- Email: [email protected]
Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions
Human Movement Science xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Human Movement Science journal homepage: www.elsevier.com/locate/humov
Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions q Alison C. Novak a, Nandini Deshpande b,⇑ a b
Toronto Rehabilitation Institute, Toronto, ON, Canada School of Rehabilitation Therapy, Queen’s University, Kingston, ON, Canada
a r t i c l e
i n f o
Article history: Available online xxxx PsycINFO classification: 2320 2330 2860 Keywords: Aging Obstacle crossing Kinematics Locomotion Sensorimotor
a b s t r a c t The ability to safely negotiate obstacles is an important component of independent mobility, requiring adaptive locomotor responses to maintain dynamic balance. This study examined the effects of aging and visual–vestibular interactions on whole-body and segmental control during obstacle crossing. Twelve young and 15 older adults walked along a straight pathway and stepped over one obstacle placed in their path. The task was completed under 4 conditions which included intact or blurred vision, and intact or perturbed vestibular information using galvanic vestibular stimulation (GVS). Global task performance significantly increased under suboptimal vision conditions. Vision also significantly influenced medial–lateral center of mass displacement, irrespective of age and GVS. Older adults demonstrated significantly greater trunk pitch and head roll angles under suboptimal vision conditions. Similar to whole-body control, no GVS effect was found for any measures of segmental control. The results indicate a significant reliance on visual but not vestibular information for locomotor control during obstacle crossing. The lack of differences in GVS effects suggests that vestibular information is not up-regulated for obstacle avoidance. This is not differentially affected by aging. In older adults, insufficient visual input appears to affect ability to minimize anterior–posterior trunk movement despite a slower obstacle crossing time and walking speed. Combined with larger
q The findings were partially presented at 1st Joint World Congress of ISPGR and Gait & Mental Function Conference, Norway in June 2012. ⇑ Corresponding author. Address: Louise D Acton Building, 31 George Street, Queen’s University, Kingston, ON K7L 3N6, Canada. Tel.: +1 613 533 2916; fax: +1 613 533 6776. E-mail address: [email protected] (N. Deshpande).
http://dx.doi.org/10.1016/j.humov.2014.03.009 0167-9457/Ó 2014 Elsevier B.V. All rights reserved.
Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
2
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
medial–lateral deviation of the body COM with insufficient visual information, the older adults may be at a greater risk for imbalance or inability to recover from a possible trip when stepping over an obstacle. Ó 2014 Elsevier B.V. All rights reserved.
1. Introduction The ability to safely negotiate obstacles is an important component of independent and safe mobility, requiring adaptive locomotor responses to maintain dynamic balance. It follows that planning, organization and generation of appropriate motor responses to facilitate dynamic equilibrium is required for successful task completion. Such control necessitates sensory information from the visual, somatosensory and vestibular systems. Failure in one or more of these systems or their integration can place unique constraints on the postural control system (Horak, 2006). Aging results in generalized decline in individual sensory functions and the ability of the central nervous system to integrate sensory information through reweighting the gain of the individual systems (Mozolic, Hugenschmidt, Peiffer, & Laurienti, 2012). Lord and Dayhew (2001) have identified reduced visual depth perception and contrast sensitivity as one of the strongest risk factors for multiple falls in community-dwelling older adults. The proactive or anticipatory control afforded by an intact visual system provides a plausible explanation why, as it allows for the type and extent of balance threats to be recognized early for appropriate modifications to the ongoing behavior (Frank & Patla, 2003; Mohagheghi, Moraes, & Patla, 2004). Physiological changes in the vestibular system (i.e., loss of vestibular nerve fibers, loss of vestibular hair cells) also occur with aging and may reduce the capacity to correctly detect head and trunk position and motion in space, limiting the ability to maintain a stable reference frame from which to generate postural responses (Pozzo, Levik, & Berthoz, 1995; Shumway-Cook & Woollacott, 2007). Deterioration in sensory function is proposed to reduce the ability to compensate for missing or conflicting sensory inputs for maintaining balance (Mozolic et al., 2012). Subsequently, older adults demonstrate decline in balance control during standing and require longer duration to complete mobility tasks when sensory input is manipulated (Deshpande, Novak, & Patla, 2006; Horak, Nashner, & Diener, 1990; Novak & Deshpande, 2011). During goal directed locomotion in an uncluttered environment, Deshpande and Patla (2007) have shown that compared to young adults, the ability of the older adult to down regulate sub-optimal vestibular input is affected despite availability of normal vision. The effects of aging on a possible reweighting of vestibular information for more challenging locomotor tasks, such as obstacle crossing, however, are not known. To achieve successful obstacle avoidance, the body’s center of mass (COM) has to be controlled within a narrow base of support defined by a single limb in contact with the ground, as the contralateral leg swings concurrently over the obstacle. To accommodate this challenge, older adults adopt a slower more conservative strategy compared to their younger counterparts, reflected by reductions in crossing velocity (Chen, Ashton-Miller, Alexander, & Schultz, 1991). Despite this, the maladaptive aspects of the conservative strategy, such as shortened landing distances, lack of adaptation in trunk range of motion (ROM) and COM displacement within a narrow base of support could potentially place older persons at risk for imbalance when stepping over an obstacle (Hahn & Chou, 2004; Lowrey, Watson, & Vallis, 2007). To date only one study has investigated visual–vestibular interaction on locomotor adaptations during obstacle crossing in healthy young adults (McFadyen, Bouyer, Bent, & Inglis, 2007). The authors reported a complex visual control but a lack of differences with deteriorated vestibular input, suggesting that vestibular information was not up-regulated for obstacle crossing when compared to level walking. In addition, study of the segmental control during obstacle crossing (i.e., individual control of the head and trunk segments) demonstrates significant deviations in frontal plane motion caused by deteriorated vestibular information, with little effect on sagittal plane Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
3
segmental motion (McFadyen et al., 2007). With advancing age, a decline in obstacle crossing performance may lead to increased risk of trips and falls. However, no study has considered the effect of aging on combined visual–vestibular interactions and movement control for obstacle avoidance. Such information would allow us to better understand the role of sensory information and effects on mobility and dynamic balance in individuals where decline in sensory information is typically superimposed on aging. The purpose of the present work was to examine the effects of deteriorated visual and vestibular inputs on whole body and segmental control during obstacle crossing in healthy young and older adults. We hypothesize that disruptions of vestibular information, particularly in the presence of deteriorated vision would be expected to result in greater instability and impaired movement control as older adults will exhibit increased weighting of vestibular information.
2. Methods 2.1. Participants Twelve young (mean age: 26.1 ± 3.7 years; 5 females) and 15 older adults (mean age: 73.1 ± 5.2 years; 8 females) participated in the study. All subjects were physically active, community dwelling volunteers, in self-reported good health. Individuals with a history of vision, vestibular system or neuromuscular disorders and/or symptomatic lower limb musculoskeletal conditions were excluded from the study. The protocol was approved by the university’s research ethics board and all subjects provided their informed consent. 2.2. Experimental procedure Experimental conditions were carried out while subjects walked along a straight pathway at their self-selected speed and stepped over one obstacle (height = 20 cm, width = 10 cm) placed at the center (at 3 m) in their path. Kinematic data were collected at 100 Hz using two Optotrak 3020 motion capture cameras (Northern Digital, Inc., Waterloo, Canada) placed at each end of the 6 m path. Ten infrared emitting diodes (IREDs) were attached to the subject’s body on the following anatomical landmarks: acromion processes (bilaterally), at the level of C6, T12, S2, lateral malleoli (bilaterally), above the ears and occiput. Following a ‘‘go’’ command subjects were instructed to walk to the end of the obstructed path. 2.2.1. Sensory manipulations Suboptimal visual conditions were created using custom-made blurring goggles. The goggles were sand-treated in a university optometry laboratory (University of Waterloo, Waterloo, ON) to create uniform and consistent blurring of vision simulating the consequences of dense cataracts (Deshpande & Patla, 2007). Vestibular information was manipulated by applying bipolar galvanic stimulation (GVS) (S48 Stimulator, Grass Technologies, Astro-Med Inc., Canada). Self-adhesive disposable electrodes were placed on each mastoid process, with the anode electrode randomly placed on either the right or left side. Individual GVS threshold was determined prior to the start of the experimental walking conditions by having the subject stand with their feet together and eyes closed. Visual identification of postural sway in response to increasing GVS intensity indicated threshold (Bent, McFadyen, & Inglis, 2002; Deshpande & Patla, 2007). For all subsequent testing, the GVS stimulation was twice the subject’s threshold intensity threshold. The onset of the GVS stimulus occurred 2 s prior to the initiation of walking (go command) to prevent initial sudden destabilization effect of GVS and lasted for a duration of 10 s to ensure constant stimulation for the entire walking trial. The subjects completed the task under two vision conditions: (1) Normal vision (V) or (2) Blurred vision (BV). Vestibular information was intact (no-GVS) or perturbed (GVS) on randomly selected trials for each vision condition. Obstacle crossing task was completed twice under each of the 4 sensory conditions (a total of 8 trials). Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
4
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
2.3. Data processing and analysis Walking speed, provided from forward trunk center of mass (COM) displacement during steady state gait, was determined for each experimental condition when walking across an unobstructed path (i.e., no obstacle was present). During the obstacle crossing task, walking speed was determined from foot contact of the lead limb before the obstacle to the foot contact of the trail limb after the obstacle (i.e., crossing strides) (Fig. 1). Temporal–spatial measures, including obstacle crossing time (time from initiation of lead limb swing to foot contact after obstacle), step width and step length (determined for the step before obstacle crossing (pre-obstacle step), step during obstacle crossing (obstacle step) and step after the obstacle (post-obstacle step) (Fig. 1) and measures of whole-body and segmental control were also determined for each experimental condition. Dependent variables included: vertical and medial–lateral whole-body center of mass (COM) displacement (cm) (determined using marker placed at S2 as a proxy measure of COM), roll and pitch angles of the head (degrees), and roll and pitch angles of the trunk (degrees); determined with respect to gravitational vertical. Roll angle refers to angular displacement in the frontal plane, while pitch angle refers to angular displacement in the sagittal plane. All variables of interest were measured through the swing phase of the lead limb crossing the obstacle, to gain insight into the period of the obstacle crossing task which places a high demand on the balance control system. Descriptive statistics (means and standard deviations) were calculated for all outcome measures (SPSS version 19.0, San Rafael, CA). A mixed factor analysis of variance [(2 (group) 2 (vision condition) 2 (GVS condition)] was conducted separately for each outcome measure. A significance level of p < .05 was adopted and post hoc analysis was performed if a significant interaction effect was detected. 3. Results 3.1. Temporal–spatial parameters All subjects completed the testing with no adverse effects. During unobstructed walking, the walking speed did not differ between BV and V conditions for both groups (p = .88). However, both YA and OA walked faster with GVS (p = .002). During the obstacle crossing task, walking speed determined for the crossing strides was significantly slower for the BV conditions (p < .001) and OA were significantly slower than YA (p < .001). A significant age vision interaction effect further showed that OA walk slower than YA (p = .017) under the BV condition. Similar to unobstructed walking, GVS resulted in faster walking speed during the crossing strides irrespective of vision or age (p = .006). Obstacle crossing time of the lead limb was significantly increased under the BV condition in both YA and
Pre-obstacle step
Obstacle step
Postobstacle step
FC-L
FC-L FC-T Foot Contact Lead limb
Foot Contact Trail limb
FC-T Foot Contact Lead limb
Foot Contact Trail limb
Fig. 1. During the obstacle crossing task, variables were analyzed from the foot contact of the lead limb (FC-L) prior to stepping over the obstacle to the foot contact of the trail limb (FC-T) after the obstacle crossing. Measures of step width, length, and step time were analyzed separately for the pre-obstacle step, obstacle step, and post-obstacle step.
Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
5
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
Fig. 2. Mean obstacle crossing time (seconds) of the lead limb in young adults (black) and older adults (gray) across vision conditions (V: full vision; BV: blurred vision) and GVS conditions (no-GVS, GVS). Error bars represent 1 SD from the mean. ⁄ Indicates a significant main effect of vision. Obstacle crossing time was significantly greater in BV compared to V conditions, irrespective of age and GVS conditions.
OA compared to V condition (p < .001). No main effect of age or GVS condition affected obstacle crossing time (p > .05) (Fig. 2). Similarly, the step time for the obstacle crossing step was significantly increased under the BV condition for both groups (p = .015) irrespective of GVS condition. The preobstacle step time and post-obstacle step time did not differ between groups, vision or GVS conditions (p > .144). Statistical analysis revealed no main effect of age, vision or GVS condition on step width for the pre-obstacle and obstacle crossing step (p > .067). However, a significant age vision interaction effect revealed that under the blurring condition, the older group adopt a larger step width for the post obstacle step (p = .006). In terms of step length, only the pre-obstacle step was significantly influenced by vision, where step length was reduced under BV compared to V (p = .006). The temporal–spatial parameters are summarized in Table 1.
Table 1 Temporal–spatial parameters (mean (SD)) during the obstacle crossing task. Variable of interest Walking speed (obstacle crossing task) (m/s) Pre-obstacle step
a, b, c, d
Step width (cm) Step length (cm)b Step time (seconds)
Obstacle step
Step width (cm) Step length (cm) Step time (seconds)b
Post-obstacle step
Step width (cm)b,
d
Step length (cm) Step time (seconds) a b c d
Indicates Indicates Indicates Indicates
significant significant significant significant
Group
V+no-GVS
BV+no-GVS
V+GVS
BV+GVS
YA OA
.92 (.09) .94 (.17)
.91 (.11) .84 (.18)
1.02 (.14) .94 (.18)
.94 (.13) .86 (.20)
YA OA YA OA YA OA
21.7 (2.7) 20.7 (4.0) 64.0 (13.4) 67.8 (10.6) .62 (.10) .67 (.12)
23.0 (2.7) 20.9 (3.5) 65.6 (14.4) 61.7 (11.1) .67 (.10) .68 (.15)
22.9 (4.9) 21.9 (4.1) 66.7 (13.6) 61.5 (13.6) .66 (.13) .63 (.09)
23.6 (3.4) 22.5 (5.9) 62.3 (9.4) 61.4 (9.0) .65 (.08) .68 (.14)
YA OA YA OA YA OA
20.6 (3.0) 21.0 (4.6) 65.2 (12.6) 72.6 (6.5) .74 (.11) .80 (.17)
20.4 (2.7) 21.8 (6.9) 66.2 (17.9) 73.0 (10.5) .79 (.14) .86 (.16)
20.2 (3.7) 21.4 (5.5) 71.1 (10.7) 73.5 (7.9) .73 (.06) .76 (.15)
21.1 (4.4) 23.6 (5.3) 71.4 (10.9) 73.3 (9.6) .77 (.12) .84 (.20)
YA OA YA OA YA OA
21.3 (1.9) 22.0 (4.3) 73.3 (10.4) 74.0 (10.8) .77 (.12) .75 (.13)
20.5 (3.9) 26.4 (4.2) 73.8 (18.2) 65.8 (18.7) .78 (.15) .74 (.08)
20.6 (3.6) 22.6 (7.2) 81.5 (15.1) 72.9 (18.2) .74 (.08) .75 (.07)
21.8 (4.2) 26.8 (5.0) 79.0 (18.6) 65.8 (21.3) .77 (.08) .75 (.10)
main effect of group. main effect of vision. main effect of GVS. interaction effect of vision in older group.
Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
6
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
3.2. Whole body and segmental control parameters In terms of whole body control, vision significantly influenced medial–lateral COM displacement, where BV condition showed greater peak M-L deviation compared to the V condition and greater vertical range compared to normal vision (p < .01), irrespective of age or GVS condition. No significant main effect of age, GVS condition or vision was found on peak vertical displacement of the COM when crossing the obstacle (p > .05) (Fig. 3). When considering segmental control, statistical analysis revealed no effect of age, vision or GVS condition on head pitch angle or trunk roll angle (p > .05). However, the OA group showed greater maximum trunk pitch and head roll angles compared to YA, under both visual and GVS conditions (p < .012) (Fig. 4). A significant age vision interaction effect revealed that under the blurring condition, the older group only also showed greater peak to peak trunk pitch angles compared to intact vision condition (Fig. 5).
4. Discussion The present study is the first to investigate age-related differences in the influence of deteriorated visual–vestibular information on locomotor control during an obstacle crossing task. The main findings demonstrate a significant reliance on visual but not vestibular information for locomotor control during obstacle crossing, and this is not differentially affected by aging. However, age-specific alterations in whole body and segmental control may place older adults at a greater risk of imbalance or inability to recover from a possible trip during obstacle crossing in the presence of sub-optimal visual information.
Fig. 3. Peak vertical COM displacement (cm) (a), range vertical COM displacement (cm) (b), peak M–L (medial–lateral) COM displacement (cm) (c), range M–L COM displacement (cm) (d) in young adults (black) and older adults (gray) across vision conditions (V: full vision; BV: blurred vision) and GVS conditions (no-GVS, GVS) when lead limb is crossing obstacle. Error bars represent 1 SD from the mean. ⁄Indicates a significant main effect of vision. Maximum M–L COM displacement was greater under BV compared to V conditions, irrespective of age and GVS conditions. Indicates significant main effect of age. Vertical COM range greater in older adults compared to young adults, irrespective of vision and GVS conditions.
Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
7
Fig. 4. Maximum head roll angle (degrees) (a), range headroll angle (degrees) (b) maximum head pitch angle (degrees) (c), range head pitch angle (degrees) (d) in young adults (black) and older adults (gray) across vision conditions (V: full vision; BV: blurred vision) and GVS conditions (no-GVS, GVS) when lead limb is crossing obstacle. Error bars represent 1 SD from the mean. ⁄ Indicates a significant main effect of group. Maximum head roll angle was greater in older adults compared to young adults, irrespective of vision and GVS conditions.
4.1. Increased reliance on visual input during obstacle crossing in older persons The important role of vision during obstacle crossing has been well-established (Mohagheghi et al., 2004; Patla & Vickers, 1997). Using custom made blurring goggles, we were able to effectively reduce contrast sensitivity to levels similar to that of dense cataracts (Patla & Deshpande, 2007). In terms of global performance, the time taken for both young and older adults to cross the obstacle increased and the walking speed was slower with sub-optimal visual information despite similar walking speed between conditions during unobstructed walking. This is not surprising, as previous research has demonstrated that control of the lead limb is influenced predominantly by vision (McFadyen et al., 2007; Mohagheghi et al., 2004). Similar to other study using cataract simulation, visual system is unable to provide accurate exteroceptive information regarding the environment such as obstacle height and boundaries, resulting in longer time to complete the action to ensure safe and appropriate avoidance of the obstacle (Heasley, Buckley, Scally, Twigg, & Elliott, 2004, 2005). However, this would effectively lengthen the time spent in single support phase (as reflected by the increased step time during the obstacle step). As a result, individuals would increase the amount of time spent having to control their COM within a narrow and moving base of support (Winter, 1990) with declines in visual information, placing them at greater risk for loss of balance. In terms of whole body control, sub-optimal visual input resulted in greater medial–lateral deviation of the COM. Again, this finding was not differentially affected by aging. When completing a single step-up from a static position, older adults have utilized a strategy which would effectively minimize risk for medial–lateral instability (Heasley et al., 2005) with deteriorated visual information. However, our present results indicate a similar strategy does not transfer to ongoing, dynamic locomotion, as is the case with our obstacle crossing task. In the presence of sub-optimal visual input, obstacle crossing appears to challenge whole body balance control in the frontal plane to a greater degree in both young Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
8
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
Fig. 5. Maximum trunk roll angle (degrees) (a), range trunk roll angle (degrees) (b) maximum trunk pitch angle (degrees) (c), range trunk pitch angle (degrees) (d) in young adults (black) and older adults (gray) across vision conditions (V: full vision; BV: blurred vision) and GVS conditions (no-GVS, GVS) when lead limb is crossing obstacle. Error bars represent 1 SD from the mean. ⁄ Indicates a significant main effect of group. Maximum trunk pitch angle was greater in older adults compared to young adults, irrespective of vision and GVS conditions. Indicates significant interaction effect. Greater peak to peak trunk pitch angle in older group only for BV condition compared to V condition.
and older adults, as indicated by the increase in peak frontal plane displacement and vertical range of the body COM, with no change in step width. In the case of older adults, greater displacement paired with reduced strength (John, Liu, & Gregory, 2009) may hinder the ability to respond sufficiently in the event of a destabilization and increases risk of falls. Visual information is critical not only to maintain whole body equilibrium, but also to regulate segment orientation during obstacle crossing (Bent et al., 2002). We have shown age-related differences in trunk pitch and head roll angles during obstacle crossing, with further increases in trunk pitch displacement in the presence of blurred vision. The older adults are able to successfully navigate over the obstacle with demonstrated increases in anterior–posterior trunk motion. Of note, the older group do not present with a more stooped posture than the younger group when measured statically. Previous research has shown that coupling of the head and trunk segments optimizes visual and vestibular contributions to postural control and is a generalized strategy adopted by older adults during locomotion (Deshpande & Patla, 2007). In this vein, the general age-related increase in trunk flexion during dynamic movement coincides with head flexion and likely occurs to acquire environmental information (i.e., ground scanning) while reducing the complexity of postural control. Although we did not measure distance of lead foot contact from obstacle, literature consistently shows that older adults place their lead limb closer to the obstacle when compared to young adults (Chen et al., 1991; Lowrey et al., 2007), which effectively shorten the base of support in the anterior–posterior direction. If this was the case in our group of older adults, they would be required to control larger motions of their trunk within reduced base of support (Lowrey et al., 2007), posing a greater threat to an older person’s dynamic stability. In the absence of optimal vision, the risk of balance instability is further emphasized. That medial–lateral trunk control was not significantly influenced by aging or vision could suggest the obstacle crossing task was not challenging enough to induce frontal plane instability under impoverished sensory conditions. Conversely, by slowing down obstacle crossing time, the older adults may
Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
9
maintain medial–lateral upper body control to similar levels of the young group even in the presence of sub-optimal sensory information.
4.2. Discordant vestibular information does not impact whole body and segmental control during obstacle crossing in older adults McFadyen et al. (2007) have investigated the role of vestibular system information during obstacle crossing in young adults when normal vision was either available or was occluded completely. The authors reported that vestibular information was not up-regulated for obstacle avoidance in healthy young adults given the lack of differences between level ground walking and obstacle crossing. Our present work took this further, and examined the effects of aging and the visual–vestibular influences on the obstacle crossing task when visual information was suboptimal but not completely absent. We found that vestibular information is not up-regulated for obstacle avoidance; this was not differentially affected by aging. This is in contrast to our hypothesis, where we expected GVS induced instability to increase further under sub-optimal visual conditions. Under similar vision manipulations, Deshpande and Patla (2007) have reported reduced path deviation while walking as the distance from the target (locate at 6.5 m from the starting point) reduced, suggesting that the dependence on the vision increases as the target distance decreases. Standing posture studies have also demonstrated differences in the integration of visual information for postural control depending of the target distance (Bonnet, Temprado, & Berton, 2010). In the obstacle crossing condition the target is at a closer distance and possibly within the distance range where the vision can be the dominant sensory information. Further, exteroceptive cues provided by the central visual field regarding the height, width and location of the obstacle in the path could be used in a feed-forward manner to plan the gait parameter adaptations required for safely negotiating the challenges (Patla & Vickers, 1997) thus minimizing dependence on the vestibular system. GVS also induces binaural stimulation resulting in a predominantly lateral perturbation whereas obstacle crossing while walking along a straight path is a largely anterior–posterior movement. McFadyen et al. (2007) showed that despite significant lateral deviations in the trunk displacement and foot trajectory associated with GVS, during obstacle crossing sagittal plane control of foot trajectory and body displacement was unaffected in young adults even when vision was completely occluded. Our lack of differences in medial–lateral head and trunk displacements in response to GVS may suggest an overall down regulation of the vestibular system gain during obstacle crossing when some visual information is available. It should be kept in mind that both older and young adults walked faster with sub-optimal vestibular information during both unobstructed walking and during the obstacle crossing task. It is plausible that when gait speed is controlled between conditions, the findings would differ. It should also be noted that the task was completed on a firm surface, providing accurate lower limb proprioceptive feedback. Future study should consider the role both gait speed and of proprioception on reweighting of the other sensory systems to navigate through obstacles.
5. Conclusion The investigation of balance control mechanisms during walking in various, challenging environments is necessary to understand how older adults perform tasks of daily living and the role of sensory information in those tasks. This is the first study to investigate the effects of aging and the visual–vestibular influences on whole body and segmental control during obstacle crossing. Even in the presence of sub-optimal visual information, the vestibular input was not up-regulated for obstacle crossing and this was not differentially affected by aging. The results indicate an increased reliance on visual information for task completion. In older adults, mal-adaptations in anterior trunk movement and larger medial–lateral displacement of the body COM with insufficient visual information may place them at a greater risk of imbalance when stepping over an obstacle. Future work should consider the role of lower limb proprioception on sensory reweighting in older adults during obstacle avoidance. Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
10
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
Role of sponsor None. Conflict of interest The authors declare that they have no conflict of interest. Acknowledgements The authors would like to thank Patricia Hewston, Mika Yoshikawa and Fang Zhang for assistance with data collection. This project was funded by the Senate Advisory and Research Committee (SARC), Queen’s University to Dr. Deshpande. References Bent, L. R., McFadyen, B. J., & Inglis, J. T. (2002). Visual–vestibular interactions in postural control during the execution of a dynamic task. Experimental Brain Research, 14, 490–500. Bonnet, C. T., Temprado, J. J., & Berton, E. (2010). The effects of the proximity of an object on human stance. Gait & Posture, 32, 124–128. Chen, H. C., Ashton-Miller, J. A., Alexander, N. B., & Schultz, A. B. (1991). Stepping over obstacles: Gait patterns of healthy adults. Journal of Gerontology, 46, M196–M203. Deshpande, N., Novak, A., & Patla, A. E. (2006). Determining functional mobility using the modified timed up and go test: Effects of sensory manipulations. Journal of the American Geriatrics Society, 54, 1157–1158. Deshpande, N., & Patla, A. E. (2007). Visual–vestibular interaction during goal directed locomotion: Effects of aging and blurring vision. Experimental Brain Research, 176, 43–53. Frank, J. S., & Patla, A. E. (2003). Balance and mobility challenges in older adults: Implications for preserving community mobility. American Journal of Preventative Medicine, 25, 157–163. Hahn, M. E., & Chou, L. S. (2004). Age-related reduction in sagittal plane center of mass motion during obstacle crossing. Journal of Biomechanics, 37, 837–844. Heasley, K., Buckley, J. G., Scally, A., Twigg, P., & Elliott, D. B. (2004). Stepping up to a new level: Effects of blurring vision in the elderly. Investigations in Opthalmology and Vision Science, 45, 2122–2128. Heasley, K., Buckley, J. G., Scally, A., Twigg, P., & Elliott, D. B. (2005). Falls in older people: Effects of age and blurring vision on the dynamics of stepping. Investigations in Opthalmology and Vision Science, 46, 3584–3588. Horak, F. B. (2006). Postural orientation and equilibrium: What do we need to know about neural control of balance to prevent falls? Age & Ageing, 35, ii7–ii11. Horak, F. B., Nashner, L. M., & Diener, H. C. (1990). Postural strategies associated with somatosensory and vestibular loss. Experimental Brain Research, 82, 167–177. John, E. B., Liu, W., & Gregory, R. W. (2009). Biomechanics of muscular effort: Age-related changes. Medicine in Science & Sports Exercise, 41, 418–425. Lord, S. R., & Dayhew, J. (2001). Visual risk factors for falls in older people. Journal of the American Geriatric Society, 49, 508–515. Lowrey, C. R., Watson, A., & Vallis, L. A. (2007). Age-related changes in avoidance strategies when negotiating single and multiple obstacles. Experimental Brain Research, 182, 289–299. McFadyen, B. J., Bouyer, L., Bent, L. R., & Inglis, J. T. (2007). Visual–vestibular influences on locomotor adjustments for stepping over an obstacle. Experimental Brain Research, 179, 235–243. Mohagheghi, A. A., Moraes, R., & Patla, A. E. (2004). The effects of distant and on-line visual information on the control of approach phase and step over an obstacle during locomotion. Experimental Brain Research, 155, 459–468. Mozolic, J. L., Hugenschmidt, C. E., Peiffer, A. M., & Laurienti, P. J. (2012). Multisensory Integration and Aging. In M. M. Murray & M. T. Wallace (Eds.), The Neural Bases of Multisensory Processes. Boca Raton, FL: CRC Press. Novak, A. C., & Deshpande, N. (2011). Comparing effects of deteriorated sensory information on sit-to-stand performance of young and older adults – A pilot study. Journal of the American Geriatric Society, 59, 562–563. Patla, A. E., & Vickers, J. N. (1997). Where and when do we look as we approach and step over an obstacle in the travel path? Neuroreport, 8, 3661–3665. Patla, A. E., & Deshpande, N. (2007). Visual-vestibular interaction during goal directed locomotion: effects of aging and blurring vision. Experimental Brain Research., 176, 43–53. Pozzo, T., Levik, Y., & Berthoz, A. (1995). Head and trunk movements in the frontal plane during complex dynamic equilibrium tasks in humans. Experimental Brain Research, 106, 327–338. Shumway-Cook, A., & Woollacott, M. H. (2007). Motor Control: Translating research into clinical practice (3rd ed.). Philadelphia: Lippincott Williams and Wilkins. Winter, D. A. (1990). Biomechanics and motor control of human movement (2nd ed.). New York: Wiley Inter-Science.
Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
Contents lists available at ScienceDirect
Human Movement Science journal homepage: www.elsevier.com/locate/humov
Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions q Alison C. Novak a, Nandini Deshpande b,⇑ a b
Toronto Rehabilitation Institute, Toronto, ON, Canada School of Rehabilitation Therapy, Queen’s University, Kingston, ON, Canada
a r t i c l e
i n f o
Article history: Available online xxxx PsycINFO classification: 2320 2330 2860 Keywords: Aging Obstacle crossing Kinematics Locomotion Sensorimotor
a b s t r a c t The ability to safely negotiate obstacles is an important component of independent mobility, requiring adaptive locomotor responses to maintain dynamic balance. This study examined the effects of aging and visual–vestibular interactions on whole-body and segmental control during obstacle crossing. Twelve young and 15 older adults walked along a straight pathway and stepped over one obstacle placed in their path. The task was completed under 4 conditions which included intact or blurred vision, and intact or perturbed vestibular information using galvanic vestibular stimulation (GVS). Global task performance significantly increased under suboptimal vision conditions. Vision also significantly influenced medial–lateral center of mass displacement, irrespective of age and GVS. Older adults demonstrated significantly greater trunk pitch and head roll angles under suboptimal vision conditions. Similar to whole-body control, no GVS effect was found for any measures of segmental control. The results indicate a significant reliance on visual but not vestibular information for locomotor control during obstacle crossing. The lack of differences in GVS effects suggests that vestibular information is not up-regulated for obstacle avoidance. This is not differentially affected by aging. In older adults, insufficient visual input appears to affect ability to minimize anterior–posterior trunk movement despite a slower obstacle crossing time and walking speed. Combined with larger
q The findings were partially presented at 1st Joint World Congress of ISPGR and Gait & Mental Function Conference, Norway in June 2012. ⇑ Corresponding author. Address: Louise D Acton Building, 31 George Street, Queen’s University, Kingston, ON K7L 3N6, Canada. Tel.: +1 613 533 2916; fax: +1 613 533 6776. E-mail address: [email protected] (N. Deshpande).
http://dx.doi.org/10.1016/j.humov.2014.03.009 0167-9457/Ó 2014 Elsevier B.V. All rights reserved.
Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
2
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
medial–lateral deviation of the body COM with insufficient visual information, the older adults may be at a greater risk for imbalance or inability to recover from a possible trip when stepping over an obstacle. Ó 2014 Elsevier B.V. All rights reserved.
1. Introduction The ability to safely negotiate obstacles is an important component of independent and safe mobility, requiring adaptive locomotor responses to maintain dynamic balance. It follows that planning, organization and generation of appropriate motor responses to facilitate dynamic equilibrium is required for successful task completion. Such control necessitates sensory information from the visual, somatosensory and vestibular systems. Failure in one or more of these systems or their integration can place unique constraints on the postural control system (Horak, 2006). Aging results in generalized decline in individual sensory functions and the ability of the central nervous system to integrate sensory information through reweighting the gain of the individual systems (Mozolic, Hugenschmidt, Peiffer, & Laurienti, 2012). Lord and Dayhew (2001) have identified reduced visual depth perception and contrast sensitivity as one of the strongest risk factors for multiple falls in community-dwelling older adults. The proactive or anticipatory control afforded by an intact visual system provides a plausible explanation why, as it allows for the type and extent of balance threats to be recognized early for appropriate modifications to the ongoing behavior (Frank & Patla, 2003; Mohagheghi, Moraes, & Patla, 2004). Physiological changes in the vestibular system (i.e., loss of vestibular nerve fibers, loss of vestibular hair cells) also occur with aging and may reduce the capacity to correctly detect head and trunk position and motion in space, limiting the ability to maintain a stable reference frame from which to generate postural responses (Pozzo, Levik, & Berthoz, 1995; Shumway-Cook & Woollacott, 2007). Deterioration in sensory function is proposed to reduce the ability to compensate for missing or conflicting sensory inputs for maintaining balance (Mozolic et al., 2012). Subsequently, older adults demonstrate decline in balance control during standing and require longer duration to complete mobility tasks when sensory input is manipulated (Deshpande, Novak, & Patla, 2006; Horak, Nashner, & Diener, 1990; Novak & Deshpande, 2011). During goal directed locomotion in an uncluttered environment, Deshpande and Patla (2007) have shown that compared to young adults, the ability of the older adult to down regulate sub-optimal vestibular input is affected despite availability of normal vision. The effects of aging on a possible reweighting of vestibular information for more challenging locomotor tasks, such as obstacle crossing, however, are not known. To achieve successful obstacle avoidance, the body’s center of mass (COM) has to be controlled within a narrow base of support defined by a single limb in contact with the ground, as the contralateral leg swings concurrently over the obstacle. To accommodate this challenge, older adults adopt a slower more conservative strategy compared to their younger counterparts, reflected by reductions in crossing velocity (Chen, Ashton-Miller, Alexander, & Schultz, 1991). Despite this, the maladaptive aspects of the conservative strategy, such as shortened landing distances, lack of adaptation in trunk range of motion (ROM) and COM displacement within a narrow base of support could potentially place older persons at risk for imbalance when stepping over an obstacle (Hahn & Chou, 2004; Lowrey, Watson, & Vallis, 2007). To date only one study has investigated visual–vestibular interaction on locomotor adaptations during obstacle crossing in healthy young adults (McFadyen, Bouyer, Bent, & Inglis, 2007). The authors reported a complex visual control but a lack of differences with deteriorated vestibular input, suggesting that vestibular information was not up-regulated for obstacle crossing when compared to level walking. In addition, study of the segmental control during obstacle crossing (i.e., individual control of the head and trunk segments) demonstrates significant deviations in frontal plane motion caused by deteriorated vestibular information, with little effect on sagittal plane Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
3
segmental motion (McFadyen et al., 2007). With advancing age, a decline in obstacle crossing performance may lead to increased risk of trips and falls. However, no study has considered the effect of aging on combined visual–vestibular interactions and movement control for obstacle avoidance. Such information would allow us to better understand the role of sensory information and effects on mobility and dynamic balance in individuals where decline in sensory information is typically superimposed on aging. The purpose of the present work was to examine the effects of deteriorated visual and vestibular inputs on whole body and segmental control during obstacle crossing in healthy young and older adults. We hypothesize that disruptions of vestibular information, particularly in the presence of deteriorated vision would be expected to result in greater instability and impaired movement control as older adults will exhibit increased weighting of vestibular information.
2. Methods 2.1. Participants Twelve young (mean age: 26.1 ± 3.7 years; 5 females) and 15 older adults (mean age: 73.1 ± 5.2 years; 8 females) participated in the study. All subjects were physically active, community dwelling volunteers, in self-reported good health. Individuals with a history of vision, vestibular system or neuromuscular disorders and/or symptomatic lower limb musculoskeletal conditions were excluded from the study. The protocol was approved by the university’s research ethics board and all subjects provided their informed consent. 2.2. Experimental procedure Experimental conditions were carried out while subjects walked along a straight pathway at their self-selected speed and stepped over one obstacle (height = 20 cm, width = 10 cm) placed at the center (at 3 m) in their path. Kinematic data were collected at 100 Hz using two Optotrak 3020 motion capture cameras (Northern Digital, Inc., Waterloo, Canada) placed at each end of the 6 m path. Ten infrared emitting diodes (IREDs) were attached to the subject’s body on the following anatomical landmarks: acromion processes (bilaterally), at the level of C6, T12, S2, lateral malleoli (bilaterally), above the ears and occiput. Following a ‘‘go’’ command subjects were instructed to walk to the end of the obstructed path. 2.2.1. Sensory manipulations Suboptimal visual conditions were created using custom-made blurring goggles. The goggles were sand-treated in a university optometry laboratory (University of Waterloo, Waterloo, ON) to create uniform and consistent blurring of vision simulating the consequences of dense cataracts (Deshpande & Patla, 2007). Vestibular information was manipulated by applying bipolar galvanic stimulation (GVS) (S48 Stimulator, Grass Technologies, Astro-Med Inc., Canada). Self-adhesive disposable electrodes were placed on each mastoid process, with the anode electrode randomly placed on either the right or left side. Individual GVS threshold was determined prior to the start of the experimental walking conditions by having the subject stand with their feet together and eyes closed. Visual identification of postural sway in response to increasing GVS intensity indicated threshold (Bent, McFadyen, & Inglis, 2002; Deshpande & Patla, 2007). For all subsequent testing, the GVS stimulation was twice the subject’s threshold intensity threshold. The onset of the GVS stimulus occurred 2 s prior to the initiation of walking (go command) to prevent initial sudden destabilization effect of GVS and lasted for a duration of 10 s to ensure constant stimulation for the entire walking trial. The subjects completed the task under two vision conditions: (1) Normal vision (V) or (2) Blurred vision (BV). Vestibular information was intact (no-GVS) or perturbed (GVS) on randomly selected trials for each vision condition. Obstacle crossing task was completed twice under each of the 4 sensory conditions (a total of 8 trials). Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
4
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
2.3. Data processing and analysis Walking speed, provided from forward trunk center of mass (COM) displacement during steady state gait, was determined for each experimental condition when walking across an unobstructed path (i.e., no obstacle was present). During the obstacle crossing task, walking speed was determined from foot contact of the lead limb before the obstacle to the foot contact of the trail limb after the obstacle (i.e., crossing strides) (Fig. 1). Temporal–spatial measures, including obstacle crossing time (time from initiation of lead limb swing to foot contact after obstacle), step width and step length (determined for the step before obstacle crossing (pre-obstacle step), step during obstacle crossing (obstacle step) and step after the obstacle (post-obstacle step) (Fig. 1) and measures of whole-body and segmental control were also determined for each experimental condition. Dependent variables included: vertical and medial–lateral whole-body center of mass (COM) displacement (cm) (determined using marker placed at S2 as a proxy measure of COM), roll and pitch angles of the head (degrees), and roll and pitch angles of the trunk (degrees); determined with respect to gravitational vertical. Roll angle refers to angular displacement in the frontal plane, while pitch angle refers to angular displacement in the sagittal plane. All variables of interest were measured through the swing phase of the lead limb crossing the obstacle, to gain insight into the period of the obstacle crossing task which places a high demand on the balance control system. Descriptive statistics (means and standard deviations) were calculated for all outcome measures (SPSS version 19.0, San Rafael, CA). A mixed factor analysis of variance [(2 (group) 2 (vision condition) 2 (GVS condition)] was conducted separately for each outcome measure. A significance level of p < .05 was adopted and post hoc analysis was performed if a significant interaction effect was detected. 3. Results 3.1. Temporal–spatial parameters All subjects completed the testing with no adverse effects. During unobstructed walking, the walking speed did not differ between BV and V conditions for both groups (p = .88). However, both YA and OA walked faster with GVS (p = .002). During the obstacle crossing task, walking speed determined for the crossing strides was significantly slower for the BV conditions (p < .001) and OA were significantly slower than YA (p < .001). A significant age vision interaction effect further showed that OA walk slower than YA (p = .017) under the BV condition. Similar to unobstructed walking, GVS resulted in faster walking speed during the crossing strides irrespective of vision or age (p = .006). Obstacle crossing time of the lead limb was significantly increased under the BV condition in both YA and
Pre-obstacle step
Obstacle step
Postobstacle step
FC-L
FC-L FC-T Foot Contact Lead limb
Foot Contact Trail limb
FC-T Foot Contact Lead limb
Foot Contact Trail limb
Fig. 1. During the obstacle crossing task, variables were analyzed from the foot contact of the lead limb (FC-L) prior to stepping over the obstacle to the foot contact of the trail limb (FC-T) after the obstacle crossing. Measures of step width, length, and step time were analyzed separately for the pre-obstacle step, obstacle step, and post-obstacle step.
Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
5
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
Fig. 2. Mean obstacle crossing time (seconds) of the lead limb in young adults (black) and older adults (gray) across vision conditions (V: full vision; BV: blurred vision) and GVS conditions (no-GVS, GVS). Error bars represent 1 SD from the mean. ⁄ Indicates a significant main effect of vision. Obstacle crossing time was significantly greater in BV compared to V conditions, irrespective of age and GVS conditions.
OA compared to V condition (p < .001). No main effect of age or GVS condition affected obstacle crossing time (p > .05) (Fig. 2). Similarly, the step time for the obstacle crossing step was significantly increased under the BV condition for both groups (p = .015) irrespective of GVS condition. The preobstacle step time and post-obstacle step time did not differ between groups, vision or GVS conditions (p > .144). Statistical analysis revealed no main effect of age, vision or GVS condition on step width for the pre-obstacle and obstacle crossing step (p > .067). However, a significant age vision interaction effect revealed that under the blurring condition, the older group adopt a larger step width for the post obstacle step (p = .006). In terms of step length, only the pre-obstacle step was significantly influenced by vision, where step length was reduced under BV compared to V (p = .006). The temporal–spatial parameters are summarized in Table 1.
Table 1 Temporal–spatial parameters (mean (SD)) during the obstacle crossing task. Variable of interest Walking speed (obstacle crossing task) (m/s) Pre-obstacle step
a, b, c, d
Step width (cm) Step length (cm)b Step time (seconds)
Obstacle step
Step width (cm) Step length (cm) Step time (seconds)b
Post-obstacle step
Step width (cm)b,
d
Step length (cm) Step time (seconds) a b c d
Indicates Indicates Indicates Indicates
significant significant significant significant
Group
V+no-GVS
BV+no-GVS
V+GVS
BV+GVS
YA OA
.92 (.09) .94 (.17)
.91 (.11) .84 (.18)
1.02 (.14) .94 (.18)
.94 (.13) .86 (.20)
YA OA YA OA YA OA
21.7 (2.7) 20.7 (4.0) 64.0 (13.4) 67.8 (10.6) .62 (.10) .67 (.12)
23.0 (2.7) 20.9 (3.5) 65.6 (14.4) 61.7 (11.1) .67 (.10) .68 (.15)
22.9 (4.9) 21.9 (4.1) 66.7 (13.6) 61.5 (13.6) .66 (.13) .63 (.09)
23.6 (3.4) 22.5 (5.9) 62.3 (9.4) 61.4 (9.0) .65 (.08) .68 (.14)
YA OA YA OA YA OA
20.6 (3.0) 21.0 (4.6) 65.2 (12.6) 72.6 (6.5) .74 (.11) .80 (.17)
20.4 (2.7) 21.8 (6.9) 66.2 (17.9) 73.0 (10.5) .79 (.14) .86 (.16)
20.2 (3.7) 21.4 (5.5) 71.1 (10.7) 73.5 (7.9) .73 (.06) .76 (.15)
21.1 (4.4) 23.6 (5.3) 71.4 (10.9) 73.3 (9.6) .77 (.12) .84 (.20)
YA OA YA OA YA OA
21.3 (1.9) 22.0 (4.3) 73.3 (10.4) 74.0 (10.8) .77 (.12) .75 (.13)
20.5 (3.9) 26.4 (4.2) 73.8 (18.2) 65.8 (18.7) .78 (.15) .74 (.08)
20.6 (3.6) 22.6 (7.2) 81.5 (15.1) 72.9 (18.2) .74 (.08) .75 (.07)
21.8 (4.2) 26.8 (5.0) 79.0 (18.6) 65.8 (21.3) .77 (.08) .75 (.10)
main effect of group. main effect of vision. main effect of GVS. interaction effect of vision in older group.
Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
6
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
3.2. Whole body and segmental control parameters In terms of whole body control, vision significantly influenced medial–lateral COM displacement, where BV condition showed greater peak M-L deviation compared to the V condition and greater vertical range compared to normal vision (p < .01), irrespective of age or GVS condition. No significant main effect of age, GVS condition or vision was found on peak vertical displacement of the COM when crossing the obstacle (p > .05) (Fig. 3). When considering segmental control, statistical analysis revealed no effect of age, vision or GVS condition on head pitch angle or trunk roll angle (p > .05). However, the OA group showed greater maximum trunk pitch and head roll angles compared to YA, under both visual and GVS conditions (p < .012) (Fig. 4). A significant age vision interaction effect revealed that under the blurring condition, the older group only also showed greater peak to peak trunk pitch angles compared to intact vision condition (Fig. 5).
4. Discussion The present study is the first to investigate age-related differences in the influence of deteriorated visual–vestibular information on locomotor control during an obstacle crossing task. The main findings demonstrate a significant reliance on visual but not vestibular information for locomotor control during obstacle crossing, and this is not differentially affected by aging. However, age-specific alterations in whole body and segmental control may place older adults at a greater risk of imbalance or inability to recover from a possible trip during obstacle crossing in the presence of sub-optimal visual information.
Fig. 3. Peak vertical COM displacement (cm) (a), range vertical COM displacement (cm) (b), peak M–L (medial–lateral) COM displacement (cm) (c), range M–L COM displacement (cm) (d) in young adults (black) and older adults (gray) across vision conditions (V: full vision; BV: blurred vision) and GVS conditions (no-GVS, GVS) when lead limb is crossing obstacle. Error bars represent 1 SD from the mean. ⁄Indicates a significant main effect of vision. Maximum M–L COM displacement was greater under BV compared to V conditions, irrespective of age and GVS conditions. Indicates significant main effect of age. Vertical COM range greater in older adults compared to young adults, irrespective of vision and GVS conditions.
Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
7
Fig. 4. Maximum head roll angle (degrees) (a), range headroll angle (degrees) (b) maximum head pitch angle (degrees) (c), range head pitch angle (degrees) (d) in young adults (black) and older adults (gray) across vision conditions (V: full vision; BV: blurred vision) and GVS conditions (no-GVS, GVS) when lead limb is crossing obstacle. Error bars represent 1 SD from the mean. ⁄ Indicates a significant main effect of group. Maximum head roll angle was greater in older adults compared to young adults, irrespective of vision and GVS conditions.
4.1. Increased reliance on visual input during obstacle crossing in older persons The important role of vision during obstacle crossing has been well-established (Mohagheghi et al., 2004; Patla & Vickers, 1997). Using custom made blurring goggles, we were able to effectively reduce contrast sensitivity to levels similar to that of dense cataracts (Patla & Deshpande, 2007). In terms of global performance, the time taken for both young and older adults to cross the obstacle increased and the walking speed was slower with sub-optimal visual information despite similar walking speed between conditions during unobstructed walking. This is not surprising, as previous research has demonstrated that control of the lead limb is influenced predominantly by vision (McFadyen et al., 2007; Mohagheghi et al., 2004). Similar to other study using cataract simulation, visual system is unable to provide accurate exteroceptive information regarding the environment such as obstacle height and boundaries, resulting in longer time to complete the action to ensure safe and appropriate avoidance of the obstacle (Heasley, Buckley, Scally, Twigg, & Elliott, 2004, 2005). However, this would effectively lengthen the time spent in single support phase (as reflected by the increased step time during the obstacle step). As a result, individuals would increase the amount of time spent having to control their COM within a narrow and moving base of support (Winter, 1990) with declines in visual information, placing them at greater risk for loss of balance. In terms of whole body control, sub-optimal visual input resulted in greater medial–lateral deviation of the COM. Again, this finding was not differentially affected by aging. When completing a single step-up from a static position, older adults have utilized a strategy which would effectively minimize risk for medial–lateral instability (Heasley et al., 2005) with deteriorated visual information. However, our present results indicate a similar strategy does not transfer to ongoing, dynamic locomotion, as is the case with our obstacle crossing task. In the presence of sub-optimal visual input, obstacle crossing appears to challenge whole body balance control in the frontal plane to a greater degree in both young Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
8
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
Fig. 5. Maximum trunk roll angle (degrees) (a), range trunk roll angle (degrees) (b) maximum trunk pitch angle (degrees) (c), range trunk pitch angle (degrees) (d) in young adults (black) and older adults (gray) across vision conditions (V: full vision; BV: blurred vision) and GVS conditions (no-GVS, GVS) when lead limb is crossing obstacle. Error bars represent 1 SD from the mean. ⁄ Indicates a significant main effect of group. Maximum trunk pitch angle was greater in older adults compared to young adults, irrespective of vision and GVS conditions. Indicates significant interaction effect. Greater peak to peak trunk pitch angle in older group only for BV condition compared to V condition.
and older adults, as indicated by the increase in peak frontal plane displacement and vertical range of the body COM, with no change in step width. In the case of older adults, greater displacement paired with reduced strength (John, Liu, & Gregory, 2009) may hinder the ability to respond sufficiently in the event of a destabilization and increases risk of falls. Visual information is critical not only to maintain whole body equilibrium, but also to regulate segment orientation during obstacle crossing (Bent et al., 2002). We have shown age-related differences in trunk pitch and head roll angles during obstacle crossing, with further increases in trunk pitch displacement in the presence of blurred vision. The older adults are able to successfully navigate over the obstacle with demonstrated increases in anterior–posterior trunk motion. Of note, the older group do not present with a more stooped posture than the younger group when measured statically. Previous research has shown that coupling of the head and trunk segments optimizes visual and vestibular contributions to postural control and is a generalized strategy adopted by older adults during locomotion (Deshpande & Patla, 2007). In this vein, the general age-related increase in trunk flexion during dynamic movement coincides with head flexion and likely occurs to acquire environmental information (i.e., ground scanning) while reducing the complexity of postural control. Although we did not measure distance of lead foot contact from obstacle, literature consistently shows that older adults place their lead limb closer to the obstacle when compared to young adults (Chen et al., 1991; Lowrey et al., 2007), which effectively shorten the base of support in the anterior–posterior direction. If this was the case in our group of older adults, they would be required to control larger motions of their trunk within reduced base of support (Lowrey et al., 2007), posing a greater threat to an older person’s dynamic stability. In the absence of optimal vision, the risk of balance instability is further emphasized. That medial–lateral trunk control was not significantly influenced by aging or vision could suggest the obstacle crossing task was not challenging enough to induce frontal plane instability under impoverished sensory conditions. Conversely, by slowing down obstacle crossing time, the older adults may
Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
9
maintain medial–lateral upper body control to similar levels of the young group even in the presence of sub-optimal sensory information.
4.2. Discordant vestibular information does not impact whole body and segmental control during obstacle crossing in older adults McFadyen et al. (2007) have investigated the role of vestibular system information during obstacle crossing in young adults when normal vision was either available or was occluded completely. The authors reported that vestibular information was not up-regulated for obstacle avoidance in healthy young adults given the lack of differences between level ground walking and obstacle crossing. Our present work took this further, and examined the effects of aging and the visual–vestibular influences on the obstacle crossing task when visual information was suboptimal but not completely absent. We found that vestibular information is not up-regulated for obstacle avoidance; this was not differentially affected by aging. This is in contrast to our hypothesis, where we expected GVS induced instability to increase further under sub-optimal visual conditions. Under similar vision manipulations, Deshpande and Patla (2007) have reported reduced path deviation while walking as the distance from the target (locate at 6.5 m from the starting point) reduced, suggesting that the dependence on the vision increases as the target distance decreases. Standing posture studies have also demonstrated differences in the integration of visual information for postural control depending of the target distance (Bonnet, Temprado, & Berton, 2010). In the obstacle crossing condition the target is at a closer distance and possibly within the distance range where the vision can be the dominant sensory information. Further, exteroceptive cues provided by the central visual field regarding the height, width and location of the obstacle in the path could be used in a feed-forward manner to plan the gait parameter adaptations required for safely negotiating the challenges (Patla & Vickers, 1997) thus minimizing dependence on the vestibular system. GVS also induces binaural stimulation resulting in a predominantly lateral perturbation whereas obstacle crossing while walking along a straight path is a largely anterior–posterior movement. McFadyen et al. (2007) showed that despite significant lateral deviations in the trunk displacement and foot trajectory associated with GVS, during obstacle crossing sagittal plane control of foot trajectory and body displacement was unaffected in young adults even when vision was completely occluded. Our lack of differences in medial–lateral head and trunk displacements in response to GVS may suggest an overall down regulation of the vestibular system gain during obstacle crossing when some visual information is available. It should be kept in mind that both older and young adults walked faster with sub-optimal vestibular information during both unobstructed walking and during the obstacle crossing task. It is plausible that when gait speed is controlled between conditions, the findings would differ. It should also be noted that the task was completed on a firm surface, providing accurate lower limb proprioceptive feedback. Future study should consider the role both gait speed and of proprioception on reweighting of the other sensory systems to navigate through obstacles.
5. Conclusion The investigation of balance control mechanisms during walking in various, challenging environments is necessary to understand how older adults perform tasks of daily living and the role of sensory information in those tasks. This is the first study to investigate the effects of aging and the visual–vestibular influences on whole body and segmental control during obstacle crossing. Even in the presence of sub-optimal visual information, the vestibular input was not up-regulated for obstacle crossing and this was not differentially affected by aging. The results indicate an increased reliance on visual information for task completion. In older adults, mal-adaptations in anterior trunk movement and larger medial–lateral displacement of the body COM with insufficient visual information may place them at a greater risk of imbalance when stepping over an obstacle. Future work should consider the role of lower limb proprioception on sensory reweighting in older adults during obstacle avoidance. Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009
10
A.C. Novak, N. Deshpande / Human Movement Science xxx (2014) xxx–xxx
Role of sponsor None. Conflict of interest The authors declare that they have no conflict of interest. Acknowledgements The authors would like to thank Patricia Hewston, Mika Yoshikawa and Fang Zhang for assistance with data collection. This project was funded by the Senate Advisory and Research Committee (SARC), Queen’s University to Dr. Deshpande. References Bent, L. R., McFadyen, B. J., & Inglis, J. T. (2002). Visual–vestibular interactions in postural control during the execution of a dynamic task. Experimental Brain Research, 14, 490–500. Bonnet, C. T., Temprado, J. J., & Berton, E. (2010). The effects of the proximity of an object on human stance. Gait & Posture, 32, 124–128. Chen, H. C., Ashton-Miller, J. A., Alexander, N. B., & Schultz, A. B. (1991). Stepping over obstacles: Gait patterns of healthy adults. Journal of Gerontology, 46, M196–M203. Deshpande, N., Novak, A., & Patla, A. E. (2006). Determining functional mobility using the modified timed up and go test: Effects of sensory manipulations. Journal of the American Geriatrics Society, 54, 1157–1158. Deshpande, N., & Patla, A. E. (2007). Visual–vestibular interaction during goal directed locomotion: Effects of aging and blurring vision. Experimental Brain Research, 176, 43–53. Frank, J. S., & Patla, A. E. (2003). Balance and mobility challenges in older adults: Implications for preserving community mobility. American Journal of Preventative Medicine, 25, 157–163. Hahn, M. E., & Chou, L. S. (2004). Age-related reduction in sagittal plane center of mass motion during obstacle crossing. Journal of Biomechanics, 37, 837–844. Heasley, K., Buckley, J. G., Scally, A., Twigg, P., & Elliott, D. B. (2004). Stepping up to a new level: Effects of blurring vision in the elderly. Investigations in Opthalmology and Vision Science, 45, 2122–2128. Heasley, K., Buckley, J. G., Scally, A., Twigg, P., & Elliott, D. B. (2005). Falls in older people: Effects of age and blurring vision on the dynamics of stepping. Investigations in Opthalmology and Vision Science, 46, 3584–3588. Horak, F. B. (2006). Postural orientation and equilibrium: What do we need to know about neural control of balance to prevent falls? Age & Ageing, 35, ii7–ii11. Horak, F. B., Nashner, L. M., & Diener, H. C. (1990). Postural strategies associated with somatosensory and vestibular loss. Experimental Brain Research, 82, 167–177. John, E. B., Liu, W., & Gregory, R. W. (2009). Biomechanics of muscular effort: Age-related changes. Medicine in Science & Sports Exercise, 41, 418–425. Lord, S. R., & Dayhew, J. (2001). Visual risk factors for falls in older people. Journal of the American Geriatric Society, 49, 508–515. Lowrey, C. R., Watson, A., & Vallis, L. A. (2007). Age-related changes in avoidance strategies when negotiating single and multiple obstacles. Experimental Brain Research, 182, 289–299. McFadyen, B. J., Bouyer, L., Bent, L. R., & Inglis, J. T. (2007). Visual–vestibular influences on locomotor adjustments for stepping over an obstacle. Experimental Brain Research, 179, 235–243. Mohagheghi, A. A., Moraes, R., & Patla, A. E. (2004). The effects of distant and on-line visual information on the control of approach phase and step over an obstacle during locomotion. Experimental Brain Research, 155, 459–468. Mozolic, J. L., Hugenschmidt, C. E., Peiffer, A. M., & Laurienti, P. J. (2012). Multisensory Integration and Aging. In M. M. Murray & M. T. Wallace (Eds.), The Neural Bases of Multisensory Processes. Boca Raton, FL: CRC Press. Novak, A. C., & Deshpande, N. (2011). Comparing effects of deteriorated sensory information on sit-to-stand performance of young and older adults – A pilot study. Journal of the American Geriatric Society, 59, 562–563. Patla, A. E., & Vickers, J. N. (1997). Where and when do we look as we approach and step over an obstacle in the travel path? Neuroreport, 8, 3661–3665. Patla, A. E., & Deshpande, N. (2007). Visual-vestibular interaction during goal directed locomotion: effects of aging and blurring vision. Experimental Brain Research., 176, 43–53. Pozzo, T., Levik, Y., & Berthoz, A. (1995). Head and trunk movements in the frontal plane during complex dynamic equilibrium tasks in humans. Experimental Brain Research, 106, 327–338. Shumway-Cook, A., & Woollacott, M. H. (2007). Motor Control: Translating research into clinical practice (3rd ed.). Philadelphia: Lippincott Williams and Wilkins. Winter, D. A. (1990). Biomechanics and motor control of human movement (2nd ed.). New York: Wiley Inter-Science.
Please cite this article in press as: Novak, A. C., & Deshpande, N. Effects of aging on whole body and segmental control while obstacle crossing under impaired sensory conditions. Human Movement Science (2014), http:// dx.doi.org/10.1016/j.humov.2014.03.009