Nonlinear Modulation of Cutaneous Reflexes with Increasing Speed of Locomotion in Spinal Cats.

Cutaneous reflexes are important for responding rapidly to perturbations, correcting limb trajectory, and strengthening support. During locomotion, they are modulated by phase to generate functionally appropriate responses. The goal of the present study was to determine whether cutaneous reflexes and their phase-dependent modulation are altered with increasing speed and if this is accomplished at the spinal level. Four adult cats that recovered stable hindlimb locomotion after spinal transection were implanted with electrodes to record hindlimb muscle activity chronically and to stimulate the superficial peroneal nerve electrically to evoke cutaneous reflexes. The speed-dependent modulation of cutaneous reflexes was assessed by evoking and characterizing ipsilateral and contralateral responses in semitendinosus, vastus lateralis, and lateral gastrocnemius muscles at four treadmill speeds: 0.2, 0.4, 0.6, and 0.8 m/s. The amplitudes of ipsilateral and contralateral responses were largest at intermediate speeds of 0.4 and 0.6 m/s, followed by the slowest and fastest speeds of 0.2 and 0.8 m/s, respectively. The phase-dependent modulation of reflexes was maintained across speeds, with ipsilateral and contralateral responses peaking during the stance-to-swing transition and swing phase of the ipsilateral limb or midstance of the contralateral limb. Reflex modulation across speeds also correlated with the spatial symmetry of the locomotor pattern, but not with temporal symmetry. That the cutaneous reflex amplitude in all muscles was similarly modulated with increasing speed independently of the background level of muscle activity is consistent with a generalized premotoneuronal spinal control mechanism that could help to stabilize the locomotor pattern when changing speed.SIGNIFICANCE STATEMENT When walking, receptors located in the skin respond to mechanical pressure and send signals to the CNS to correct the trajectory of the limb and to reinforce weight support. These signals produce different responses, or reflexes, if they occur when the foot is contacting the ground or in the air. This is known as phase-dependent modulation of reflexes. However, when walking at faster speeds, we do not know if and how these reflexes are changed. In the present study, we show that reflexes from the skin are modulated with speed and that this is controlled at the level of the spinal cord. This modulation could be important in preventing sensory signals from destabilizing the walking pattern.

Lack of adaptation during prolonged split-belt locomotion in the intact and spinal cat.

KEY POINTS: During split-belt locomotion in humans where one leg steps faster than the other, the symmetry of step lengths and double support periods of the slow and fast legs is gradually restored. When returning to tied-belt locomotion, there is an after-effect, with a reversal in the asymmetry observed in the early split-belt period, indicating that the new pattern was stored within the central nervous system. In this study, we investigated if intact and spinal-transected cats show a similar pattern of adaptation to split-belt locomotion by measuring kinematic variables and electromyography before, during and after 10 min of split-belt locomotion. The results show that cats do not adapt to prolonged split-belt locomotion. Our results suggest an important physiological difference in how cats and humans respond to prolonged asymmetric locomotion. ABSTRACT: In humans, gait adapts to prolonged walking on a split-belt treadmill, where one leg steps faster than the other, by gradually restoring the symmetry of interlimb kinematic variables, such as double support periods and step lengths, and by reducing muscle activity (EMG, electromyography). The adaptation is also characterized by reversing the asymmetry of interlimb variables observed during the early split-belt period when returning to tied-belt locomotion, termed an after-effect. To determine if cats adapt to prolonged split-belt locomotion and to assess if spinal locomotor circuits participate in the adaptation, we measured interlimb variables and EMG in intact and spinal-transected cats before, during and after 10 min of split-belt locomotion. In spinal cats, only the hindlimbs performed stepping with the forelimbs stationary. In intact and spinal cats, step lengths and double support periods were, on average, symmetric, during tied-belt locomotion. They became asymmetric during split-belt locomotion and remained asymmetric throughout the split-belt period. Upon returning to tied-belt locomotion, symmetry was immediately restored. In intact cats, the mean EMG amplitude of hindlimb extensors increased during split-belt locomotion and remained increased throughout the split-belt period, whereas in spinal cats, EMG amplitude did not change. Therefore, the results indicate that the locomotor pattern of cats does not adapt to prolonged split-belt locomotion, suggesting an important physiological difference in the control of locomotion between cats and humans. We propose that restoring left-right symmetry is not required to maintain balance during prolonged asymmetric locomotion in the cat, a quadruped, as opposed to human bipedal locomotion.

Split-belt walking alters the relationship between locomotor phases and cycle duration across speeds in intact and chronic spinalized adult cats.

During overground or treadmill walking, the stance phase and cycle durations are reduced as speed increases, whereas swing phase duration remains relatively invariant. When the speed of the left and right sides is unequal, as is the case during split-belt locomotion or when walking along a circular path, adjustments in stance and swing phases are observed, which could alter the phase/cycle duration relationships. Here, we tested this hypothesis in the left and right hindlimbs of four intact and two chronic spinal-transected adult cats during tied-belt (i.e., equal left and right speeds) and split-belt (i.e., unequal left and right speeds) walking. During split-belt walking, one side (i.e., constant limb) walked at a constant speed while the other side (varying limb) varied its speed from 0.3 to 1.0 m/s. We show that the phase/cycle duration relationships differed in both hindlimbs concurrently during split-belt walking. Specifically, the slope of the phase/cycle duration relationships for the stance/extension phase increased in the varying limb from tied-belt to split-belt walking, whereas that of the swing/flexion phase decreased. In contrast, in the constant limb, the slope of the phase/cycle duration relationships for the stance/extension phase decreased, whereas that of the swing/flexion phase increased. The results were qualitatively similar in intact and spinal-transected cats, indicating that the modulation was mediated within the spinal cord. In conclusion, we propose that neuronal networks within the spinal cord that control left and right hindlimb locomotion can differentially and simultaneously modulate phase variations when the two sides walk at different speeds.

Speed-dependent modulation of phase variations on a step-by-step basis and its impact on the consistency of interlimb coordination during quadrupedal locomotion in intact adult cats.

It is well established that stance duration changes more than swing duration for a given change in cycle duration. Small variations in cycle duration are also observed at any given speed on a step-by-step basis. To evaluate the step-by-step effect of speed on phase variations, we measured the slopes of the linear regressions between the phases (i.e., stance, swing) and cycle duration during individual episodes at different treadmill speeds in five adult cats. We also determined the pattern of dominance, defined as the phase that varies most with cycle duration. We found a significant effect of speed on hindlimb phase variations, with significant differences observed between the slowest speed of 0.3 m/s compared with faster speeds. Moreover, although patterns of phase dominance were primarily stance/extensor dominated at the slowest speeds, as speed increased the patterns were increasingly categorized as covarying, whereby both stance/extensor and swing/flexor phases changed in approximately equal proportion with cycle duration. Speed significantly affected the relative duration of support periods as well as interlimb phasing between homolateral and diagonal pairs of limbs but not between homologous pairs of limbs. Speed also significantly affected the consistency of interlimb coordination on a step-by-step basis, being less consistent at the slowest speed of 0.3 m/s compared with faster speeds. We found a strong linear relationship between hindlimb phase variations and the consistency of interlimb coordination. Therefore, results show that phase variations on a step-by-step basis are modulated by speed, which appears to influence the consistency of interlimb coordination.

Modulation of phase durations, phase variations, and temporal coordination of the four limbs during quadrupedal split-belt locomotion in intact adult cats.

Stepping along curvilinear paths produces speed differences between the inner and outer limb(s). This can be reproduced experimentally by independently controlling left and right speeds with split-belt locomotion. Here we provide additional details on the pattern of the four limbs during quadrupedal split-belt locomotion in intact cats. Six cats performed tied-belt locomotion (same speed bilaterally) and split-belt locomotion where one side (constant side) stepped at constant treadmill speed while the other side (varying side) stepped at several speeds. Cycle, stance, and swing durations changed in parallel in homolateral limbs with shorter and longer stance and swing durations on the fast side, respectively, compared with the slow side. Phase variations were quantified in all four limbs by measuring the slopes of the regressions between stance and cycle durations (rSTA) and between swing and cycle durations (rSW). For a given limb, rSTA and rSW were not significantly different from one another on the constant side whereas on the varying side rSTA increased relative to tied-belt locomotion while rSW became more negative. Phase variations were similar for homolateral limbs. Increasing left-right speed differences produced a large increase in homolateral double support on the slow side, while triple-support periods decreased. Increasing left-right speed differences altered homologous coupling, homolateral coupling on the fast side, and coupling between the fast hindlimb and slow forelimb. Results indicate that homolateral limbs share similar control strategies, only certain features of the interlimb pattern adjust, and spinal locomotor networks of the left and right sides are organized symmetrically.

Synchronous and asynchronous electrically evoked motor activities during wind-up stimulation are differentially modulated following an acute spinal transection.

In this study, we used a novel technique to study reflex wind-up when the spinal cord is intact and following an acute spinal transection. Specifically, we evaluated reflex responses evoked by a series of 10 electrical pulses to the tibial or superficial peroneal nerves in 9 decerebrate adult cats, before and after an acute spinal transection. Electromyograms were recorded in four hindlimb muscles (lateral gastrocnemius, tibialis anterior, semitendinosus, and sartorius) to evaluate reflex amplitude, duration, and the temporal summation of reflex responses, so-called wind-up. We identified two distinct reflex responses evoked by electrical stimulation of the tibial or superficial peroneal nerves on the basis of their pattern of change following acute spinal transection, a short-latency (∼10 ms) compound action potential (CAP) that was followed by a burst of sustained activity (SA). Wind-up of CAP and SA amplitudes was clearly present when the spinal cord was intact but was drastically reduced after acute spinalization in some muscles. Moreover, CAP and SA reflex responses were differentially modified by the acute spinalization. When the effects of acute spinal transection were significant, CAP responses were increased after acute spinalization, whereas SA responses were reduced, suggesting that the two signals are regulated by different neuronal mechanisms. The present results provide the first assessment of reflex wind-up before and after an acute spinal transection in the same animals and indicate that different reflex components must be considered separately when evaluating changes in neuronal excitability following SCI.

The division of visual attention affects the transition point from level walking to stair descent in healthy, active older adults.

BACKGROUND: Stair descent is a frequent daily activity that poses great risks for injury due to falling. Very little is understood about the attentional demands of stair descent and their changes with aging. The present study compared combined locomotor and cognitive functioning during different phases of stair descent between healthy young and older individuals. METHODS: Sixteen young and sixteen healthy older subjects walked down a 5-step staircase, performing a simultaneous visual Stroop task (i.e., a dual task) during the approach, transition or steady-state descent phases in some trials. Three dimensional kinematics of trunk and foot motion were recorded along with the accuracy and dual task costs (DTCs) for responses to the Stroop stimuli. RESULTS: Dual tasking influenced both gait and cognitive performance for all subjects, and older adults generally walked slower with higher foot clearances and had greater DTCs. Specific age differences were found at stair transition where older adults showed more attentional effects. CONCLUSIONS: Healthy, active older adults showed changes to attention and planning due to normal aging specifically associated with a crucial point of fall risk during stair descent.