The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 62:1042-1047 (2007)
© 2007 The Gerontological Society of America
Age-Related Deficits in Early Response Characteristics of Obstacle Avoidance Under Time Pressure
Vivian Weerdesteyn,
Bart Nienhuis,
Alexander C. H. Geurts and
Jacques Duysens
1 Department of Rehabilitation Medicine, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands.
2 Sint Maartenskliniek Research, Development & Education, Nijmegen, The Netherlands.
3 Institute for Fundamental and Clinical Human Movement Sciences, Faculty of Human Movement Sciences, Vrije Universiteit, Amsterdam, The Netherlands.
Address correspondence to Vivian Weerdesteyn, PhD, Department of Rehabilitation Medicine, Radboud University Nijmegen Medical Centre, PO Box 9101, 6500 HB Nijmegen, The Netherlands. E-mail: v.weerdesteyn{at}reval.umcn.nl
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Abstract
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Background. Obstacles in the travel path are a frequent cause of falls among elderly persons. In obstacle avoidance under time pressure, elderly persons have been reported to be less successful than young persons, but possible age-related deficits at the neuromuscular control level have not been studied yet.
Methods. In the present study, obstacle avoidance reactions were investigated in 15 young and 9 older adults. While the participants walked on a treadmill, an obstacle was dropped in front of the left foot either in late stance, early swing, or mid-swing. Muscle activity in response to the obstacle was measured from the left biceps femoris (BF), rectus femoris (RF), tibialis anterior (TA), and medial head of gastrocnemius (GM). Avoidance success rates, as well as initial response latencies and response amplitudes over the first 50 ms of the response, were determined.
Results. In both young and older adults, a large initial response was consistently observed in BF at very short latencies (104–111 ms in the young group), especially for mid-swing obstacle presentations (yielding the highest time pressure). Onset latencies in the elderly group were delayed by 10 ms on average. Response amplitudes were larger in young than in older adults, most prominently in BF and RF, but with a similar tendency in TA. Both onset latency and response amplitude were significantly associated with avoidance success rates.
Conclusions. The results of the present study suggest that age-related deficits in the neuromuscular control of obstacle avoidance could play a role in the large numbers of obstacle-related falls in the elderly population.
APPROXIMATELY 30% of people older than 65 years fall at least once a year, and these falls are a common source of injuries (1–4). The majority of falls in community-dwelling elderly persons have been reported to occur during walking (5), and 44% of falls occur in the presence of environmental hazards, such as obstacles or slippery surfaces (1). These statistics suggest a role of declined adaptive walking skills in elderly persons. Insight into the nature of these deficits could help to improve intervention strategies to prevent falls and related injuries.
Previous studies of aging effects on slips and trips during walking have shown that aging only had a very limited effect on response latencies of lower extremity muscles (6–9). Electromyogram (EMG) response amplitudes, however, exhibited a more pronounced decline. It was also shown that reduced force generation in response to a trip was associated with unsuccessful balance recovery (8). In daily life, however, visually guided step adjustments to prevent obstacle contacts that can lead to trips and consequent falls occur much more frequently. For these types of gait adjustments, which can be made at surprisingly short latencies (EMG onsets at 
95 ms, kinematic changes at 120 ms) (10–12), the effects of aging on neuromuscular characteristics have not been studied yet. Direct inferences on aging effects on these types of reactions cannot be made from previous studies on trips or slips, because the responses originate from different input sources (visual vs cutaneous or proprioceptive information). The implications of deficits in both types of response, however, are functionally important. Delayed and less efficient responses would place elderly persons at a larger risk for both obstacle contact and consequent falls.
Previous studies of visually guided gait adjustments under time pressure have provided clear evidence that elderly persons have increased difficulties in adequately performing these fast reactions. It was shown that advancing age had a detrimental effect on the success of obstacle avoidance (13–16). In addition, lower avoidance success rates appeared to be associated with increased fall risk in daily life (15), although it remained unclear whether reduced success was related to delayed reactions and/or to insufficient power or strength. Hence, to further understand the relationship between obstacle avoidance skills, falls, and the potential targets for training, there is a clear need to gain insight into the nature of age-related neuromuscular control deficits in obstacle avoidance under time pressure in the elderly population. In the present study the hypothesis was tested that, in response to a sudden obstacle, elderly persons would have delayed muscle onset latencies and lower initial response amplitudes (50 ms after response onset) and that these age-related deficits were associated with reduced success.
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METHODS
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Participants
A total of 15 young (13 women, 2 men, mean age 24.4 ± 2.8 years) and 9 older adults (7 women, 2 men, mean age 70.8 ± 4.9 years) participated in this study. The young participants were students at the Radboud University. The elderly participants were recruited from the community by an advertisement posted in a local newspaper. All individuals regularly participated in sports activities, and none of them suffered from any neuromuscular disorder, as confirmed by self-report. They all gave written informed consent to participate in the study. The study was approved by the local medical ethics committee.
Procedure
The participants walked on a treadmill (Type EN-tred Reha; ENRAF Nonius, Rotterdam, The Netherlands) at a fixed gait speed of 3 km/h and at a fixed position so that the most anterior position of the toes was approximately 10 cm in front of the obstacle prior to its release. A bridge, to which an electromagnet was attached, was placed over the front of the treadmill [see (9,11,15–17)] and held the wooden obstacle via an embedded piece of iron (see Figure 1a). The length, width, and height of the obstacle were 40 cm, 30 cm, and 1.5 cm, respectively. The obstacle could be released by a trigger from a computer and always fell in front of the left foot. To prevent falls, the participants wore a safety harness that was fixed to the ceiling.
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Figure 1. a, Schematic diagram of the experimental setup. Inset: Stick figures show the three phases of obstacle release, late stance (LSt), early swing (ESw), and mid-swing (MSw). b, Single trial electromyogram (EMG) responses (black lines) of biceps femoris (BF), rectus femoris (RF), tibialis anterior (TA), and medial head of the gastrocnemius (GM) in reaction to the obstacle. Gray area: mean ± 2 standard deviations of the EMG activity during unperturbed walking. Time = 0 ms corresponds to the moment of obstacle release. Dashed line: BF onset. Response amplitudes were determined for five 10 ms bins (dotted lines) following BF onset
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Reflective markers were attached to the left heel, the left hallux, and the obstacle. A three-dimensional motion analysis system (Primas; TU Delft, The Netherlands) recorded marker positions at a sample rate of 100 Hz. To determine the correct moment of obstacle release, heel marker positions were processed in real time. Algorithms, based on heel strike moment and position, were used to predict the normal landing position (11). Based on this information, the moment at which the obstacle had to be dropped to achieve a given step cycle condition was determined. The obstacle was only released when a stable walking pattern was accomplished such that there were five strides with a maximum difference of 50 ms between consecutive strides.
Prior to the experimental procedure, each participant performed five practice trials of obstacle avoidance to become familiar with treadmill walking and stepping over the obstacle. The experimental procedure consisted of three series of 10 obstacle avoidance trials. To introduce three levels of time pressure, the obstacle was dropped randomly at three different moments of the step cycle: late stance (LSt, 45%–60% of the step cycle), early swing (ESw, 60%–70%), or mid-swing (MSw, 70%–85%). These phases corresponded to available response times (ARTs) of 450 ms, 350 ms, and 250 ms, respectively. ART is defined as the time between obstacle release and the moment that the hallux marker would cross the front of the obstacle when no avoidance reaction would occur. Obstacle avoidance trials with smaller ARTs were more challenging.
After the release of the obstacle, participants were requested to step over it. Contact of the left foot with the obstacle was considered a failure. Surface EMG data were collected from left tibialis anterior (TA), medial head of gastrocnemius (GM), rectus femoris (RF), and biceps femoris (BF) using self-adhesive electrodes (Ag/AgCl) (Conmed Neotrode, Utica, NY) placed approximately 2 cm apart and longitudinally on the belly of the muscle, according to international guidelines (18). The EMG signals were band-pass filtered (10–500 Hz) and sampled at 2400 Hz.
Data Sampling and Analysis
First, avoidance success rates were calculated for each of the three phases of obstacle release. For the analysis of EMG data, EMG activity of the selected muscles was full-wave rectified and low-pass filtered at 25 Hz (zero-lag, second order Butterworth filter). Strides prior to obstacle release in the 30 trials were used as control strides. Control stride muscle activity was ensemble averaged, and 2 standard deviations (SD) around the mean were calculated.
Subsequently, the muscle onset latency was determined by a combination of computer algorithm and visual inspection (to ensure data quality) on a single trial basis. Onset latency was defined as the time between obstacle release and the instant at which the EMG activity exceeded, for at least 30 ms, the average control stride activity plus 2 SD. BF was consistently activated first for nearly all the avoidance responses following obstacle release (Figure 1b). Consequently, the latency of this muscle was the main focus of the present study.
Because in time-critical conditions the kinematic responses are expected to depend heavily on the early muscle activations, we were particularly interested in the EMG amplitudes of the initial 50 ms after onset. Hence, response amplitudes of the four selected muscles were calculated over five bins of 10 ms following BF onset (see Figure 1b). For every bin and every muscle, response amplitudes were normalized with respect to the average control activity in the corresponding phase of the step cycle during unperturbed gait.
Repeated-measures analyses of variance (ANOVAs) with post hoc contrasts and pairwise comparisons were conducted to investigate the effects of age on avoidance success rates, and onset latencies, whereas a multivariate ANOVA (MANOVA) was used to analyze response amplitudes. Phase and Bin were introduced as within-subject factors and Age as a between-subject factor. Because the distribution of response amplitudes was skewed due to a number of relatively large values (as confirmed by analyses of normality), statistical analysis was conducted on logarithm-transformed data. In addition, a linear regression analysis was conducted to examine whether onset latencies and response amplitudes could predict success rates. The alpha level was set at 0.05.
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RESULTS
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Avoidance Success Rates
Success rates of the older adults on the obstacle avoidance task were significantly lower than those in the young group (mean ± SD, 89.7 ± 5.8% vs 96.31 ± 7.3%, F(1,22) = 6.06, p =.022, 95% confidence interval [CI], 1.0–12.2%) (Figure 2). In both young and older adults, obstacle avoidance success rates decreased with increasing time pressure. Overall, success rates in LSt (98.8 ± 2.9%) were significantly larger than in ESw (92.9 ± 8.7%, p <.001, 95% CI, 3.1–8.7%) and in MSw (87.2 ± 16.2%, p =.003, 95% CI, 4.2–18.9%). The effect of time pressure was more pronounced in the elderly participants, as indicated by a significant Age x Phase interaction effect on success rates (F(2,21) = 6.344, p =.007). The young participants had similar near-optimal success rates in LSt and ESw, whereas in the older adults increasing time pressure already affected the performance in ESw.
Response Onset Latencies and Amplitudes
The response to the approaching obstacle was characterized by an initial fast (on average 112.3 ms) and large-amplitude burst of BF (on average 14.4 times larger than the activity in the corresponding phase during unperturbed walking), followed by enhanced activity of RF, TA, and GM after about 0–20 ms (Figure 1b). Compared to BF onsets in the young participants, those in the older adults were significantly delayed (108.4 ± 11.0 vs 118.9 ± 10.9 ms, F(1,22) = 5.18, p =.033, 95% CI, 0.9–20.1 ms) (Figure 3). In both age groups, BF onset latencies decreased with increasing time pressure. Onsets in MSw were significantly shorter than in LSt (108.3 ± 12.7 ms vs 114.9 ± 10.7 ms, p =.022, 95% CI, 1.0–11.7 ms) and in ESw (108.3 ± 12.7 ms vs 113.8 ± 15.2 ms, p =.027, 95% CI, 0.6–10.0 ms). There was no significant Age x Phase interaction (F(2,21) = 0.04, p =.961).
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Figure 3. Mean values ± standard error of the mean of the onset latencies of the biceps femoris (BF) in response to the obstacle for young and older adults for late stance (LSt), early swing (ESw), and mid-swing (MSw) obstacle release conditions. *Age effect, p <.05;  phase effect, p <.05
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Overall, response amplitudes (ln transformed normalized values) in the older adults were significantly smaller than those in the young group (1.01 ± 0.17 vs 1.38 ± 0.36, F(1,22) = 5.44, p =.029, 95% CI, 0.03–0.56) (Figure 4). At the level of the individual muscles, post hoc ANOVAs yielded significant age-related differences in response amplitudes of both upper leg muscles (BF: 2.54 ± 0.57 vs 2.13 ± 0.43, p =.039, 95% CI, 0.03–0.91; RF: 0.89 ± 0.56 vs 0.49 ± 0.23, p =.042, 95% CI, –0.02 to 0.74), although a similar tendency of smaller amplitudes in the older adults could be observed in TA (1.03 ± 0.41 vs 0.75 ± 0.40, p =.153, 95% CI, –0.11 to 0.63). GM amplitudes were quite comparable between young and older adults (1.05 ± 0.45 vs 0.95 ± 0.26, p =.332, 95% CI, –0.18 to 0.51). In addition, following onset, BF activity increased faster in the young compared to the older adults (Age x Bin interactions, bin 1 vs bin 2 and bin 1 vs bin 3, F(1,22) = 4.92–7.33, p <.05) (Figure 5). Both BF onset latency and overall response amplitude were significantly associated with success rate (p =.037 and p =.010, respectively), explaining 46.8% of variance. Longer onset latencies and smaller amplitudes were associated with lower success rates.
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Figure 4. Mean values ± standard error of the mean of the ln-transformed normalized response amplitudes of biceps femoris (BF), rectus femoris (RF), tibialis anterior (TA), and medial head of the gastrocnemius (GM) for late stance (LSt), early swing (ESw), and mid-swing (MSw) obstacle release conditions for young and older adults. *Age effect, p <.05; phase effect, p <.05. EMG = electromyogram
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Figure 5. Mean values ± standard error of the mean of the ln-transformed normalized response amplitudes of biceps femoris (BF) for young and older adults for the five 10-ms bins following onset. *Age effect, p <.05; Age x Bin interaction, p <.05. EMG = electromyogram
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DISCUSSION
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To our knowledge, this is the first study to investigate the effects of aging on EMG onset latencies and response amplitudes in a time-critical obstacle avoidance task. The results confirmed the hypothesis that, compared to young adults, elderly persons have both delayed onsets and reduced response amplitudes, and that this could partly explain their lower avoidance success rates. The lower success of our elderly participants is in line with previous findings (13–16), but in addition, the present study provides insight into the potential mechanisms underlying this deficit.
In the present task, BF was consistently activated first in response to the obstacle. The preferential recruitment of upper leg muscles, and particularly of BF, in this visually guided reaction is remarkably similar to both ipsilateral and contralateral responses in other types of gait perturbations (7,19). The prominent role of BF in obstacle avoidance can be understood from its function as a knee flexor. Active knee flexion is necessary to lift the leg over the obstacle. The small difference in onset latencies between the young and elderly participants (10.4 ms) corresponds well with the previously observed delayed onsets of responses to induced slips and trips in elderly persons (6–9), and of balance-correcting responses to support surface perturbations (20,21). The small delay seems to be in contrast with the larger age-related muscle onset delays as reported for more cognitively mediated gait adjustments, such as starting or stopping after a visual go or stop signal (22,23). However, previous studies have provided evidence that step adjustments in response to obstacles or target displacements are probably not controlled cognitively (10–12). The response latencies indicated that the first adjustments occur well before voluntary control comes into play. It follows that the observed age-related delay in onset latencies in response to a sudden obstacle is not likely to be due to slowing of cognitive processing. Instead, the slowing could result from other elements, such as increased visual motion detection thresholds (24) and/or reduced nerve conduction velocity (25).
The smaller response amplitudes also agree very well with the results from previous reactive balance and gait studies (6,7,9,21). In addition, prolonged burst durations and increased EMG rise times have been reported in combination with reduced amplitudes, which can be regarded as compensatory mechanisms for a decreased rate of muscle activation (6,7). In the present study, however, there was no clear indication of such compensations, as in the most prominent (BF) response, both age groups reached maximum activity 30–40 ms after onset (see Figure 5). The reduced amplitude, in combination with the lower rate of activation of BF and the delayed onset of the response, indicates that the flexion movement of the obstructed leg may be too little and too late in elderly persons to avoid contact with obstacles when under time pressure. This could explain why, in the present study, response onset and amplitude were significantly associated with avoidance success rates. The smaller EMG amplitudes may be explained by various age-related physiological changes, both in the nervous system (e.g., smaller numbers of motor neurons) (26) and in skeletal muscle properties (e.g., a reduced proportion of type II muscle fibers and overall muscle atrophy) (27).
It should be emphasized that the present results apply to a highly select group of elderly participants. Poorer performance can be expected from less active elderly persons in the general population. The individuals tested in the present study were still engaged in sports activities and may be regarded as an elite group, which was also reflected by their relatively high avoidance success rates. In a previous study, using the same setup and procedure, a group of ‘average’ elderly persons had much smaller success rates in the most time-critical conditions (67% for ARTs of 250–300 ms) (15), whereas the elderly participants in the present study were successful in 83% of mid-swing obstacle release trials with corresponding ARTs. However, as the participants were not screened by a physician to exclude subtle neuromuscular, neurosensory, or cognitive abnormalities, the possibility of some of these impairments to be present cannot be excluded.
A limitation of our study was that the experiments were conducted on a treadmill. Although previous studies using the same setup have yielded results on critical parameters that compared very well to over ground obstacle avoidance (13,15,16), the present results do not necessarily transfer to a real obstacle avoidance task on fixed ground. As a second limitation, obstacle avoidance success rates may be artificially inflated in this test due to the fact that participants knew that the obstacle would always fall in front of the left foot. In real life, one does not necessarily know which foot will be obstructed.
Conclusion
Both delayed onset latencies and reduced response amplitudes contributed to the impaired performance of elderly persons in avoiding obstacles under time pressure. The characteristics of the observed age-related declines were similar to those previously reported for automated gait and posture-correcting responses (6,7,9,20,21), but at present they are reported for fast, visually triggered responses. Deteriorated performance in these types of tasks has been shown to relate to increased fall risk (8,15,28). Hence, to prevent falls, it may be beneficial to specifically aim at the improvement of balance- and gait-correcting responses. Only few intervention studies, however, have addressed this issue. As a result, it is largely unknown what kind of exercises can improve these responses and at which levels of control these improvements could be achieved. A few sensorimotor training programs have shown beneficial effects on response latencies of balance-correcting responses (29,30), whereas high-intensity strength training may improve response amplitudes in response to a perturbation (31). With respect to time-critical obstacle avoidance, one study has reported increased avoidance success rates in conjunction with reduced numbers of falls as a result of a specialized training program, but neuromuscular avoidance characteristics were not investigated (32). Hence, to improve fall-preventive strategies, there is a clear need to further explore the working mechanisms of targeted interventions by evaluating training effects on balance- and gait-corrective responses at the neuromuscular control level.
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Acknowledgments
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This study was supported by the Organization for Healthcare Research in the Netherlands (ZonMW) and by an EU grant (Eurokinesis, QLK6-CT-2002-00151).
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Footnotes
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Decision Editor: Luigi Ferrucci, MD, PhD
Received June 12, 2006
Accepted November 20, 2006
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Abstract
Methods
Age x Phase interaction, p <.01