by the Natural Sciences and Engineering Research Council of Canada (McFadyen; bursaries to Charette) and from a Research Career Award of the Fonds de recherche du Québec - Santé (Routhier). References
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