Interlimb Timing Research Articles

Joint-level coordination patterns for split-belt walking across different speed ratios.

Locomotion is a highly flexible process, requiring rapid changes to gait due to changes in the environment or goals. Here, we used a split-belt treadmill to examine how the central nervous system coordinates a novel gait pattern. Existing research has focused on summary measures, most often step lengths, when describing changes induced while walking on the split-belt treadmill and during subsequent aftereffects. Here, we asked how the nervous system adjusts individual joint motions and the coordination pattern of the legs when people walk with one leg moving at either 2×, 3×, or 4× the speed of the other leg. We found that relative to tied-belt walking, split-belt perturbations change the timing relationships between the legs while most joint angle peaks and range of motion change little. The kinematic changes over the course of adaptation (i.e., from the beginning to end of a single split-belt walking bout) were subtle, particularly when comparing individual joint motions. The magnitude of the belt speed differences impacted intralimb coordination but did not produce consistent differences in most other measures. Most significant changes in kinematics occurred in the fast leg. Overall, interlimb timing changes drove a large proportion of the differences observed between tied-belt and split-belt gaits. Thus, it appears that the central nervous system can produce novel gait patterns through changes in coordination between legs that lead to new configurations at significant time points. These patterns can use within-limb and within-joint patterns that closely resemble those of normal walking.NEW & NOTEWORTHY We studied how the nervous system coordinates limb movements during asymmetric gait. Using a split-belt treadmill, we found that most changes in motion occurred when comparing motions between limbs, rather than among joints within a limb. Individual joint patterns resembled speed-matched comparisons, but this meant that joint movements became asymmetric during split-belt walking. These findings demonstrate that the nervous system can use consistent joint motions that are reconfigured in time to achieve new gait patterns.

Corticospinal drive is associated with temporal walking adaptation in both healthy young and older adults.

Healthy aging is associated with reduced corticospinal drive to leg muscles during walking. Older adults also exhibit slower or reduced gait adaptation compared to young adults. The objective of this study was to determine age-related changes in the contribution of corticospinal drive to ankle muscles during walking adaptation. Electromyography (EMG) from the tibialis anterior (TA), soleus (SOL), medial, and lateral gastrocnemius (MGAS, LGAS) were recorded from 20 healthy young adults and 19 healthy older adults while they adapted walking on a split-belt treadmill. We quantified EMG-EMG coherence in the beta-gamma (15-45 Hz) and alpha-band (8-15 Hz) frequencies. Young adults demonstrated higher coherence in both the beta-gamma band coherence and alpha band coherence, although effect sizes were greater in the beta-gamma frequency. The results showed that slow leg TA-TA coherence in the beta-gamma band was the strongest predictor of early adaptation in double support time. In contrast, early adaptation in step length symmetry was predicted by age group alone. These findings suggest an important role of corticospinal drive in adapting interlimb timing during walking in both young and older adults.

A TMS-induced cortical silent period delays the contralateral limb for bimanual symmetrical movements and the reaction time delay is reduced on startle trials.

Bimanual actions are typically initiated and executed in a temporally synchronous manner, likely due to planning bilateral commands as a single motor "program." Applying high-intensity transcranial magnetic stimulation (TMS) to the motor cortex can result in a contralateral cortical silent period that delays reaction time (RT), if timed to coincide with the final motor output stage. The current study examined the impact of a unilateral TMS silent period on the RT and interlimb timing of bilateral wrist extension. In addition, because a loud, startling acoustic stimulus (SAS) can result in the involuntary release of preprogrammed actions via increased reticulospinal activation, it was of interest whether startle-induced speeding of response initiation would moderate the impact of the TMS-induced RT delay. Participants performed blocks of unilateral and bilateral wrist extension in response to an acoustic (82 dB) go-signal. On selected trials, either TMS was applied to the left motor cortex 70 ms before the expected EMG response onset, a SAS (120 dB) replaced the go-signal, or both TMS and SAS were delivered. Results showed that TMS led to a significant RT delay in the right limb during both unimanual and bimanual extension but had no impact on the left limb initiation. In addition, the magnitude of the right limb RT delay was smaller when the response was triggered by a SAS. These results imply that preplanned bimanually synchronous movements are susceptible to lateralized dissociation late into the cortical motor output stage and movements triggered by startle involve increased reticulospinal output.NEW & NOTEWORTHY Bilateral responses are typically planned synchronously and performed symmetrically. Here, we show that delaying the initiation of one limb using transcranial magnetic stimulation (TMS) to produce a cortical silent period does not impact the other limb during bimanual movements. Also, the TMS-induced delay is reduced when a startling acoustic stimulus (SAS) triggers the movement. These results confirm that tightly coupled bilateral responses can be dissociated by contralateral TMS- and SAS-triggered responses involve greater reticulospinal output.

Spatial and Temporal Control Contribute to Step Length Asymmetry During Split-Belt Adaptation and Hemiparetic Gait

Background. Step length asymmetry (SLA) is a common hallmark of gait poststroke. Though conventionally viewed as a spatial deficit, SLA can result from differences in where the feet are placed relative to the body (step position strategy), the timing between foot strikes (step time strategy), or the velocity of the body relative to the feet (step velocity strategy). Objective. The goal of this study was to characterize the relative contributions of each of these strategies to SLA. Methods. We developed an analytical model that parses SLA into independent step position, step time, and step velocity contributions. This model was validated by reproducing SLA values for 25 healthy participants when their natural symmetric gait was perturbed on a split-belt treadmill moving at either a 2:1 or 3:1 belt-speed ratio. We then applied the validated model to quantify step position, step time, and step velocity contributions to SLA in 15 stroke survivors while walking at their self-selected speed. Results. SLA was predicted precisely by summing the derived contributions, regardless of the belt-speed ratio. Although the contributions to SLA varied considerably across our sample of stroke survivors, the step position contribution tended to oppose the other 2—possibly as an attempt to minimize overall SLA. Conclusions. Our results suggest that changes in where the feet are placed or changes in interlimb timing could be used as compensatory strategies to reduce overall SLA in stroke survivors. These results may allow clinicians and researchers to identify patient-specific gait abnormalities and personalize their therapeutic approaches accordingly.

Limb kinematics during locomotion in the two-toed sloth ( Choloepus didactylus, Xenarthra) and its implications for the evolution of the sloth locomotor apparatus

In order to gain insight into the function of the extant sloth locomotion and its evolution, we conducted a detailed videoradiographic analysis of two-toed sloth locomotion (Xenarthra: Choloepus didactylus). Both unrestrained as well as steady-state locomotion was analyzed. Spatio-temporal gait parameters, data on interlimb coordination, and limb kinematics are reported. Two-toed sloths displayed great variability in spatio-temporal gait parameters over the observed range of speeds. They increase speed by decreasing the durations of contact and swing phases, as well as by increasing step length. Gait utilization also varies with no strict gait sequence or interlimb timing evident in slow movements, but a tendency to employ diagonal sequence, diagonal couplet gaits in fast movements. In contrast, limb kinematics were highly conserved with respect to ‘normal’ pronograde locomotion. Limb element and joint angles at touch down and lift off, element and joint excursions, and contribution to body progression of individual elements are similar to those reported for non-cursorial mammals of small to medium size. Hands and feet are specialized to maintain firm connection to supports, and do not contribute to step length or progression. In so doing, the tarsometatarsus lost its role as an individual propulsive element during the evolution of suspensory locomotion. Conservative kinematic behavior of the remaining limb elements does not preclude that muscle recruitment and neuromuscular control for limb pro- and retraction are also conserved. The observed kinematic patterns of two-toed sloths improve our understanding of the convergent evolution of quadrupedal suspensory posture and locomotion in the two extant sloth lineages.

Response preparation changes during practice of an asynchronous bimanual movement

For synchronous bimanual movements, we have shown that a different amplitude can be prepared for each limb in advance and this preparation improves with practice (Maslovat et al. 2008). In the present study, we tested whether an asynchronous bimanual movement can also be prepared in advance and be improved with practice. Participants practiced (160 trials) a discrete bimanual movement in which the right arm led the left by 100 ms in response to an auditory "go" signal (either 80 dB control stimulus or 124 dB startle stimulus). The startle stimulus was used to gauge whether inter-limb timing could be pre-programed. During startle trials, the asynchronous bimanual movement was triggered at early latency suggesting the entire movement could be prepared in advance. However, the triggered movement had a shorter between-arm delay and a temporally compressed within-arm EMG pattern, results that we attribute to increased neural activation caused by the startling stimulus. However, as both startle and control trials improved over time, it does appear response preparation of interval timing can improve with practice.

Limb proportions and the ontogeny of quadrupedal walking in infant baboons (Papio cynocephalus)

AbstractMuch of the diversity in preferred walking gait (footfall sequence, interlimb timing) observed among mammals can be understood as a biomechanical response to variation in body shape, in conjunction with efforts to maintain stability. Primates, unlike most other mammals, exhibit a preference for diagonal sequence, diagonal couplets (DSDC) walking gait, but there remains no clear consensus on this gait's possible biomechanical or adaptive advantages. This study examines primate gait from an ontogenetic perspective, and tests the hypothesis that ontogenetic gait transitions are influenced by changes in body shape. Support for this hypothesis could provide insight on the biomechanics and evolution of DSDC gait preferences in adult primates. Data on limb proportions, footfall sequence and interlimb timing were collected at 2‐week intervals for four infant baboons (Papio cynocephalus) as they aged from 1 to 9 months. Despite some variation among individuals, DSDC walking was the most frequently used gait throughout the developmental period, but it was nearly always used in combination with lateral sequence walking. An important transition occurred at c. 5 months, when limb couplets used in lateral sequence walking shifted from diagonal to lateral, and the frequency of DSDC walking increased. The couplets shift within lateral sequence walking coincided with a relative increase in hind limb length, and was most likely attributable to the avoidance of ipsilateral limb interference. Limb proportions thus appear to have a functional influence on lateral sequence walking, but do not explain the consistent use of DSDC walking during the sampled developmental period.

The co-ordination of bimanual rapid aiming movements following stroke

To determine the role of anticipatory and movement control processes for the coordination of bimanual target aiming in individuals post stroke. Thirty adults with chronic stroke and 30 individuals without stroke history. A two-group (stroke, control) by two-aiming type (unimanual, bimanual) by two-limb (paretic, nonparetic; left, right for controls) design with repeated measures on the last two factors. Kinematic analyses of performance and psychometric measures of reaction time, movement time, peak resultant velocity, time to and after peak resultant velocity and interlimb timing for movement initiation and target impact. Compared with unimanual aiming, the nonparetic limb exhibited a prolonged movement time in the bimanual condition; the locus for prolongation was primarily in the deceleration phase. This adaptive response allowed for a nearly simultaneous (both limbs) target impact in 81% of trials. Compared with the unimanual condition, the nonparetic limb exhibited a lower peak velocity (10%) in the bimanual condition. Conversely, compared with the unimanual condition, the paretic limb exhibited a higher peak velocity (4%) in the bimanual condition. This disociation between limb and condition was observed for the stroke group but not the control group. The interlimb coordination that emerged for the stroke group revealed a complex and asymmetric contribution from each limb mediated through anticipatory and motor control processes. We suggest that this coordination may be harnessed for future bimanual intervention approaches to rehabilitation of upper limb function after stroke.

Lateral sequence walking in infant Papio cynocephalus: implications for the evolution of diagonal sequence walking in primates.

One of the most distinctive aspects of primate quadrupedal walking is the use of diagonal sequence footfalls in combination with diagonal-couplets interlimb timing. Numerous hypotheses have been offered to explain why primates might have evolved this type of gait, yet this important question remains unresolved. Because infant primates use a wider variety of quadrupedal gaits than do adults, they provide a natural experiment with which to test hypotheses about the evolution of unique aspects of primate quadrupedalism. In this study, we present kinematic data on two infant baboons (Papio cynocephalus) in order to test the recent hypothesis that diagonal sequence, diagonal couplets walking might have evolved in primates because their limb positioning provides stability in a small branch environment (Cartmill et al. [2002] Zool J Linn Soc 136:401-420). To assess hindlimb position at the moment of forelimb touchdown, we measured hindlimb angular excursion and ankle position for 84 walking strides, across three different types of gaits (diagonal sequence, diagonal couplets (DSDC); lateral sequence lateral couplets (LSLC); and lateral sequence diagonal couplets (LSDC)). Results indicate that if a forelimb were to contact an unstable substrate, LSLC walking provides as much, and perhaps more, stability when compared to DSDC walking. Therefore, it appears that this moment in a stride was unlikely to be a particularly important selective factor in the evolution of DSDC walking. Further insight into this issue will likely be gained by observations of primate quadrupedalism in natural environments, where the use of lateral sequence gaits might be more common than currently known.

Temporal stride patterns in horses with experimentally induced fore‐ or hindlimb lameness

SummaryIn a kinematic study of equine lameness, temporal stride variables were investigated for their significance as diagnostic indicators and as a means of compensation for lameness. Kinematics of 11 clinically sound Dutch Warmblood horses were recorded while walking (1.6 m/s) and trotting (3.5 m/s) on a treadmill. A transient lameness model, provoking pain on the hoof sole, was used to induce 3degreesof fore‐ and hindlimb lameness. Intra‐ and interlimb stride variables as well as left‐to‐right symmetry were analysed using a 2 way analysis of variance (significance level: P<0.05). At the walk, stride duration was not affected by fore‐ or hindlimb lameness, while intra‐ and interlimb timing showed minor changes. At the trot, the stride duration in forelimb lameness decreased by 3.1% and relative stance duration of all limbs became longer (5.3% in forelimbs, 1.5% and 3.2% in hindlimbs). The diagonal advanced placement of the forelimbs increased and the duration of the suspension phase following the lame diagonal decreased by 61%. Left‐to‐right symmetry decreased for the suspension phase and contralateral advanced placement, while the stance durations remained symmetrical. In hindlimb lameness the stride duration at the trot decreased by 3.7% and the stance duration of the sound hind limb increased by 2.7%. Diagonal advanced placement, suspension phase and symmetry variables remained unaffected. It was concluded that compensation for lameness by changing temporal stride patterns is more pronounced in fore than in hindlimb lameness. The maintenance of symmetry in most stride variables in mild lamenesses limits their value as lameness indicators.

The Development of Locomotor Coordination

Developmental sequence, relative timing, center of gravity, and phase-plane analyses were used to study a minimum of 15 years of longitudinal, filmed data on the development of hopping in 7 children. The developmental sequences revealed common, qualitative changes in the movement of the children, although each child progressed through the changes at his/her own rate. The timing analyses showed that, in the advanced hop, the tightest limb relationships were found within the hopping leg, then between contralateral limbs of the same girdle, and then between legs and arms. Relative-timing calculations revealed (a) intralimb, timing invariances that were present in first attempts to perform the skill at age 3 and remained for 15 years across all developmental levels; (b) emergent, interlimb timings that gradually became invariant; and (c) intra- and interlimb timing showing gradual development over the 15 years. One invariant, the time between landing and deepest knee flexion, is also invariant in the walk and the run (Shapiro, Zernicke, Gregor, & Diestel, 1981). Phase plane analyses indicated that the timing of peak and zero velocities may be the coordinative constant accounting for a relative timing invariance between the two legs. Position of the body's center of gravity may explain the invariant relative time between landing and deepest knee flexion, or the explanation could lie in the "equation of constraint" regulating joint equilibrium points. The data suggest that modeling the developing hop as the evolving interaction of four vibratory systems would be promising.

Proprioceptive feedback as a mediator in interlimb timing.

Prior findings regarded as evidence for proprioceptive feedback as a mediator in interlimb timing can also be interpreted as evidence for motor outflow because they came from research that had subjects make voluntary movements, and such movements allow for both feedback and outflow to operate. The present study was designed to resolve this controversy by determining if these findings could be replicated with passive movements which allow for feedback, but not outflow, to operate. The interlimb timing task studied was one where subjects made the timing response with their right hand while moving their left arm during the 1.5-sec interval to be timed. Three groups of 16 male college students performed 50 trials of the right-hand response with knowledge of results, under one of three left-arm conditions: (a) passive movement, (b) voluntary movement, and (c) no movement. The results indicated that the findings were replicated with passive movements and this was interpreted as support for the involvement of proprioceptive feedback in interlimb timing.

Kinematics of treadmill galloping by cats: II. Steady-state coordination under positive reinforcement control

This report, the second of three, describes treadmill galloping by cats that were trained solely by food reward. Four young adult animals provided data at various velocities from 2.3 to 4.1 m/sec. Another cat galloped at 2.0 m/sec. The overall speed range was lower than in the first study, probably because the animals were not punished for failure to run and, also, because they were slightly smaller and younger cats. At any one velocity, several successive strides were available whose footfall pattern was steady state, or invariant. The same three galloping patterns were seen that had been found previously in an aversive test situation: rotatory galloping, transverse galloping, and the half bound. The rotatory gallop was most frequently used. In general, the findings for movements of a single limb, and also the interlimb timings (with some exceptions during slow transverse galloping), were similar to those seen in the first study, as were such overall measures as stride length and the percentage of zero support. For one cat that provided a substantial number of test runs at increments between 3.1 and 4.1 m/sec, it was possible to show a linear trend of stride duration as a function of velocity, although the total change was only approximately 30 msec. The low-speed transverse gallop was of special interest, because its footfall patterns showed that a continuum of interlimb coordination could occur from trotting to this type of gallop. It was concluded that the overall similarities of food-reinforced galloping and galloping under aversive control far outweighed the differences, to imply economy of their neural control.

Kinematics of treadmill galloping by cats: III. Coordination during gait conversions and implications for neural control

Two previous reports described steady-state galloping by cats, in which the footfall pattern was invariant for a number of successive strides at one velocity. There were three such patterns: rotatory galloping, transverse galloping, and the half bound. This final report concerns mixed galloping on a treadmill, in which the cat converted from one to another of the three gallops from one stride to the next. Cinematographic measurements were taken of conversions that occurred at speeds from 2.0 to 4.6 m/sec. The conversions were in almost every instance flawless, so that each individual stride (a cycle of movement by the four limbs) was readily distinguished as a typical rotatory or transverse gallop or a half bound. Placement order of the two hindlimbs, or the two forelimbs, or both, shifted. Conversions were accomplished by an average increase of 50–100 msec, or decrease of 50 msec, from the usual 200-msec-long swing (up) duration, since stance (down) durations were unchanged. The normal swing, then, is under more flexible neural control than has previously been believed possible. From an examination of a number of interlimb timings, it was concluded that in every expression of galloping by cats on a treadmill a complete stride is demarcated by successive descents of the trailing (rear) hindlimb. This four-limb ensemble is subdivided into paired movements of the hindlimbs and also the forelimbs, each pair also being marked initially by descent of the trailing limb. Selection of left or right limbs as trailing or leading (front) may be arbitrary, may prevent fatigue in individual limbs, or could offset roll at high speeds.

Kinematics of locomotion by cats with a single hindlimb deafferented.

1. Cinematographic measurements were made of stepping by cats on a motor-driven treadmill, both normally and 2-3 wk after deafferentation of the LH (left hind) limb. 2. After surgery, rhythmic cycling of the LH limb was blurred whether the leg was dragged, as by some cats, or if it was lifted from the surface, as by others. 3. Interlimb coordination was also blurred with respect to normal, although distinct rhythms were still seen. The RH (right hind) limb descended prematurely and, in the walk, had a prolonged stance phase. The interval between touchdowns of hind- and forelimb on the left side no longer equaled that interval on the right side. 4. As is true for a normal cat, if the LH-deafferented animal stumbled, relatively normal single and interlimb cyclings were regained after several strides. 5. By kinematic analysis, force deficits were found in the deafferented LH limb both during the stance, when extensors should be most active, and the swing, when the limb failed to attain a normal position above the surface of the belt. Weight bearing by the LF (left fore) limb was altered in some animals. 6. At high speed, mean LH stance duration failed to decrease in the normal fashion. Inter-limb timings were reset to greater extent than in low-speed walking, as if the LH limb was being used only minimally. 7. It was concluded that both rhythm and force were impaired in the deafferented limb and also in the three intact limbs, whose weight bearing had to compensate for LH weakness. The changed mechanical demands after surgery were probably met by interactions between the remaining afferent input and central pattern generators so as to secure fairly effective and expedient locomotion.

Reinforcement influences upon topography of treadmill locomotion by cats

Cats were trained to walk and trot on a treadmill for different reinforcers: food alone, food plus avoidance of an air jet, or food plus shock avoidance. Cinematographic measurements of ankle angles differed significantly across treatments at liftoff and at touchdown. Angles were widest for the food group and most closely approximated those seen previously in normal overground stepping. An interlimb timing between ipsilateral hindlimb and forelimb touchdowns did not differ significantly in trotting, but during walking the footfalls in the food-shock group were most normal and widely spaced. Swing-stance durations (the limb is off and then on the belt) were relatively invariant across treatments during walking, but not trotting. The observed mutability of stepping topography was concluded to be due in part to reinforcement type and in part to segmental afferentation, as these various inputs are integrated with central stepping commands.