Mark A. Hollands

“Look where you’re going!”: gaze behaviour associated with maintaining and changing the direction of locomotion

In order to fully understand how vision is used to guide locomotion it is necessary to know what people look at as they move through the environment. This study provides information, hitherto lacking, regarding gaze behaviour associated with both maintaining and changing the direction of locomotion: activities that are essential for efficient navigation through our cluttered environment. Participants’ spatiotemporal gaze patterns were recorded whilst they performed a task requiring that they either maintained a straight walking trajectory or changed their direction of walking by 30° or 60°, left or right, at the midpoint of a 9-m path. Participants were either visually cued to turn when they stepped on a trigger mat placed one step before the mid-point of the walkway (cued trials) or given verbal instruction about the required route prior to the start of each trial (advance knowledge trials). Our clear finding was that for the large majority of the time participants’ gaze was aligned with environmental features lying in their current plane of progression both prior to and following the onset of the transition stride during which the direction change was implemented. This gaze behaviour was observed both during cued trials (78% of total fixation time prior to the transition stride onset and 89% following the transition stride onset) and advance knowledge trials (67% prior to transition stride onset, 92% following transition stride onset). When not aligned with the plane of progression, gaze was normally fixated on environmental features related to either known or potential future routes. Prior to changing the direction of walking, individuals invariably made saccadic eye movements in order to align gaze with the end-point of the required travel path. This gaze realignment was invariably accompanied by head reorientation, which was initiated, on average, at the same time as the saccade. On average, participants fixated gaze on their goal (represented by the cue light at the travel path end-point) until after head realignment with the new path was achieved. Additionally, the head was consistently aligned with participants’ current walking direction prior to and following the transition stride even on the minority of occasions when they were looking elsewhere. These findings challenge the ecological validity of existing theories of how visual information is used to determine heading direction and are consistent with the proposal that aligning the head with the desired travel direction through coordinated eye and head movements provides the CNS with an allocentric frame of reference that is used to control the movement of the body in space.

Visually guided stepping under conditions of step cycle-related denial of visual information

We recently reported that subjects performing a task that requires visual guidance of each step onto irregularly placed “stepping stones” usually fixate the next target of footfall just before they lift the foot to be repositioned, i.e. towards the end of that limbs stance phase. When negotiating the same walkway without ambient lighting, and with each stones location indicated by a central light spot (LED), stepping and eye movements were unchanged. Under conditions of intermittent visual denial, in which all LEDs (the only visual cues) were temporarily extinguished at irregular intervals, temporal changes in the normal stepping pattern were sometimes observed, but stepping was not always affected. The primary effect of visual denial was on the leg that was in stance (foot in place on a stepping stone) at the moment of LED extinction, rather than on the leg that was in swing, and was an increase in stance duration, suggesting an effect on planning during this stance of the next swing towards the next target rather than on execution of the ongoing swing of the other leg. Subjects rarely failed to step onto the targets. Prolongations of stance under visual denial lasting 400 or 500 ms were less than 200 ms, much less than the duration of denial; subjects did not simply wait for the footfall target to reappear. There was no effect for denial lasting 300 ms; subjects performed as well as with a constantly visible target. Under 400 and 500 ms denial, there was no effect when the targets disappeared in the first 100 ms of stance (of the foot to be repositioned); stance durations were indistinguishable from control. This suggests that there is no crucial visuomotor processing by the control system(s) for eye and limb guidance until the target reappeared near the usual end of stance, when feedforward planning of the next saccade and/or swing to a target reaches a crucial stage, and is affected by intrusion of the period of visual denial. With longer (800 ms) denial there was an effect regardless of when in stance it began. A smaller effect of 800 ms denial sometimes visible in swing duration is attributable to interlimb coordination. Accurate saccades, followed by accurate steps, to the next target are almost always made, even when the target is invisible. Our results demonstrate that uninterrupted on-line visual information is not necessary for accurate stepping even when (as here) each step requires visual guidance. Also, since stance prolongations did not always result, and they were always much shorter than the periods of denial, we conclude that the visuomotor control mechanism(s) are robust in the face of substantial denial of all visual information including normally preferred inputs (foveal or peripheral images) at the normally preferred times. The fact that a saccade is still made to an invisible target location implies that this is useful in itself, since it does not result in a visible foveal image. We propose that skilled, visually guided stepping onto irregularly placed targets is executed under predominantly feedforward visuomotor control mechanisms, and suggest that the ability to function effectively in this way is dependent upon the integrity of the lateral cerebellum.

Effects of head immobilization on the coordination and control of head and body reorientation and translation during steering

Abstract. Changing the direction of locomotion involves lateral translation of the body in addition to body reorientation to align with the new travel direction. We designed this study to investigate the CNS control of these postural adjustments. The specific aims of the study were: first, to test the hypothesis that anticipatory head movements towards the new travel path are proactively controlled by the CNS to provide a stable frame of reference for body reorientation and, second, to investigate the relative contribution of foot placement and other mechanisms to the control of lateral body translation during steering. We achieved these aims by carrying out a comprehensive biomechanical analysis of participants performing a steering paradigm and observing the effects of immobilizing the head (by fixing it to the trunk) on postural control and the sequencing of body segment reorientation. Participants performed a task whereby they were visually cued to change their direction of walking by 30° or 60°, left or right, at the midpoint of a 9-m path. The temporal sequence of body reorientation was consistent with previous findings that the head starts to turn in the direction of travel before the rest of the body. Translation of the centre of mass (COM) in the new travel direction was achieved both through alternate placement of the contralateral foot prior to the turn step and use of a hip strategy to control the body pendulum during swing. Immobilizing the head resulted in the following significant changes: earlier onset of trunk yaw with respect to cue delivery, later trunk roll onset and a reduction in trunk roll amplitude. These results provide valuable information regarding the biomechanics of steering and support the hypothesis that aligning the head with motor or locomotor goals using vision provides the CNS with a stable frame of reference, independent of gaze, that can be used to control the repositioning of the body in space.

A new paradigm to investigate the roles of head and eye movements in the coordination of whole-body movements

Although previous studies have demonstrated the existence of coordinated eye and head movements during gaze shifts, none has studied the temporal and spatial characteristics of the various body segments during gaze transfers that require whole body movements. Without this information it is not possible to determine the extent of the interaction between the oculomotor control system and the motor control systems responsible for moving other body parts. Presented here is a detailed analysis of the timing and kinematic characteristics of participants’ (N=5) eye, head, upper body and feet during rotation of their body to align with light cues positioned at eccentric locations (45, 90, and 135°, left and right of centre). For all rotation amplitudes there was a clear sequence of body segment orientation (eye, head, upper body and feet) consistent with previous studies of locomotor steering and significant correlations between the onset latency times of the eyes and all body segments. There were also significant correlations between temporally aligned kinematic profiles of the feet and the eye in space for all movement amplitudes. The extent of correlation was significantly lower for displacement profiles of the feet versus head and of the feet versus upper body. These findings demonstrate substantial eye-foot coordination during a novel whole-body rotation paradigm and provide evidence that the output of the motor systems responsible for moving the feet is heavily influenced by the motor systems responsible for generating and coordinating eye and head movements to peripheral targets.

Evidence for interactive locomotor and oculomotor deficits in cerebellar patients during visually guided stepping

Abstract. Eight patients suffering from primary cerebellar degenerative diseases undertook a walkway task, demanding precise foot placement at each step, and a visual fixation task, requiring only eye movements. Step cycle and horizontal eye movements were recorded throughout the tasks and compared to those of healthy adults (including age- and sex-matched controls). Cerebellar patients displayed both locomotor and oculomotor deficits. Increases in duration of the stance, swing and double support phases of the step cycle were all shown to contribute to ataxic gait. Dysmetric saccades to fixate the footfall targets were seen more frequently in patients than in controls. These hypometric saccades were followed by one or more corrective saccades (patients: >45% accompanied by one or more corrective saccades; controls: <10% accompanied by a single corrective saccade). Similarities between the oculomotor deficits displayed by patients during the visual fixation task and when walking indicate that the latter are not merely a consequence of ataxic gait. The existence of several links between these locomotor and oculomotor deficits provides evidence for considerable interaction between the two control systems in the production of patterned eye and stepping movements. These results also suggest that the cerebellum plays an active role in the co-ordination of visually guided eye and limb movements during visually guided stepping.

Gaze Behavior of Young and Older Adults During Stair Walking

The authors quantitatively described gaze behavior of young (n = 10) and older (n = 10) adults during stair negotiation, which is information that is crucial for understanding the underlying visuomotor control of stair walking and the effects of aging on this control. Both age groups spent the majority of time looking at central aspects of the stairs approximately 3 steps ahead. Older adults showed less variability in the extent to which they looked ahead (p < .05), and all participants fixated the stairs for briefer periods during descent as opposed to ascent (p < .001). Older adults fixated stairs significantly longer than did young adults before stepping onto the stairs (p < .05). The authors conclude that adults need central visual information describing future stepping locations and that there are age-related differences in visual sampling that reflect changes in the visuomotor control processes subserving locomotion.

Interventions for coordination of walking following stroke: Systematic review

Impairments in gait coordination may be a factor in falls and mobility limitations after stroke. Therefore, rehabilitation targeting gait coordination may be an effective way to improve walking post-stroke. This review sought to examine current treatments that target impairments of gait coordination, the theoretical basis on which they are derived and the effects of such interventions. Few high quality RCTs with a low risk of bias specifically targeting and measuring restoration of coordinated gait were found. Consequently, we took a pragmatic approach to describing and quantifying the available evidence and included non-randomised study designs and limited the influence of heterogeneity in experimental design and control comparators by restricting meta-analyses to pre- and post-test comparisons of experimental interventions only. Results show that physiotherapy interventions significantly improved gait function and coordination. Interventions involving repetitive task-specific practice and/or auditory cueing appeared to be the most promising approaches to restore gait coordination. The fact that overall improvements in gait coordination coincided with increased walking speed lends support to the hypothesis that targeting gait coordination gait may be a way of improving overall walking ability post-stroke. However, establishing the mechanism for improved locomotor control requires a better understanding of the nature of both neuroplasticity and coordination deficits in functional tasks after stroke. Future research requires the measurement of impairment, activity and cortical activation in an effort to establish the mechanism by which functional gains are achieved.

Stepping characteristics and Centre of Mass control during stair descent: Effects of age, fall risk and visual factors

Stair edges provide important visual cues for appropriate foot placement on the stair and balance control during stair descent. Previous studies explored age-related changes in stepping performance and balance control during stair descent and included fit older adults. The present study investigates both age- and frailty-related changes to stepping parameters and Centre of Mass (COM) control during stair descent and how these measures are affected by visual factors. Older adults were split into two groups containing participants with the lowest (LROA, n=7) and highest (HROA, n=8) combined scores on tests of balance and confidence to negotiate stairs. Data were also collected from younger adult participants (YA, n=8). Kinematic data were collected from participants while they descended stairs under combinations of ambient light (bright and dimmed) and stair edge contrast conditions (high and low). A three (group) × two (illumination)×two (contrast) ANCOVA was performed with average stair walking speed as covariate. HROA cleared the stair edge vertically (p=0.001) and horizontally (p<0.001) with less distance than LROA. Dimmed ambient light resulted in decreased step length in HROA (p=0.006) compared to bright lighting. High stair edge contrast led to reduced vertical COM acceleration variability in HROA (p=0.009) and increased distance between COM and anterior base of support (p=0.017) in LROA. YA increased horizontal foot clearance (p=0.011) when stair edge contrast was high. We conclude that the aforementioned differences in stepping behaviour shown by HROA may contribute towards an increased risk of tripping and that high stair edge contrast has a beneficial effect on balance control in older adults.

Age-related differences in stepping performance during step cycle-related removal of vision

The aim of the present study was to investigate whether there are age-related changes in the ability of individuals to use vision to plan (feedforward control) and guide (on-line control) foot placement during locomotion. This aim was achieved by constraining the availability of vision and comparing the effects on the stepping performances of older and young adults during a precision stepping task. We experimentally controlled the availability of visual information such that: (1) vision was only available during each stance phase of the targeting limb, (2) vision was only available during each swing phase of the targeting limb or (3) vision was always available. Our visual manipulations had relatively little effect on younger adults’ stepping performance as demonstrated by their missing the target on less than 10% of occasions. However, there were clear visual condition-related differences in older adults’ stepping performance. When vision was only available during the stance phase of the targeting limb, older adults demonstrated significantly larger foot placement error and associated task failure rate (23%) than trials in which vision was always available (10%). There was an even greater increase in older adults’ foot placement error and task failure rate (42%) during trials in which vision was only available in the swing phase than the other visual conditions. These findings suggest that older adults need vision at particular times during the step cycle, to effectively pre-plan future stepping movements. We discuss the evidence that these age-related changes in performance reflect decline in visual and visuomotor CNS pathways.

Kinematics of turning 180 degrees during the timed up and go in stroke survivors with and without falls history

Background. Community-dwelling, chronic stroke survivors are at risk of falling during turning and are more likely to sustain a hip fracture when they fall. Objective. This study quantifies kinematic differences between stroke survivors (mean ± SD: 38.3 ± 31.3 months poststroke, 59.9 ± 10.1 years of age), with (n = 9) and without a falls history (n = 9), and age-matched healthy counterparts (n = 18) in turning coordination during the 180° turn around in the Timed “Up & Go„ (TUG) test. Methods. Full-body kinematics were recorded while participants performed the 180° turn around in the TUG. Dependent measures were time to turn, number of steps to turn, and measures of axial segment coordination. Result. Although participants who had a stroke and falls history took significantly longer to turn (mean ± SD: 4.4 ± 1.7 seconds) than age-matched controls (2.5 ± 0.6 seconds), no kinematic differences were found in performance or in the axial segment coordination during turning that could contribute to falls history or falls risk. Conclusions. These results indicate incidences of falls during turning following stroke may not be due to impaired movement patterns but due to the many other factors that are associated with falls, such as deficits in cognitive processes—attention or central integration—and/or sensory deficits.