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. 2017 Dec 20;119(4):1528–1537. doi: 10.1152/jn.00979.2016

Age-related erosion of obstacle avoidance reflexes evoked with electrical stimulation of tibial nerve during walking

Sandra R Hundza 1,2,✉, Amit Gaur 1,2, Ryan Brodie 1,2, Drew Commandeur 1,2, Marc D Klimstra 1,2
PMCID: PMC5966742  PMID: 29357472

Abstract

In young healthy adults, characteristic obstacle avoidance reflexes have been demonstrated in response to electrical stimulation of cutaneous afferents of the foot during walking. It is unknown whether there is an age-related erosion of this obstacle avoidance reflex evoked with stimulation to the tibial nerve innervating the sole of the foot. The purpose of this study was to identify age-dependent differences in obstacle avoidance reflexes evoked with electrical stimulation of the tibial nerve at the ankle during walking in healthy young and older (70 yr and older) adults with no history of falls. Toe clearance, ankle and knee joint displacement and angular velocity, and electromyograms (EMG) of the tibialis anterior, medial gastrocnemius, biceps femoris, and vastus lateralis were measured. A significant erosion of kinematic and EMG obstacle avoidance reflexes was seen in the older adults compared with the young. Specifically, during swing phase, there was reduced toe clearance, ankle dorsiflexion, and knee flexion angular displacement in older adults compared with the young as well as changes in muscle activation. These degraded reflexes were superimposed on altered kinematics seen during unperturbed walking in the older adults including reduced toe clearance and knee flexion and increased ankle dorsiflexion compared with the young. Notably, during mid-swing the toe clearance was reduced in the older adults compared with the young by 2 cm overall, resulting from a combination of 1-cm reduced reflex response in the older adults superimposed on 1-cm less toe clearance during unperturbed walking. Together, these age-related differences could represent the prodromal phase of fall risk.

NEW & NOTEWORTHY This study demonstrated age-dependent erosion of obstacle avoidance reflexes evoked with electrical stimulation of the tibial nerve at the ankle during walking. There was significant reduction in toe clearance, ankle dorsiflexion, and knee flexion reflexes as well as changes in muscle activation during swing phase in older adults with no history of falls compared with the young. These degraded reflexes, superimposed on altered kinematics seen during unperturbed walking, likely represent the prodromal phase of fall risk.

Keywords: aging, cutaneous reflex, EMG, fall risk, kinematics, tibial nerve, toe clearance

INTRODUCTION

Influences of normal aging on the sensorimotor system results in age-related differences in gait and dynamic postural stability (Granata and Lockhart 2008; Kang and Dingwell 2008). However, some older adults experience falls whereas others do not, and it is currently unclear which changes specifically contribute to fall risk. It is, therefore, important to investigate age-related alterations in muscle activity and kinematics during walking in older adults with no fall history to better understand the normal aging process such that it can be differentiated from the clinical changes that contribute to fall risk (O’Loughlin et al. 1993). Studying reflexes evoked with perturbations to the foot during walking has provided a useful medium to probe the integrity in the neural control of walking (Zehr et al. 1998, 2012; Zehr and Loadman 2012). Given that for older adults, 59% of falls during walking result from tripping (Berg et al. 1997), examining reactions to perturbations to the foot during walking is particularly relevant to understand age-related changes in the integrity of the neuromechanical control of walking. In young healthy adults, previous work has demonstrated that characteristic stumble-corrective (obstacle avoidance) reflexes were elicited with both mechanically and electrically evoked perturbations to the foot during walking and resulted in similar obstacle avoidance strategies (Zehr et al. 1997). Furthermore, the obstacle avoidance reflexes produced a coordinated muscle and kinematic response that was functionally useful in avoiding the obstacle during continued walking. The reflexes were specific to the anatomical location of the perturbation on the foot (i.e., nerve stimulated) as well as the phase of gait cycle during human locomotion (Duysens et al. 1992; Zehr et al. 1997). In young healthy adults, perturbation to the dorsum of the foot resulted in reduced ankle dorsiflexion and greater knee flexion during swing phase (Eng et al. 1994; Zehr et al. 1997). In contrast, perturbations to the sole of the foot produced an ankle dorsiflexion reflex during stance-to-swing transition as well as a knee flexion reflex during mid-swing (Zehr et al. 1997).

Age-related changes in motor control have been shown to alter the obstacle avoidance reflex evoked with mechanical perturbations during walking (Schillings et al. 2005). Schillings et al. (2005) found that mechanical perturbation applied to the top of the foot during walking evoked smaller amplitude muscle reflexes in older adults. They did not see significant kinematic differences between age groups; however, this could possibly be explained by the lack of sensitivity of the kinematic measurement tool (i.e., electric goniometers). Recent work in our laboratory employed high-resolution kinematic analysis to investigate cutaneous reflexes evoked with electrical stimulation to the dorsum of the foot during walking in healthy younger and older adults (Hundza et al. 2015). We found that in older adults, obstacle avoidance reflexes for both the kinematic and muscle activation were affected. The reflex amplitude for toe clearance, ankle plantarflexion displacement and velocity, and knee flexion displacement and angular velocity were significantly reduced during swing phases. In accordance with the kinematics, tibialis anterior reflex amplitude was reduced in older adults (Hundza et al. 2015).

It is currently unclear if the age-related erosion of reflexes seen with stimulation to the dorsum of the foot would present similarly with perturbation to the sole of the foot. To that end, this study sought to determine if obstacle avoidance reflexes, including kinematic and muscle responses, evoked during walking with electrical stimulation of the tibial nerve at the ankle (innervating the sole of the foot), were reduced in magnitude in older adults with no history of falls compared with young adults. On the basis of previous findings of age-related changes to stumble reactions evoked with stimulation to the superficial peroneal nerve, we hypothesized that there would be an age-related degradation in both the EMG and kinematic (toe clearance as well as ankle and knee joint displacement and velocity) reflexes to tibial nerve stimulation during walking whereby older adults with no history of falls will have reduced amplitude compared with young adults. Furthermore, we hypothesize that the erosion will be nerve specific and will reduce the capacity to remove the end-point effector, the foot, from the perturbation during continued walking.

METHODS

Participants and Procedure

Twelve healthy young adults (Young) below the age of 40 yr (6 men, 6 women; mean age 25.4 ± 5.4 yr) and 12 healthy older adults (Old) above the age of 70 yr (8 men, 4 women; mean age 76.7 ± 4.8 yr) with no history of falls and free of any known neurological, musculoskeletal, or metabolic conditions participated in the study. A fall history included nonsyncopal falls in the previous 12 mo. Participants walked for ~10 min on a treadmill at an average walking speed of 2.24 ± 0.34 m/s for the Old and 2.56 ± 0.5 m/s for the Young (P = 0.06). Participants wore an overhead safety harness that was loosely suspended so that it did not provide extra stability during the experiment and that allowed for natural arm swing and would support the participant in case of an accidental fall. In addition, the treadmill had an automatic shutoff mechanism that was triggered in case there was a fall. The study protocol was approved by the Human Research Ethics Committee at the University of Victoria, and participants provided written and informed consent.

Nerve Stimulation

Surface electrodes (Thought Technology, Montreal, PQ, Canada) were applied over the distal tibial nerve at the right ankle. Throughout the walking cycle, electrical stimulation was delivered pseudorandomly with trains of five 1.0-ms pulses at 300 Hz using a stimulator (Grass S88; Grass Instruments, Astro-Med) connected in series with an SUI5 isolator and CCU1 constant current unit with no more than one stimulation per gait cycle and up to 3 gait cycles without simulation for a total of 240 stimulated cycles. The tibial nerve was stimulated at ~2 times radiating threshold (RT; where a clear radiating paresthesia was reported in the nerve innervation area) with a mean stimulation intensity of 2.1 ± 0.4 and 2.0. ± 0.4 times RT for the Old and Young, respectively (P = 0.29).

Electromyography

Bipolar surface EMG was recorded from ipsilateral (right) medial gastrocnemius (MG), tibialis anterior (TA), vastus lateralis (VL), and biceps femoris (BF) using disposable Ag-AgCl surface electrodes (Uni-Gel T3425; Thought Technology). Recording sites were shaved, gently abraded, and cleansed using an alcohol swab. Bipolar electrodes were positioned in accordance with SENIAM 8 guidelines (Hermens et al. 1999). Ground electrodes for EMG recordings were placed on nearby electrically neutral areas such as the patella. EMG recordings from all muscles were preamplified at a gain of 5,000, bandpass filtered at 30–300 Hz (Grass P511 AC amplifier; Grass Instruments, Astro-Med), and full-wave rectified.

Kinematics

Lower-limb kinematics and gait parameters were measured using eight Vicon MX-T20S three-dimensional motion analysis cameras (Vicon Motion Systems, Oxford, UK). Reflective markers were placed bilaterally on the pelvis, knee, ankle, head of the fifth metatarsal, and heel, and clustered makers were placed on the thigh, shank, and feet. Reconstruction of anatomical landmarks was based on the 6-degrees-of-freedom model (Collins et al. 2009) and used to determine joint angle, angular velocity, and toe height. Sagittal plane joint angles were calculated for the ankle and knee bilaterally from segment markers for the foot, shank, thigh, and pelvis. Joint angular velocity was calculated as the time differential of joint angular displacement. Toe clearance was determined as the vertical height of the fifth metatarsal head marker relative to the walking surface. The beginning of each gait cycle, corresponding to the timing of heel strike, was based on the time index when the ipsilateral heel marker reached its lowest vertical point.

Data Acquisition and Analysis

EMG data were sampled at 1,000 Hz using a 16-bit analog-to-digital converter connected to a computer running custom-written LabView software (National Instruments, Austin, TX), whereas kinematic data were sampled at 100 Hz using Vicon Nexus 1.7.2 software and analyzed using Visual 3D software. Kinematics data were interpolated using cubic spline, synchronized with EMG data, and Butterworth filtered at 10 Hz using custom-written MATLAB software (The MathWorks, Natick, MA). Postacquisition, all data were partitioned into 16 equal time bins based on division of the gait cycle, beginning with initiation of stance at heel strike (Zehr et al. 1997). EMG and kinematic responses (i.e., perturbed) to the stimuli occurring in each bin were averaged. EMG and kinematic data recorded without stimulation (i.e., background) for each bin were also averaged. Subtracted reflex traces for EMG and kinematic responses to stimulation were calculated by subtracting background EMG from the reflex EMG for each bin of the gait cycle (~10–20 observations per bin).

EMG Analysis

EMG reflexes were only considered significant if their amplitude was over a 2-SD band calculated from prestimulus subtracted values. The reflexes for each participant were analyzed for “net reflex effect” using the average cumulative reflex activity stimulation (ACRE125) (adapted from Zehr et al. 1997, 2000). This sum was then divided by the time interval (i.e., 75 ms; adapted from Zehr et al. 1997, 2000). A window of 50–125 ms was chosen to capture the response necessary to relate the net EMG reflex effect with the net mechanical outcome (i.e., movement kinematics; see below) while minimizing significant voluntary contributions (Zehr et al. 1995, 1997). All EMG amplitudes (i.e., mean reflex and background) were normalized to the maximum background EMG recorded during the unperturbed walking cycle.

Kinematic Analysis

Angular displacement reflexes were taken as the maximal excursion in mean subtracted traces from a 70- to 220-ms window ACRE(150). This window was chosen to reflect the delays between the EMG response and the peak mechanical response based on an electromechanical delay in human skeletal muscle (Cavanagh and Komi 1979), as well as the presence of the peak response in both the Young and Old. Angular velocity reflexes were taken as the peak amplitude of mean subtracted velocity within this window. Toe clearance was the vertical height of the fifth metatarsal head marker relative to the walking surface.

Statistical Analysis

Using Statistica 10.0 (StatSoft) a 2 × 16 repeated-measures analysis of variance (ANOVA) was conducted separately for unperturbed background EMG and kinematics (joint angular displacement and velocity and toe clearance), as well as for reflex (subtracted) EMG and kinematics, to determine significant main effects for age and significant age-bin interactions. A Fisher’s least significant difference (LSD) post hoc analysis was used when significant interactions were found to determine significant differences between age groups at each bin; this less conservative approach was chosen to match the exploratory nature of the study. Descriptive statistics include mean and SE. Statistical significance level was set at P ≤ 0.05.

RESULTS

Cutaneous Reflexes During Walking

Toe clearance reflex.

Group means for toe clearance reflex are displayed in Fig. 1A. There was a significant main effect for toe clearance reflex between the cohorts [F(1,22) = 6.8, P = 0.02] and a significant interaction between age and bin [F(15,330) = 2.0, P = 0.02], with significantly different reflex amplitudes between cohorts at terminal stance (bin 9) and early-mid swing (bins 11 and 12). The toe clearance reflex moved the toe closer to the ground by 6.5 mm at bin 11 in the Old compared with the Young, and at bin 12 the movement of the toe away from the ground was 9.7 mm less in the Old compared with the Young (see Table 1). Interestingly, at terminal stance (bin 9) there was a reduction in toe clearance in the Old of 4.9 mm, whereas there was an increase in toe clearance in the Young of 4.3 mm, with a total difference between cohorts of 9.3 mm (see Fig. 1A and Table 1). For each of these differences, the reflex resulted in the foot being closer to the ground in the Old compared with the Young. Representative single-subject reflex data for toe clearance for bin 12 are displayed in Fig. 2E.

Fig. 1.

Fig. 1.

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Toe clearance. Data are group means across the gait cycle in older adults (Old) and young adults (Young) for reflex (perturbed minus unperturbed; A), background (unperturbed; B) and perturbed (background + reflex; C) toe clearance. †P < 0.05, significant main effect for age. #P < 0.05, significant interaction. *P < 0.05, subsequent significant difference between groups at the indicated bin (post hoc Fisher’s LSD of significant interactions).

Table 1.

Differences in kinematics between age cohorts

Gait Cycle Bins
9 10 11 12 13 14 15 16 1
Toe clearance, mm
    Background 0.6 1.7 10.2 9.5 −0.7 −7.2 −6.2 8.3 5.0
    Reflex 9.3 3.2 6.5 9.7 4.2 1.5 −3.0 3.3 1.8
    Combined 9.9 4.9 16.7 19.1 3.5 −5.7 −9.2 11.5 3.1
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Values represent differences between cohort means (Young minus Old). Values in bold type represent a significant difference between cohorts based on post hoc LSD of significant interactions. Only swing phase is displayed from toe-off (bin 9) to heel strike (bin 1). Swing phase is typically when the foot encounters an obstacle.

Fig. 2.

Fig. 2.

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Single-participant mid-swing toe clearance and ankle traces. Background (A–D) and reflex traces (E–H) are shown for bin 12 in an Old and Young participant for toe clearance (A, E), ankle angular displacement (B, F), MG EMG (C, G), and TA EMG (D, H).

Ankle kinematic and EMG reflexes.

Group means for ankle kinematic reflexes for the Old and Young during perturbed walking are displayed in Fig. 3, E and F. A main effect for age for ankle displacement [F(1,22) = 8.15, P = 0.01] and a significant interaction of age and bin [F(15,330) = 2.4, P = 0.003] were found. A reduced reflex amplitude of dorsiflexion displacement was found in the Old compared with the Young during terminal stance, toe off, and swing (Bins 9, 10, 12, 13, and 15) with mean differences of 4.38°, 3.75°, 2.23°, 2.71°, and 2.09° at each bin, respectively. Group comparisons of ankle angular velocity showed a significant main effect for age [F(1,22) = 5.8, P = 0.03] with an overall slower angular velocity in the Old; however, there was no significant interaction.

Fig. 3.

Fig. 3.

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Ankle kinematics and EMG. Data are group means across the gait cycle in Old and Young for background (unperturbed; A–D) and reflex (perturbed minus unperturbed; E–H) angular displacement, angular velocity, MG EMG, and TA EMG. EMG values are represented as the average cumulative reflex EMG 50–125 ms (ACRE125) and are normalized to peak background muscle activation throughout the gait cycle for each subject. †P < 0.05, significant main effect for age. #P < 0.05, significant interaction. *P < 0.05, subsequent significant difference between groups at the indicated bin (post hoc Fisher’s LSD of significant interactions). DF, dorsiflexion; PF, plantarflexion.

In TA, there was a significant main effect for age [F(1,22) = 6.5, P = 0.02] and interaction [F(15,330) = 2.8, P = 0.0004; see Fig. 3H]. The Old had a significantly lower EMG reflex amplitude in TA compared with the Young in stance (bin 2), stance-swing transition (bins 9 and 10), mid-swing (bins 12 and 13), and terminal swing (bin 16). In MG, there was a significant interaction [F(15,330) = 2.9, P = 0.0003], with the Old showing an inhibition at mid-swing (bins 12 and 13), whereas the Young had an excitation reflex (see Fig. 3G). In stance (bin 7), both cohorts demonstrated an inhibitory reflex; however, there was a smaller amplitude inhibition in the Old. Representative single-subject reflex data for ankle angular displacement as well as EMG for MG and TA for mid-swing (bin 12) are displayed in Fig. 2, F, G, and H, respectively.

Knee kinematic and EMG reflexes.

Group means for knee kinematic and EMG reflexes are shown in Fig. 4, E–H. There was no main effect for age for knee displacement or angular velocity reflexes, nor was there a significant interaction for knee angular velocity reflex; however, there was a significant interaction in knee displacement reflex [F(15,330) = 1.8, P = 0.03; see Fig. 4E]. The Old had a significantly reduced knee flexion reflex compared with the Young in mid-swing (bin 13) by 4.26° and at heel strike (bin 1) by 3.41°. There was no significant main effect for age or interaction between groups in the EMG reflexes in VL and BF. Representative single subject reflex data for knee angular displacement as well as EMG for BF and VL for mid-swing (bin 13) are displayed in Fig. 5, D, E, and F, respectively.

Fig. 4.

Fig. 4.

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Knee kinematics and EMG. Data are group means across the gait cycle in Old and Young for background (unperturbed; A–D) and reflex (perturbed minus unperturbed; E–H) angular displacement, angular velocity, BF EMG, and VL EMG. EMG values are represented as the average cumulative reflex EMG 50–125ms (ACRE125) and are normalized to peak background muscle activation throughout the gait cycle for each subject. #P < 0.05, significant interaction. *P < 0.05, subsequent significant difference between groups at the indicated bin (post hoc Fisher’s LSD of significant interactions). Flex, flexion; Ext, extension.

Fig. 5.

Fig. 5.

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Single-participant mid-swing knee traces. Background (A–C) and reflex traces (D–F) are shown for bin 13 in an Old and Young participant for knee angular displacement (A, D); BF EMG (B, E), and VL EMG (C, F).

Background Walking Pattern

Background toe clearance.

Group means for toe height during unperturbed walking are shown in Fig. 1B. There was a significant interaction [F(15,330) = 2.1, P = 0.01]. During swing (bins 11, 12, 14, and 16), the toe was significantly closer to the ground in the Old compared with the Young. For differences in toe clearance between cohorts, see Table 1. Representative single-subject data for background toe clearance for bin 12 are displayed in Fig. 2A.

Background ankle kinematics and EMG.

Group means for joint angular displacement and angular velocities for the ankle during unperturbed walking are shown in Fig. 3, A–D. For ankle angular displacement, there was a significant main effect for age [F(1,22) = 11.6, P = 0.003] as well as significant bin × age interaction [F(15,330) = 4.24, P < 0.0001]. The Old had greater dorsiflexion at the stance-swing transition at bin 10. The Old also had reduced plantarflexion in swing at bins 11–16 compared with the Young. Therefore, the Old held the ankle in more dorsiflexion throughout swing. For ankle angular velocity, there was a significant bin × age interaction [F(15,330) = 3.03, P < 0.0001]. The Old had reduced plantarflexion velocity at bins 10 and 11 and reduced dorsiflexion velocity at bins 12 and 13 compared with the Young.

The pattern of muscle activity in the lower limb during unperturbed walking trials was similar for the two groups. There were no significant differences across muscles acting at the ankle except in MG, which showed a significant main effect for age [F(1,22) = 8.5, P = 0.008], indicating a greater level of overall activity in the Old compared with the Young (Fig. 3C). Representative single-subject data for background ankle angular displacement as well as MG and TA activity for mid-swing (bin 12) are displayed in Fig. 2, F, G, and H, respectively.

Background knee kinematics and EMG.

Group means for joint angular displacement and velocities as well as EMG at the knee during unperturbed walking are shown in Fig. 4, A–D. For knee angular displacement, there was a significant bin × age interaction [F(15,330) = 3.1, P < 0.0001]. In the Old, the knee was less extended at bins 1, 15, and 16 compared with the Young. For knee angular velocity, there was a significant bin × age interaction [F(15,330) = 2.8, P = 0.0005], and the Old had reduced knee extension velocity at mid-to-late swing (bins 14 and 15) and at heel strike (bin 1) compared with the Young. In BF, there was a significant bin × age interaction [F(15,330) = 2.9, P = 0.0002] with higher activation levels in the Old than in the Young during stance Bins 3 and 4 and again leading into heel strike at bin 16. There was no difference in VL activity between the cohorts. Representative single-subject data for background knee angular displacement as well as BF and VL activity for mid-swing (bin 13) are displayed in Fig. 5, A, B, and C, respectively.

Toe Clearance During Walking with Perturbations

Group means for toe clearance throughout gait cycle during walking with perturbations are shown in Fig. 1C. These toe clearance values reflect the sum of the differences between the Old and Young cohorts for background and reflex toe clearance. A main effect for age between the cohorts [F(1,22) = 7.28, P = 0.013] as well as a significant interaction [F(15,330) = 3.0, P = 0.0001] was found for toe clearance during walking with perturbations. In the Old, toe heights were significantly closer to the ground during mid-swing with differences of 16.7 mm at bin 11 and 19.1 mm at bin 12 (see Table 1). Toe clearance was also reduced in the Old at transition from stance to swing phase (bin 9) with a difference of 9.9 mm and from swing to stance phase (bin 16) with differences of 11.5 mm. At bin 15, the Old were further from the ground by 9.2 mm.

DISCUSSION

This is the first study to compare and contrast kinematic and EMG reflexes evoked with nonnoxious, electrical stimulation to the sole of the foot during walking between healthy young and older adults. Furthermore, this is the first study to explicitly measure toe clearance reflexes following stimulation to the sole of the foot. The main finding of this work was that older adults without a fall history demonstrated an erosion of the characteristic obstacle avoidance reflexes seen in young adults. This erosion was evident in the reduction in reflex amplitudes in toe clearance, ankle and knee joint displacement and ankle velocity, and ankle muscle activity in the Old compared with the Young cohorts. A sign reversal in the toe clearance reflex was also present. These degraded reflexes were superimposed on altered kinematics observed during background (unperturbed) walking in the Old compared with the Young. This combination of degraded reflexes and altered background kinematics resulted in significantly reduced toe clearance in the Old cohort and could reflect the normal aging process or suggest that these older adults are in the prodromal stage of fall risk. These age-related changes, seen primarily during swing and gait transition phases, have functional ramifications to fall risk as discussed below. Swing phases are defined in this study as bins 11–15 with stance-to-swing and swing-to-stance transition phases defined as bins 9 and 10 and bins 16 and 1, respectively.

Swing Phase: Reflex and Background

Encountering an object or the ground with the foot during swing phase can be destabilizing to dynamic postural control during gait and may result in falls (Berg et al. 1997). Therefore, reduced toe clearance and the resultant increased potential impact of the swing leg with obstacles or the ground could contribute to increased fall risk (Lai et al. 2012). Such mechanical perturbations have potential to activate both muscle and cutaneous afferents. Responses to distal tibial nerve stimulation are typically considered cutaneous reflexes (Zehr and Stein 1999); however, this is a mixed nerve containing both muscle and cutaneous afferents. It should be noted that obstacle avoidance reflex characteristics are known to be similar between mechanical and electrical perturbations (Zehr and Stein 1999). In the present study, there was significantly reduced amplitude in toe clearance reflex in response to stimulation in the Old during swing (bins 11 and 12; Fig. 1A). This reduced reflex amplitude was superimposed on the significantly decreased toe clearance also observed in the Old during swing (bins 11 and 12; Fig. 1B) in unperturbed walking, which together increased the difference in toe clearance between the Young and Old to nearly 2 cm. Despite the Old cohort in the current study having no 12-mo history of falls, the additive effect of altered reflexes and reduced background toe clearance increased the risk of tripping in these healthy older adults compared with the Young. The current toe clearance findings are corroborated by the findings of Santhiranayagam et al. (2015), where a similar toe clearance trajectory over the gait cycle during unperturbed walking on a treadmill was found. Specifically, immediately following toe off, there was a steep incline to maximum toe clearance (Santhiranayagam et al. 2015). Furthermore, they also found age-related differences in toe clearance responses to an attentional task during walking.

The reduced toe clearance in the Old compared with the Young in both background (unperturbed) and perturbed walking could result from a combination of altered kinematics throughout the kinematic chain in the lower body bilaterally. Although this study recorded from ipsilateral knee and ankle joints, we acknowledge that toe clearance could be affected by altered reflexes at the ipsilateral hip joint as well as the contralateral limb. In the present study, significantly reduced dorsiflexion ankle displacement reflex seen in the Old during mid-swing (bins 12 and 13; Fig. 3E) compared with the Young contributes to the lower toe clearance reflex (bins 12 and 13; Fig. 1A) observed in the Old. This decreased ankle dorsiflexion displacement reflex amplitude could be due to the decrease in motor units within aged muscle (Deschenes 2004; Lexell et al. 1983; Vaillancourt et al. 2003) or increased joint stiffness in passive joint structures limiting the kinematic expression of a reflex (Vandervoort et al. 1992) or altered EMG reflexes. Another possible reason for the decrease amplitude of the dorsiflexion reflex in the Old cohort is that during unperturbed walking, the ankle in the Old sits in a more dorsiflexed position during swing (bins 10–16; Fig. 3A) relative to the Young, which could limit the expression of the dorsiflexion reflex as they are closer to end-range dorsiflexion.

It is interesting that in the Old cohort during mid-swing of unperturbed walking, the toe was closer to the ground despite the Old adults holding their ankle joint in increased dorsiflexion (i.e., less plantarflexion) throughout swing phase. This suggests that during unperturbed walking, there is involvement of joints other than the ipsilateral ankle contributing to the reduced toe clearance. Moreover, during unperturbed walking, the Old had reduced ankle dorsiflexion velocity during mid-swing, which could have contributed to the decreased dorsiflexion displacement reflex due to decreased ongoing foot angular momentum.

Age-related differences in ankle kinematics during unperturbed walking cannot be explained by background EMG recorded in this study because no related differences in background EMG between the cohorts was found. However, previous findings of an age-related relative decrease in plantarflexion over dorsiflexion force (Christ et al. 1992) as well as a relative decrease in plantarflexion force at push off (Winter et al. 1990) could contribute to the increased dorsiflexion in the Old seen in this study. Furthermore, there is the potential for contribution of other muscles, such as soleus, which have not been recorded. The excitatory reflex in TA seen in the current study in the Young during mid-swing (bins 12 and 13; Fig. 3H) is significantly reduced in the Old. This finding supports the decreased amplitude in the dorsiflexion displacement reflex observed in the Old during mid-swing (bin 12; Fig. 3E). Furthermore, the excitatory reflex seen in MG in the Young during mid-swing (bins 12 and 13; Fig. 3G) was absent in the Old. The excitatory reflex seen in the young in both MG and TA would result in a coactivation of muscles acting at the ankle joint, as seen by Zehr et al. (1997). This coactivation reflex is thought to stabilize the ankle as the limb passes the obstacle (Zehr et al. 1997) and is missing in the Old.

Similarly to Zehr et al. (1997), we found that in the Young, stimulation to the sole of the foot evoked a significant knee flexion displacement reflex during mid-swing. Our comparisons between the Young and Old cohorts show that the contributions of knee flexion reflex to the obstacle avoidance strategy were impaired in the Old, as evidenced by the significantly reduced knee flexion reflex amplitude at mid-swing (bin 13; Fig. 4E), compared with the Young. The present results are similar to the reduced but nonsignificant knee flexion displacement reflex observed in older adults when a mechanical perturbation was applied to the foot during swing (Schillings et al. 2005). The lack of a significant flexion reflex seen by Shillings and colleagues (Schillings et al. 2005) may be related to the smaller relative proportion of the cutaneous field stimulated and the lower phase resolution of the gait cycle for analysis (Domingo et al. 2014), as well as the limited sensitivity of the kinematic measurement tool employed. The reported accuracy for electrogoniometers is ±2° (Biometrics 2015), whereas the accuracy for three-dimensional motion capture similar to that employed in the present study is <0.5° (Schmitz et al. 2014). This difference in accuracy is critical when dealing with differences in angles between cohorts of 1–2°.

The obstacle avoidance reflexes in the Young as well as the erosion of these reflexes in the Old were specifically sculpted based on the anatomical location of the stimulus. Stimulation to the sole of the foot evoked knee flexion and ankle dorsiflexion in the Young in mid-swing, whereas stimulation to the top of the foot evoked an obstacle avoidance reflex comprising plantarflexion and knee flexion in mid-swing (Zehr et al. 1997). In another study, we found a reduction in amplitude in these mid-swing reflexes at both the ankle and knee in the older adults compared with the young, contributing to decreased toe clearance seen throughout swing (Hundza et al. 2015).

Stance-to-Swing Transition: Reflex and Background

During terminal stance (bin 9; Fig. 1A), there was a reflex reversal in toe clearance between the age groups. The reflex in the Old brought the toe closer to the ground by 4.3 mm, whereas in the Young, the reflex moved the toe upward, away from the ground/stimulus, by 4.9 mm. Concurrently, the Young and Old were at the peak of the ankle dorsiflexion reflex, although this dorsiflexion was significantly less in amplitude for the Old compared with the Young. This ankle reflex supports the toe movement away from the ground in the Young. The movement of the toe closer to the ground in the Old can potentially be explained by the Old having a dorsiflexion reflex that promotes weighting on the stimulated limb where the tibia moves forward over the planted foot, whereas in the Young, the dorsiflexion reflex could contribute to toe elevation as the lower limb continues to progress forward into earlier toe-off. Another explanation is that perhaps the Old invert their ankle in terminal stance. Because the toe marker is placed on the head of the fifth metatarsal, ankle inversion could cause the fifth toe to move closer to the ground in the Old.

During unperturbed stepping, the Old demonstrated greater dorsiflexion (or reduced plantarflexion) at the stance-to-swing transition (bins 9 and 10; Fig. 3A) and at initial swing than the Young. Our results of reduced plantarflexion at stance-to-swing transition in the Old corroborate findings from earlier studies (Arnold et al. 2014; Begg and Sparrow 2006; Hundza et al. 2015).This reduced plantarflexion through swing (bins 11–13; Fig. 3A) is likely related to age-related strength and power loss in plantar flexors resulting in reduced push-off force at stance-to-swing transition in the Old, as noted in previous work (Christ et al. 1992; Judge et al. 1996; Winter et al. 1990). Of note, this reduced plantarflexion at stance-to-swing transition in the Old was not supported by muscle activity recorded in this study; there was significantly higher overall activity in MG in the Old as reflected by a main effect for age.

Swing-to-Stance Transition: Reflex and Background

During late swing and swing-to-stance transition in unperturbed stepping, knee kinematics show significantly reduced knee extension angular displacement (bins 15, 16, and 1; Fig. 4A) and slower angular velocity (bins 14, 15, and 1; Fig. 4B) in the Old. This is similar to the findings of Begg and Sparrow (2006), who showed that older adults favored a flexed-knee gait during weight acceptance. This limited knee extension can be attributed to physiological strength loss in quadriceps with age (Young et al. 1984) or osteoarthritis-related quadriceps weakness (Omori et al. 2013). Reduced BF activity in terminal swing (bin 16; Fig. 4C) in unperturbed walking in the old suggests a reduction in co-contraction at terminal swing in preparation for heel strike. Furthermore, there was higher overall activity in MG, as seen during stance, perhaps contributing to a “tentative” gait often seen in older adults, characterized by knee flexion in stance phase and decreased excursion at the ankle joint in swing (Nigg and Skleryk 1988).

Potential anthropometric and strength differences between the cohorts would affect their ability to respond to a perturbation. It was important that nonnormalized kinematic responses be examined to reflect the ability of each cohort to respond to the perturbation in an absolute context. For example, clearing an object involves the same toe clearance regardless of anthropometric or strength differences.

Clinical Implications

The significantly reduced kinematic and EMG reflexes to tibial nerve stimulation in the Old cohort that are seen primarily during swing and gait transition phases suggest that their functional capacity to respond to perturbations during walking may be eroded; however, this erosion is subclinical given that these older adults have no history of falls. Furthermore, during gait, these reduced reflexes are superimposed on altered kinematics seen during unperturbed walking in the Old compared with the Young. Together, these changes in neural control, which ostensibly can be ascribed to the normal aging process, potentially place these older adults in the prodromal phase for fall risk. Given the exploratory nature of the current research, the notably liberal LSD post hoc analysis was employed; more conservative statistical approaches may be warranted in replication studies. Further research is required to assess the impact of environmental influences, such as physical activity history, to tease out the normal vs. pathological nature of these observed age-related changes in neural control. Although the current study does not isolate the locus of impairment in the nervous system, previous research has found reduced sensitivity of sensory receptors of the foot (Maki et al. 1999; Perry 2006), reduced amplitudes in stretch reflexes (Burke and Kamen 1996), and longer latencies in electrical and mechanical reflexes in older adults (Bernard and Seidler 2012; Schillings et al. 2005). Thus this study of the integrity of obstacle avoidance reflexes adds to a basic understanding of age-related changes in neuromechanical control of gait and has potential application for the evaluation of fall prevention rehabilitation interventions (Maki et al. 1999).

GRANTS

This work was financially supported by Natural Science and Engineering Research Council of Canada.

DISCLOSURES

No conflicts of interest, financial or otherwise, are declared by the authors.

AUTHOR CONTRIBUTIONS

S.R.H. and M.D.K. conceived and designed research; A.G., R.B., D.C., and M.D.K. performed experiments; S.R.H., A.G., R.B., D.C., and M.D.K. analyzed data; A.G., D.C., and M.D.K. interpreted results of experiments; D.C. prepared figures; S.R.H. and A.G. drafted manuscript; S.R.H., D.C., and M.D.K. edited and revised manuscript; S.R.H., A.G., R.B., D.C., and M.D.K. approved final version of manuscript.

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