Interlimb coordination during fictive locomotion in the thalamic cat

Summary Efferent discharges in muscle nerves of the four limbs were recorded simultaneously during spontaneous fictive locomotion in thalamic cats with the goal of understanding how the central nervous system controls interlimb coordination during stepping. The onset of the bursts of activity in the nerve of a selected flexor muscle in each limb allowed the temporal and the phase relationships between the fictive step cycle of a pair of limbs to be determined. Our main results are the following: 1) the fictive step cycles of the two forelimbs are always strictly alternated whereas the phasing of the step cycles of either the two hindlimbs or pairs of homolateral or diagonal limbs is more variable; 2) the time interval between the onsets of the flexor bursts of one of the two pairs of diagonal limbs is independent of the step cycle duration; 3) distinct patterns of interlimb coordination exist during fictive locomotion; a small number of patterns of coordination involving all four limbs, which correspond to the walking and the trotting gaits in the intact cat, occur very frequently. The results demonstrate that the central nervous system deprived of phasic afferent inputs from the periphery has the capacity to generate most of the patterns of interlimb coordination which occur during real locomotion. They further support the view that the central pattern of interlimb coordination essentially results from diagonal interactions between a forelimb generator for locomotion and a hindlimb one.Abbreviations CD step cycle duration - LF left forelimb - LH left hindlimb - m slope of correlation curve - N number of step cycles - r correlation coefficient - RF right forelimb - RH right hindlimb - Ti time interval     

Interlimb coordination in cat locomotion investigated with perturbation

Summary During locomotion of decerebrate and awake walking cats, perturbation (mechanical tap) was applied to the paw dorsum of the left forelimb (LF), and the responses of both forelimbs were recorded cinematographically and electromyographically (EMG). When the tap was applied during the LF stance phase, the duration of the ongoing LF stance was shortened by 10%; in the right forelimb (RF), the duration of the concomitant swing was shortened by 32%. A tap during the LF swing phase prolonged the duration of the ongoing LF swing phase and the concomitant RF stance phase by 55 and 15%, respectively. Analysis of RF joint angle excursions showed that the shortening of the RF swing phase was related mainly to acceleration of extension movement in the late swing phase; the prolongation of the RF stance phase was related to prolonged extension movement in the late stance phase. While EMG activities were relevant to these limb movements, a notable observation was that, by tapping the LF during the LF stance phase, EMG activity in the RF extensor started well before onset of the elbow extension movement to place down the limb; without the tap, the extensor activity started shortly after onset of the extension. Closely related to changes in phase durations of each forelimb, the period of bisupport phase where both forelimbs were in stance, was retained for more than 40% of that of unperturbed steps, even when the RF or LF made the first touchdown after the tap. The rostrocaudal level at RF touchdown after the tap was comparable to unperturbed steps. These findings on interlimb relation suggest that neural control ensures coordinated movements between symmetric limbs during locomotion.Supported by grant no. 557033 from the Japanese Ministry of Education, Science, and Culture     

The locomotion of the low spinal cat. II. Interlimb coordination

The interaction of the two hindlimbs were investigated by an analysis of the muscular activity and the movements in 14 chronic spinal kittens during treadmill locomotion (i.e. in kittens subjected to a transection of the spinal cord (Th_10–12) one or two weeks after birth). At low speed the limbs were alternating (walk or trot). At higher they were activated more simultaneous, as during gallop. The two limbs could walk at different velocities, as during walking in a circle, when the two belts of the treadmill were driven at different speeds. The duration of the support phases was mainly influenced by the speed of the belt on which the limb was walking. The limbs could still maintain a common rhythm up to a two or three fold speed difference, as the flexion or the first extension phase of the limb walking on the “fast” belt was prolonged and the flexion phase of the “slow limb” was shortened. At extreme speed differences the limb on the “fast belt” performed 2, 3 and even 4 steps during one stepcycle of the “slow limb”. The placement of the feet was found to maintain the most stable relationship during alternating gaits at different speed differences. It is concluded that all phases of the step cycle are modifiable and that there are several mechanisms coordinating the limbs within the spinal cord.     

Stumbling corrective reaction during fictive locomotion in the cat

An obstacle contacting the dorsal surface of a cat's hind foot during the swing phase of locomotion evokes a reflex (the stumbling corrective reaction) that lifts the foot and extends the ankle to avoid falling. We show that the same sequence of ipsilateral hindlimb motoneuron activity can be evoked in decerebrate cats during fictive locomotion. As recorded in the peripheral nerves, twice threshold intensity stimulation of the cutaneous superficial peroneal (SP) nerve during the flexion phase produced a very brief excitation of ankle flexors (e.g., tibialis anterior and peroneus longus) that was followed by an inhibition for the duration of the stimulus train (10-25 shocks, 200 Hz). Extensor digitorum longus was always, and hip flexor (sartorius) activity was sometimes, inhibited during SP stimulation. At the same time, knee flexor and the normally quiescent ankle extensor motoneurons were recruited (mean latencies 4 and 16 ms) with SP stimulation during fictive stumbling correction. After the stimulus train, ankle extensor activity fell silent, and there was an excitation of hip, knee, and ankle flexors. The ongoing flexion phase was often prolonged. Hip extensors were also recruited in some fictive stumbling trials. Only the SP nerve was effective in evoking stumbling correction. Delivered during extension, SP stimulus trains increased ongoing extensor motoneuron activity as well as increasing ipsilateral hip, knee, and ankle hindlimb flexor activity in the subsequent step cycle. The fictive stumbling corrective reflex seems functionally similar to that evoked in intact, awake animals and involves a fixed pattern of short-latency reflexes as well as actions evoked through the lumbar circuitry responsible for the generation of rhythmic alternating locomotion.     

Human neuronal interlimb coordination during split-belt locomotion

Human interlimb coordination and the adaptations in leg muscle activity were studied during walking on a treadmill with split belts. Four different belt speeds (0.5, 1.0, 1.5, 2.0 m/s) were offered in all possible combinations for the left and right leg. Subjects adapted automatically to a difference in belt speed within 10–20 stride cycles.This adaptation was achieved by a reorganization of the stride cycle with a relative shortening of the duration of the support and lengthening of the swing phase of the fast leg and, vice versa, in support and swing duration on the slow leg. The electromyogram EMG patterns were characterized by two basic observations: (1) onset and timing of EMG activity were influenced by biomechanical constraints. A shortening of the support phase on the faster side was related to an earlier onset and increase in gastrocnemius activity, while a coactivation pattern in the antagonistic leg muscles was predominant during a prolonged support phase on the slower side. (2) A differential modulation of the antagonistic leg muscles took place. An increase in ipsilateral belt speed in combination with a constant contralateral belt speed was associated with an almost linear increase in ipsilateral gastrocnemius and contralateral tibialis anterior EMG activity, while the contralateral gastrocnemius and ipsilateral tibialis anterior EMG activity were little affected. It is concluded that a modifiable timing within the stride cycle takes place with a coupling between ipsilateral support and contralateral swing phase. The neuronal control of this coupling is obviously based on ipsilateral modulation of leg extensor EMG by proprioceptive feedback and an appropriate central (e.g. spinal) modulation of contralateral tibialis anterior EMG activity.     

Signals from load sensors underlie interjoint coordination during stepping movements of the stick insect leg

During stance and swing phase of a walking stick insect, the retractor coxae (RetCx) and protractor coxae (ProCx) motoneurons and muscles supplying the thorax-coxa (TC)-joint generate backward and forward movements of the leg. Their activity is tightly coupled to the movement of the more distal leg segments, i.e., femur, tibia, and tarsus. We used the single middle leg preparation to study how this coupling is generated. With only the distal leg segments of the middle leg being free to move, motoneuronal activity of the de-afferented and -efferented TC-joint is similarly coupled to leg stepping. RetCx motoneurons are active during stance and ProCx motoneurons during swing. We studied whether sensory signals are involved in this coordination of TC-joint motoneuronal activity. Ablation of the load measuring campaniform sensilla (CS) revealed that they substantially contribute to the coupling of TC-joint motoneuronal activity to leg stepping. Individually ablating trochanteral and femoral CS revealed the trochanteral CS to be necessary for establishing the coupling between leg stepping and coxal motoneuron activity. When the locomotor system was active and generated alternating bursts of activity in ProCx and RetCx motoneurons, stimulation of the CS by rearward bending of the femur in otherwise de-afferented mesothoracic ganglion terminated ongoing ProCx motoneuronal activity and initiated RetCx motoneuronal activity. We show that cuticular strain signals from the trochanteral CS play a major role in shaping TC-joint motoneuronal activity during walking and contribute to their coordination with the stepping pattern of the distal leg joints. We present a model for the sensory control of timing of motoneuronal activity in walking movements of the single middle leg.     

Climbing fiber afferent modulation during treadmill locomotion in the cat

The relationship of the climbing fiber afferent discharge to the unperturbed and perturbed step cycle was evaluated in the cat. Following a precollicular-premamillary decerebration, cats walked spontaneously on a motorized treadmill. Purkinje cells were recorded extracellularly and simple and complex spikes were discriminated. Right forelimb displacement, biceps and triceps EMG activity, as well as treadmill velocity, were also monitored. In some animals pressure measurements of the contact of the footpad with the treadmill were obtained. Cells were studied during both "normal" and perturbed locomotion. The perturbation consisted of a braking of the treadmill at different phases in the step cycle. Histograms of the simple and complex spike activity, and averages of the right forelimb displacement, biceps, and triceps EMG activity and treadmill velocity were constructed. The complex spike activity of 163 Purkinje cells was averaged through a minimum of 50 sweeps in either normal and/or perturbed locomotion. Statistical analysis revealed that the probability of the climbing fiber afferent discharge in 54% of the cells (36/67) studied during normal locomotion was significantly modulated with the step cycle. For most Purkinje cells the onset of the increase in climbing fiber afferent discharge was coupled to triceps activity and the onset of stance phase. A group of cells exhibited complex spike discharge in association with biceps onset and swing. These observations suggest that complex spike discharge occurs preferentially at the phase transition periods in the step cycle when the trajectory of the forelimb changes from swing to stance or stance to swing. During treadmill braking 51% of the cells exhibited complex spike modulation (70/137). A number of different patterns of climbing fiber afferent modulation occurred. The most common pattern was an increase in complex spike discharge with the resumption of the treadmill movement and locomotion. Analysis of the time of these periods of increased climbing fiber activity suggests that, although in some cells the response is coupled to the treadmill onset, in other cells the modulation occurs at longer latencies. Subsequent analysis aligning the EMG, displacement, and treadmill velocity signals with the times of the climbing fiber afferent discharge suggested some responses were coupled to the reinitiation of the locomotor cycle. The second most common pattern was an increase in climbing fiber afferent discharge at the onset of the perturbation. Also, in some cells, complex spike discharge decreased during the period in which the step cycle was arrested.(ABSTRACT TRUNCATED AT 400 WORDS)     

Gamma-motoneurone discharge patterns during fictive locomotion in the decerebrate cat

Triceps surae gamma-motoneurones were recorded during fictive locomotion in the paralysed high decerebrate cat. Two distinctive patterns of discharge were observed which were similar to those reported for static and dynamic gamma-motoneurones during locomotion in the same preparation, but without paralysis (Murphy, Stein & Taylor, 1984). These results suggest that movement-related afferent feedback is not essential for the generation of the basic patterns of static and dynamic gamma-motoneurone activity during locomotion. The results are discussed in relation to the generation of alpha and gamma locomotor rhythms.     

Somatosensory control of balance during locomotion in decerebrated cat

Postmammillary decerebrated cats can generate stepping on a moving treadmill belt when the brain stem or spinal cord is stimulated tonically and the hindquarters are supported both vertically and laterally. While adequate propulsion seems to be generated by the hindlimbs under these conditions, the ability to sustain equilibrium during locomotion has not been examined extensively. We found that tonic epidural spinal cord stimulation (5 Hz at L5) of decerebrated cats initiated and sustained unrestrained weight-bearing hindlimb stepping for extended periods. Detailed analyses of the relationships among hindlimb muscle EMG activity and trunk and limb kinematics and kinetics indicated that the motor circuitries in decerebrated cats actively maintain equilibrium during walking, similar to that observed in intact animals. Because of the suppression of vestibular, visual, and head-neck-trunk sensory input, balance-related adjustments relied entirely on the integration of somatosensory information arising from the moving hindquarters. In addition to dynamic balance control during unperturbed locomotion, sustained stepping could be reestablished rapidly after a collapse or stumble when the hindquarters switched from a restrained to an unrestrained condition. Deflecting the body by pulling the tail laterally induced adaptive modulations in the EMG activity, step cycle features, and left-right ground reaction forces that were sufficient to maintain lateral stability. Thus the brain stem-spinal cord circuitry of decerebrated cats in response to tonic spinal cord stimulation can control dynamic balance during locomotion using only somatosensory input.     

Evidence that popliteal fat provides damping during locomotion in the cat

Current models and concepts of motor control represent the limb as a neuro-musculoskeletal system and rarely include other potentially important supporting tissues such as fascia and adipose tissue. It is possible that a normal complement of adipose tissue could contribute to the viscoelastic properties of supporting limbs and enhance stability during locomotion. The purpose of this study was to determine if the popliteal fat pad plays a role in locomotion in the cat. It is hypothesized that the fat pad limits flexion and reduces angular acceleration of the included hip, knee and ankle joints in the sagittal plane throughout the step cycle. 3D kinematics from 3 spontaneously locomoting decerebrate cats both before and after lipectomy were recorded during treadmill walking. Four time points throughout the step cycle were chosen for angular acceleration analysis: mid-stance, paw off, mid-swing and peak deceleration at the end of the re-extension of the knee. Significant increases in maximum angular acceleration for the hip, knee and ankle joints at these time points were observed. No significant increase in range of motion was found across all 3 included angles after lipectomy. Therefore, the hypothesis that the popliteal fat pad acts to decrease the angular acceleration is supported by these findings. The data indicate that the popliteal fat pad contributes to the damping component of the viscoelastic properties of the limb. These results may be applied to models of the hindlimb and knowledge of the effects of obesity on movement.     

Timing and distance characteristics of interpersonal coordination during locomotion

Most studies about human locomotion only tend to consider single subjects walking alone in a stationary environment. Nevertheless, human subjects have often to plan and generate their locomotor trajectories according to one another's displacements. Therefore, in the present study we address the question of the interpersonal coordination when pairs of subjects walk simultaneously. Six pairs of subjects walking face to face, backwards and forwards on a 8 m x 2 m track were involved in our experiment. Within each pair, the leader (L) was required to break the initial interpersonal distance whereas the follower (F) had to maintain this distance constant (1, 2 or 3 m). We measured their position and analyzed their travelled distance, the time course of their linear displacement, and the kinematics parameters of their steps. Our results show that F travels smaller distances than L and that even if they are highly correlated, some temporal delays exist between displacements of L and F with greater values when the interpersonal distance increases (from 1 to 3 m). These results are discussed in terms of high level imitation, i.e. bidirectional interactions with mutual influences of each subject on one another.     

Intra-axonal recordings of cutaneous primary afferents during fictive locomotion in the cat

1. Cutaneous primary afferents were recorded intracellularly during fictive locomotion in decorticated cats with the goal of improving our understanding of how locomotor networks might centrally control the transmission in cutaneous pathways at a presynaptic level. 2. Identified cutaneous axons from superficialis peroneal nerve (SP) or tibialis posterior nerve (TP) were recorded intracellularly together with the electroneurograms (ENGs) of representative flexor and extensor muscle nerves of the hindlimb as well as dorsal root potential from L6 or L7 (DRP). Fictive locomotion occurred spontaneously after decortication (n = 12) or was induced by stimulation of the mesencephalic locomotor region (MLR) (n = 6). 3. The results revealed that all cutaneous axons (82 units with resting potential greater than 45 mV) showed fluctuations of their membrane potential (greater than or equal to 0.5 mV) at the rhythm of the fictive locomotion. The characteristics of fluctuation patterns, common to all cutaneous units, consisted of two depolarization waves per cycle: one related to the flexor activity, the other related to the extensor activity. The flexor-related depolarization was followed by a sharp trough of membrane repolarization. The extensor-related depolarization usually overlapped partly with the flexor-depolarization of the following cycle. The relative size of each depolarization could vary among different afferents of the same nerve in the same animal. Hence, maximal depolarization could occur in different parts of the locomotor cycle, but, for the majority of units (82%), it occurred during the flexor activity. These results were similar for SP and TP units. 4. Twenty percent of the units were discharging with a constant or irregular frequency. Phasic antidromic discharges related to locomotor ENGs were rarely encountered (5/82 units). 5. Linear regression analysis of the temporal relationships between fluctuations of membrane potential of cutaneous axons and locomotor bursts over several cycles showed that the timing of presynaptic events in cutaneous afferents is related to the events of the locomotor output. However, the same type of analysis showed that the amplitude of axonal depolarizations and the amplitude of flexor and extensor locomotor bursts could vary independently. Tight temporal relationships were also found between the depolarizations recorded in cutaneous units and the fluctuations recorded at the dorsal root level (DRP). 6. Based on the assumption that the locomotor fluctuations of cutaneous membrane potential are mediated through the primary afferent depolarization (PAD) pathways associated with presynaptic inhibition, it is proposed that the central pattern generator for locomotion (CPG) could phasically control the efficacy of transmission of cutaneous pathways at a presynaptic level as part of the locomotor program.     

Short-latency crossed inhibitory responses in extensor muscles during locomotion in the cat

During locomotion, contacting an obstacle generates a coordinated response involving flexion of the stimulated leg and activation of extensors contralaterally to ensure adequate support and forward progression. Activation of motoneurons innervating contralateral muscles (i.e., crossed extensor reflex) has always been described as an excitation, but the present paper shows that excitatory responses during locomotion are almost always preceded by a short period of inhibition. Data from seven cats chronically implanted with bipolar electrodes to record electromyography (EMG) of several hindlimb muscles bilaterally were used. A stimulating cuff electrode placed around the left tibial and left superficial peroneal nerves at the level of the ankle in five and two cats, respectively, evoked cutaneous reflexes during locomotion. During locomotion, short-latency ( approximately 13 ms) inhibitory responses were frequently observed in extensors of the right leg (i.e., contralateral to the stimulation), such as gluteus medius and triceps surae muscles, which were followed by excitatory responses ( approximately 25 ms). Burst durations of the left sartorius (Srt), a hip flexor, and ankle extensors of the right leg increased concomitantly in the mid- to late-flexion phases of locomotion with nerve stimulation. Moreover, the onset and offset of Srt and ankle extensor bursts bilaterally were altered in specific phases of the step cycle. Short-latency crossed inhibition in ankle extensors appears to be an integral component of cutaneous reflex pathways in intact cats during locomotion, which could be important in synchronizing EMG bursts in muscles of both legs.     

Sensory integration in presynaptic inhibitory pathways during fictive locomotion in the cat

The aim of this study is to understand how sensory inputs of different modalities are integrated into spinal cord pathways controlling presynaptic inhibition during locomotion. Primary afferent depolarization (PAD), an estimate of presynaptic inhibition, was recorded intra-axonally in group I afferents (n = 31) from seven hindlimb muscles in L(6)-S(1) segments during fictive locomotion in the decerebrate cat. PADs were evoked by stimulating alternatively low-threshold afferents from a flexor nerve, a cutaneous nerve and a combination of both. The fictive step cycle was divided in five bins and PADs were averaged in each bin and their amplitude compared. PADs evoked by muscle stimuli alone showed a significant phase-dependent modulation in 20/31 group I afferents. In 12/20 afferents, the cutaneous stimuli alone evoked a phase-dependent modulation of primary afferent hyperpolarization (PAH, n = 9) or of PADs (n = 3). Combining the two sensory modalities showed that cutaneous volleys could significantly modify the amplitude of PADs evoked by muscle stimuli in at least one part (bin) of the step cycle in 17/31 (55%) of group I afferents. The most common effect (13/17) was a decrease in the PAD amplitude by 35% on average, whereas it was increased by 17% on average in the others (4/17). Moreover, in 8/13 afferents, the PAD reduction was obtained in 4/5 bins i.e., for most of the duration of the step cycle. These effects were seen in group I afferents from all seven muscles. On the other hand, we found that different cutaneous nerves had quite different efficacy; the superficial peroneal (SP) being the most efficient (85% of trials) followed by Saphenous (60%) and caudal sural (44%) nerves. The results indicate that cutaneous interneurons may act, in part, by modulating the transmission in PAD pathways activated by group I muscle afferents. We conclude that cutaneous input, especially from the skin area on the dorsum of the paw (SP), could subtract presynaptic inhibition in some group I afferents during perturbations of stepping (e.g., hitting an obstacle) and could thus adjust the influence of proprioceptive feedback onto motoneuronal excitability.     

Effect of hindlimb unloading on interlimb coordination during treadmill locomotion in the rat

Effects of hindlimb unloading on interlimb coordination were examined in adult rats walking on a treadmill at moderate speed. In the first group of animals, the electromyographic activity (EMG) of soleus muscle of both hindlimbs was recorded after 7 and 14 days of unloading. In the second group, the EMG was recorded daily until the 14th day of unloading. The general organization of locomotion was preserved in the two groups whatever the duration of the unloading. The step cycles of the two hindlimbs were always strictly alternating. However, the locomotor pattern was very irregular. A lateral instability was observed. It was accompanied by an abduction of the hindlimbs, and frequent hyperextensions of the ankle when walking. The EMG analysis showed an increase in step cycle duration and in coactivation duration of the soleus muscles (i.e. in the double stance duration). In the rats recorded daily, mean EMG was dramatically reduced the 1st day of unloading, suggesting a decrease in the neural drive. Taken together, these data indicate that 14 days of hindlimb unloading can alter the neuromuscular pattern during locomotion. It is proposed that these changes are related to changes in the peripheral sensory information.     

An analytical formulation of the law of intersegmental coordination during human locomotion

The law of intersegmental coordination is a kinematic law that describes the coordination patterns among the elevation angles of the lower limb segments during locomotion (Borghese et al. in J Physiol 494:863–879, 1996). This coordination pattern reduces the number of degrees of freedom of the lower limb to two, i.e. the elevation angles covary along a plane in angular space. The properties of the plane that constrains the time course of the elevation angles have been extensively studied, and its orientation was found to be correlated with gait velocity and energy expenditure (Bianchi et al. in J Neurophysiol 79:2155–2170, 1998). Here, we present a mathematical model that represents the rotations of the elevation angles in terms of simple oscillators with appropriate phase shifts between them. The model explains what requirements the time courses of the elevation angles must fulfill in order for the angular covariation relationship to be planar. Moreover, an analytical formulation is proposed for both the orientation of the plane and for the eccentricity of the nearly elliptical shape that is generated within this plane, in terms of the amplitudes and relative phases of the first harmonics of the segments elevation angles. The model presented here sheds some new light on the possible interactions among the Central Pattern Generators possibly underlying the control of biped locomotion. The model precisely specifies how any two segments in the limb interact, and how a change in gait velocity affects the orientation of the intersegmental coordination plane mainly through a change in phase shifts between the segments. Implications of this study with respect to neural control of locomotion and other motor activities are discussed. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.