Contribution of the motor cortex to the structure and the timing of hindlimb locomotion in the cat: a microstimulation study

We used microstimulation to examine the contribution of the motor cortex to the structure and timing of the hindlimb step cycle during locomotion in the intact cat. Stimulation was applied to the hindlimb representation of the motor cortex in 34 sites in three cats using either standard glass-insulated microelectrodes (16 sites in 1 cat) or chronically implanted microwire electrodes (18 sites in 2 cats). Stimulation at just suprathreshold intensities with the cat at rest produced multi-joint movements at a majority of sites (21/34, 62%) but evoked responses restricted to a single joint, normally the ankle, at the other 13/34 (38%) sites. Stimulation during locomotion generally evoked larger responses than the same stimulation at rest and frequently activated additional muscles. Stimulation at all 34 sites evoked phase-dependent responses in which stimulation in swing produced transient increases in activity in flexor muscles while stimulation during stance produced transient decreases in activity in extensors. Stimulation with long (200 ms) trains of stimuli in swing produced an increased level of activity and duration of flexor muscles without producing changes in cycle duration. In contrast, stimulation during stance decreased the duration of the extensor muscle activity and initiated a new and premature period of swing, resetting the step cycle. Stimulation of the pyramidal tract in two of these three cats as well as in two additional ones produced similar effects. The results show that the motor cortex is capable of influencing hindlimb activity during locomotion in a similar manner to that seen for the forelimb.     

A kinematic and electromyographic study of cutaneous reflexes evoked from the forelimb of unrestrained walking cats

A kinematic and electromyographic (EMG) analysis was undertaken of the responses evoked in the forelimb of the cat by either mechanical obstruction of the forelimb during the swing phase of locomotion or by electrical stimulation of low-threshold cutaneous afferents during both swing and stance. Mechanical obstruction of the forelimb with a stiff metal rod evoked a complex response that allowed the cat to smoothly negotiate the obstacle without undue disruption of the overall locomotor rhythm. The initial movements were a flexion of the shoulder, together with a locking of the elbow joint, and a dorsiflexion of the wrist, which caused the limb to withdraw from the obstacle. They were followed by an extension of the shoulder, a flexion of the elbow, and a ventroflexion of the wrist, which together brought the limb forward and above the obstacle. The associated and complex pattern of short- and long-latency EMG responses was shown to be related to different aspects of the movement. At the shoulder there was a strong activation of flexor muscles; these responses were of long duration (greater than or equal to 100 ms) and generally lasted throughout the period of shoulder flexion. At the elbow, both flexor and extensor muscles were activated at short latency (9-13 ms). In flexors, this was followed by a cessation and subsequently an augmentation and prolongation of their activity. Dorsiflexors of both the wrist and digits were activated at short latency (10-12 ms) and remained active throughout the period of dorsiflexion of these joints. An injection of a local anesthetic into the area of skin contacted by the metal rod reduced or abolished all of the reflex responses, which suggests that the integrity of cutaneous reflex pathways is essential for the elaboration of these responses. Electrical stimulation of a cutaneous nerve innervating the distal forelimb (the superficial radial nerve) resulted in qualitatively similar, although weaker, responses to those obtained with the mechanical stimulation. Terminal experiments confirmed that these responses were mediated by low-threshold cutaneous afferents. Electrical stimulation also evoked short-latency excitatory responses (10-12 ms) in extensor muscles of the elbow. Generally, the largest reflex effects were obtained during the period of swing for flexor, extensor, and bifunctional muscles. During stance the stimulus was normally ineffective in exciting flexor muscles and in extensors evoked a short-latency inhibition, which was frequently followed by an increase in activity.(ABSTRACT TRUNCATED AT 400 WORDS)     

Functional organization within the medullary reticular formation of the intact unanesthetized cat. III. Microstimulation during locomotion.

1. This article presents the results from stimulation in 21 loci within the medullary reticular formation (MRF; between 0.5 and 2.5 mm from the midline) and in 5 loci in the medial longitudinal fasciculus (MLF) of four intact, unanesthetized cats during locomotion. Stimulus trains (11 pulses, 0.2-ms duration, 330 Hz, stimulus strength 35 microA) were applied at those loci in each track at which the most widespread effects in each of the four limbs were obtained with the cat at rest. Electromyograms were recorded from flexor and extensor muscles of each limb. 2. As previously reported, stimulation with the cat at rest generally evoked brief, short-latency, twitch responses in both flexor and extensor muscles of more than one limb. In contrast, stimulation during locomotion evoked a more complex pattern of activity in which responses were normally evoked in one or other of the muscle pairs and incorporated into the locomotor pattern. 3. In the majority of sites, the stimulation evoked excitatory responses in the flexor muscles of each of the four limbs during that period of the step cycle in which each respective muscle was naturally active; stimulation in the stance phase of locomotion, although less effective, was also capable of producing responses in these muscles. All three ipsilateral extensor muscles studied [long and lateral heads of triceps and vastus lateralis (Tri, TriL, and VL, respectively)] were normally inhibited during their phase of muscle activity, although excitatory responses were occasionally seen. Responses in the contralateral (co) Tri were invariably excitatory and were largest during the period of muscle activity, whereas responses during the period of activity of the coVL were mixed, with both excitatory and inhibitory responses being seen from any one locus. 4. Excitatory responses were normally largest when stimulation was applied during the time that the muscle was active during the locomotor cycle. Responses evoked at times when the muscle was inactive were sometimes larger than those evoked with the animal at rest; such responses were most commonly seen in the hindlimb flexors and in the coVL. 5. In both flexors and extensors of each of the four limbs, the latency of the responses was greatest when the cat was at rest and least for stimuli given during the period of activity of the respective muscle. Average latencies during the period of muscle activity ranged from a minimum of 9.0 +/- 2.6 (SD) ms for inhibitory responses in the ipsilateral Tri and TriL to a maximum of 17.1 +/- 3.0 ms for the responses evoked in the ipsilateral semitendinosus.(ABSTRACT TRUNCATED AT 400 WORDS)     

Discharge characteristics of neurons in the red nucleus during voluntary gait modifications: a comparison with the motor cortex

We have examined the contribution of the red nucleus to the control of locomotion in the cat. Neuronal activity was recorded from 157 rubral neurons, including identified rubrospinal neurons, in three cats trained to walk on a treadmill and to step over obstacles attached to the moving belt. Of 72 neurons with a receptive field confined to the contralateral forelimb, 66 were phasically active during unobstructed locomotion. The maximal activity of the majority of neurons (59/66) was centered around the swing phase of locomotion. Slightly more than half of the neurons (36/66) were phasically activity during both swing and stance. In addition, some rubral neurons (14/66) showed multiple periods of phasic activity within the swing phase of the locomotor cycle. Periods of phasic discharge temporally coincident with the swing phase of the ipsilateral limb were observed in 7/66 neurons. During voluntary gait modifications, most forelimb-related neurons (70/72) showed a significant increase in their discharge activity when the contralateral limb was the first to step over the obstacle (lead condition). Maximal activity in nearly all cells (63/70) was observed during the swing phase, and 23/63 rubral neurons exhibited multiple increases of activity during the modified swing phase. A number of cells (18/70) showed multiple periods of increased activity during swing and stance. Many of the neurons (35/63, 56%) showed an increase in activity at the end of the swing phase; this period of activity was temporally coincident with the period of activity in wrist dorsiflexors, such as the extensor digitorum communis. A smaller proportion of neurons with receptive fields restricted to the hindlimbs showed similar characteristics to those observed in the population of forelimb-related neurons. The overall characteristics of these rubral neurons are similar to those that we obtained previously from pyramidal tract neurons recorded from the motor cortex during an identical task. However, in contrast to the results obtained in the rubral neurons, most motor cortical neurons showed only one period of increased activity during the step cycle. We suggest that both structures contribute to the modifications of the pattern of EMG activity that are required to produce the change in limb trajectory needed to step over an obstacle. However, the results suggest an additional role for the red nucleus in regulating intra- and interlimb coordination.     

Corticospinal input in human gait: modulation of magnetically evoked motor responses

 Transcranial magnetic stimulation (TMS) of the motor cortex was applied during locomotion to investigate the significance of corticospinal input upon the gait pattern. Evoked motor responses (EMR) were studied in the electromyogram (EMG) of tibialis anterior (TA), gastrocnemius (GM) and, for reference, abductor digiti minimi (AD) muscles by applying below-threshold magnetic stimuli during treadmill walking in healthy adults. Averages of 15 stimuli introduced randomly at each of 16 phases of the stride cycle were analysed. Phase-dependent amplitude modulation of EMR was present in TA and GM which did not always parallel the gait-associated modulation of the EMG activity. No variation of onset latency of the EMR was observed. The net modulatory response was calculated by comparing EMR amplitudes during gait with EMR amplitudes obtained (at corresponding background EMG activities) during tonic voluntary muscle contraction. Large net responses in both muscles occurred prior to or during phasic changes of EMG activity in the locomotor pattern. This facilitation of EMR was significantly higher in leg flexor than extensor muscles, with maxima in TA prior to and during late swing phase. A comparison of this facilitation of TA EMR prior to swing phase and prior to a phasic voluntary foot dorsiflexion revealed a similar onset but an increased amount of early facilitation in the gait condition. The modulated facilitation of EMR during locomotion could in part be explained by spinal effects which are different under dynamic and static motor conditions. However, we suggest that changes in corticospinal excitability during gait are also reflected in this facilitation. This suggestion is based on: (1) the similar onset yet dissimilar size of facilitatory effects in TA EMR prior to the swing phase of the stride cycle and during a voluntary dynamic activation, (2) the inverse variation of EMR and EMG amplitudes during this phase, and (3) the occurrence of this inversion at stimulation strengths below motor threshold (motor threshold was determined during weak tonic contraction and EMR were facilitated during gait). It is hypothesized that the facilitation is phase linked to ensure postural stability and is most effective during the phases prior to and during rhythmical activation of the leg muscles resulting in anticipatory adjustment of the locomotor pattern. Received: 17 May 1996 / Accepted: 29 November 1996     

Facilitation from ventral premotor cortex of primary motor cortex outputs to macaque hand muscles

We demonstrate that in the macaque monkey there is robust, short-latency facilitation by ventral premotor cortex (area F5) of motor outputs from primary motor cortex (M1) to contralateral intrinsic hand muscles. Experiments were carried out on two adult macaques under light sedation (ketamine plus medetomidine HCl). Facilitation of hand muscle electromyograms (EMG) was tested using arrays of fine intracortical microwires implanted, respectively, in the wrist/digit motor representations of F5 and M1, which were identified by previous mapping with intracortical microstimulation. Single pulses (70-200 microA) delivered to F5 microwires never evoked any EMG responses, but small responses were occasionally seen with double pulses (interval: 3 ms) at high intensity. However, both single- and double-pulse stimulation of F5 could facilitate the EMG responses evoked from M1 by single shocks. The facilitation was large (up to 4-fold with single and 12-fold with double F5 shocks) and occurred with an early onset, with significant effects at intervals of only 1-2 ms between conditioning F5 and test M1 stimuli. A number of possible pathways could be responsible for these effects, although it is argued that the most likely mechanism would be the facilitation, by cortico-cortical inputs from F5, of corticospinal I wave activity evoked from M1. This facilitatory action could be of considerable importance for the coupling of grasp-related neurons in F5 and M1 during visuomotor tasks.     

The role of cutaneous afferents in controlling locomotion evoked by epidural stimulation of the spinal cord in decerebrate cats

The effects of the cutaneous input on the formation of the locomotor pattern in conditions of epidural stimulation of the spinal cord in decerebrate cats were studied. Locomotor activity was induced by rhythmic stimulation of the dorsal surface of spinal cord segments L4-L5 at a frequency of 3-5 Hz. Electromyograms (EMG) recorded from the antagonist muscles quadriceps, semitendinosus, tibialis anterior, and gastrocnemius lateralis were recorded, along with the kinematics of stepping movements during locomotion on a moving treadmill and reflex responses to single stimuli. Changes in the pattern of reactions observed before and after exclusion of cutaneous receptors (infiltration of lidocaine solution at the base of the paw or irrigation of the paw pads with chlorothane solution) were assessed. This treatment led to impairment of the locomotor cycle: the paw was placed with the rear surface downward and was dragged along in the swing phase, and the duration of the stance phase decreased. Exclusion of cutaneous afferents suppressed the polysynaptic activity of the extensor muscles and the distal flexor muscle of the ipsilateral hindlimb during locomotion evoked by epidural stimulation of the spinal cord. The effects of exclusion of cutaneous afferents on the monosynaptic component of the EMG response were insignificant.     

Stimulation of the group I extensor afferents prolongs the stance phase in walking cats

Group I afferents in nerves innervating the lateral gastrocnemius-soleus (LG-Sol), plantaris (P1), and vastus lateralis/intermedius (VL/VI) muscles were stimulated during walking in decerebrate cats. The stimulus trains were triggered at a fixed delay following the onset of bursts in the medial gastrocnemius muscle. Stimulation of all three nerves with long stimulus trains (>600 ms) prolonged the extensor bursts and delayed the onset of flexor burst activity. LG-Sol nerve stimulation had the strongest effect; often delaying the onset of flexor burst activity until the stimulus train was ended. By contrast, flexor bursts were usually initiated before the end of the stimulus train to the P1 and VL/VI nerves. The minimum stimulus strength required to increase the cycle period was between 1.3×threshold and 1.6×threshold for all three nerves. Simultaneous stimulation of the P1 and VL/VI nerves produced a larger effect on the cycle period than stimulation of either nerve alone. The spatial summation of inputs from knee and ankle muscles suggests that the excitatory action of the group I afferents during the stance phase is distributed to all leg extensor muscles. Stimulation of the group I afferents in extensor nerves generally produced an increase in the amplitude of the heteronymous extensor EMG towards the end of the stance phase. This increase in amplitude occurred even though there were only weak monosynaptic connections between the stimulated afferents and the motoneurones that innervated these heteronymous muscles. This suggests that the excitation was produced via oligosynaptic projections onto the extensor motoneuronal pool. Stimulation with 300 ms trains during the early part of flexion resulted in abrupt termination of the swing phase and reinitiation of the stance phase of the step cycle. The swing phase resumed coincidently with the stimulus offset. Usually, stimulation of two extensor nerves at group I strengths was required to elicit this effect. We were unable to establish the relative contributions of input from the group 1a and group 1b afferents to prolonging the stance phase. However, we consider it likely that group Ib afferents contribute significantly, since their activation has been shown to prolong extensor burst activity in reduced spinal preparations. Thus, our results add support to the hypothesis that unloading of the hindlimb during late stance is a necessary condition for the initiation of the swing phase in walking animals.     

Gating and reversal of reflexes in ankle muscles during human walking

Summary Phase-dependent reflex modulation was studied by recording the electromyographic (EMG) responses in ankle flexors (Tibialis Anterior, TA) and extensors (Gastrocnemius Medialis, GM and Soleus, SOL) to a 20 ms train of electrical pulses, applied to the tibial or sural nerve at the ankle, in human volunteers walking on a treadmill at 4 km/h. For low intensity stimuli (i.e. 1.6 times perception threshold), given during the swing phase, the most common response was a suppression of the TA activity with a latency of 67 to 118 ms. With high intensity of stimulation (i.e. 2.8 × T), a facilitatory response appeared in TA with a latency of 74 ms. This latter response was largest during the middle of the swing phase, when it was correlated with exaggerated ankle dorsiflexion. The TA reflex amplitude was not a simple function of the level of spontaneous ongoing activity. During stance, TA responses were small or absent and accompanied by a suppression of the GM activity with a latency ranging from 62 to 101 ms. A few subjects showed an early facilitatory, instead of a suppressive, GM response (88 to 136 ms latency). They showed a phase-dependent reflex reversal from a dominant TA response during swing to a facilitatory GM response with an equivalent latency during stance. The GM facilitation occurred exclusively during the early stance phase and habituated more than the TA responses. It is concluded that phase-dependent gating of reflexes occurs in ankle muscles of man, but only when vigorous extensor reflexes are present. More commonly, a phase-dependent modulation is seen, both of facilitatory and suppressive responses.     

Simultaneous control of two rhythmical behaviors. I. Locomotion with paw-shake response in normal cat

We investigated the ability of normal cats, trained to maintain a constant position while walking on a treadmill, to combine the paw-shake response with quadrupedal locomotion. Hindlimb paw-shake responses were elicited during walking after the right hindpaw was wrapped with tape. To assess intralimb and interlimb coordination of the combined behaviors, electromyographic (EMG) recordings from forelimb extensor muscles and from selected flexor and extensor muscles at the three major hindlimb joints were correlated with joint motion by using high-speed, cinefilm analysis. When paw shaking was combined with walking, the response occurred during the swing phase of the taped hindlimb. To accommodate the paw-shake response, swing duration of the shaking hindlimb and of the homolateral forelimb increased and was followed by a brief recovery step. Concurrently, to compensate for the response, stance durations of the contralateral forelimb and hindlimb increased. The magnitude of these adjustments in interlimb coordination was influenced by the number of paw-shake cycles, which ranged from one to four oscillations. Transitions between the muscle synergies for the paw-shake response and swing were smooth in the shaking limb. Early in the swing phase, when the flexor muscles were still active (F phase), the paw shake was initiated by an early onset of knee extensor activity, which preceded extensor activity at the hip and ankle. This action provided a transition from the general reciprocal synergy between flexor and extensor muscles of locomotion to the mixed synergy that is typical of the paw shake (30). Following the last paw-shake cycle, an extensor synergy initiated the E-1 phase of swing, and the resultant joint motion was in-phase extension of the hip, knee, and ankle to lower the paw for stance. Average cycle period and burst duration for muscles participating in the paw-shake response were similar to those reported for normal cats assuming a standing posture (28, 30). The average number of paw-shake cycles, however, decreased from eight to three when the response occurred during walking, suggesting that the response was truncated to provide for continued locomotion. Further, hip motion was variable when the paw shake was combined with swing, and sometimes the hip failed to oscillate and its trajectory was similar to that of an unperturbed swing phase. When hip joint oscillations occurred during the paw-shake response, they were in-phase with ankle motions.(ABSTRACT TRUNCATED AT 400 WORDS)     

Motor-unit responses in human wrist flexor and extensor muscles to transcranial cortical stimuli

1. Transcranial cortical stimuli (TCCS) were used to elicit motor responses in contralateral wrist flexor and extensor muscles of healthy adult subjects. The motor responses were assessed by surface EMG recordings, by needle recordings of single motor-unit discharges, and by measurements of wrist twitch force. Our main aim was to analyze the single-unit events underlying those changes in latency, amplitude, and duration of the compound EMG responses, which could be induced by voluntary preactivation of target muscles and by changes in stimulation strength. 2. Different stimulus strengths were tested with and without background contractions in the flexor or extensor muscles. For each test (consisting of a series of 20 stimuli) the compound EMG responses were averaged and displayed together with the averaged wrist force signals. Responses of individual flexor and extensor motor units were displayed in raster diagrams and peristimulus time histograms. For units exhibiting a background firing, the mean background interdischarge interval was calculated and compared with the subsequent poststimulus intervals. 3. In relaxed muscles, a shortening of onset latency of evoked compound EMG responses was observed when raising stimulation strength. A similar latency reduction was not seen in any of the single-unit recordings. This would be consistent with the size principle of motoneuron recruitment. 4. A shortening of onset latency of evoked EMG potentials was observed also as a result of a voluntary preactivation. Such latency shifts, which were seen also in single-unit recordings, might be attributed to variations in the time required for D and I wave temporal summation at the anterior horn cell. 5. When raising stimulation strength or when adding voluntary background contraction, the evoked compound EMG potential grew not only in amplitude but also in duration, as later peaks of activity were added to the initial ones. Under optimal conditions (strong stimulus + background contraction), the period of excitation (termed E1) had an onset latency of approximately 15 ms and a duration of approximately 35 ms and was similar for wrist flexor and extensor muscles. 6. We never saw the same flexor or extensor unit fire more than once during the E1 period. For units preactivated by a background contraction, the stimulus-triggered impulse exhibited latency shifts, which, to a large extent, depended on the timing of the stimulus in relation to a preceding background discharge and which could be influenced by a change in stimulation strength.(ABSTRACT TRUNCATED AT 400 WORDS)     

Effects of pontomedullary reticular formation stimulation on the neuronal networks responsible for rhythmical jaw movements in the guinea pig

1. In the ketamine-anesthetized guinea pig, electromyographic (EMG) responses of the digastric muscle and vertical and horizontal movements of the mandible were studied when loci within the caudal pontine and rostral medullary reticular formation were stimulated during rhythmic jaw movements (RJMs) evoked by stimulation of the masticatory area of the cortex. 2. Within these regions electrical brain stem stimulation of the pontis nucleus caudalis and nucleus gigantocellularis (PnC-Gi) of the reticular formation completely blocked RJMs at stimulus intensities as low as 10 microA while suppressing the short-latency digastric EMG response that was time locked to each cortical stimulus in the train. PnC-Gi stimulation did not, however, reduce the excitability of the short-latency corticotrigeminal excitatory pathway to digastric motoneurons when tested by short pulse train stimulation at 2 Hz (3 pulses, 500 Hz, 0.3 ms) in the absence of RJMs. 3. Short trains (80 ms) of PnC-Gi stimuli delivered at various phases of the RJM cycle produced a permanent phase shift of the RJM rhythm. If the stimulus train was delivered at an early phase of the cycle (8-40%) the next cycle onset was advanced; if the train was delivered later in the cycle (60-80%) the next cycle onset was delayed. Long trains of PnC-Gi stimuli (100, 200, 300, and 400 ms) increased the time of onset of the next cycle by an amount directly proportional to the duration of the stimulus train. 4. Digastric EMG activity occurring during cortically evoked RJMs occupied nearly 50% of the cycle. If a short train of PnC-Gi stimuli was delivered between approximately 5 and 125 ms after the onset of the burst, the duration of the burst was significantly shortened. 5. These results demonstrate that the suppression of cortically evoked RJMs resulting from PnC-Gi stimulation is due to direct effects on central circuits responsible for the production of the RJM behavior and not on the motoneurons themselves. The evidence presented is consistent with our previously presented hypothesis that the neurons involved in mediating the short-latency corticotrigeminal pathway to digastric motoneurons are separate and distinct from those neurons comprising the central networks responsible for the production of the fundamental jaw oscillation during RJMs.     

Intracortical origin of the short latency facilitation produced by pairs of threshold magnetic stimuli applied to human motor cortex

Under certain conditions, EMG responses evoked by pairs of transcranial magnetic stimuli over the motor cortex are larger than the sum of the responses to each stimulus given alone. This occurs with interstimulus intervals of around 1.3, 2.5 and 4.3 ms and could be due to interaction between the responses to each stimulus at either the cortex or spinal cord. We recorded the descending volleys set up by such pairs of stimuli from the cervical epidural space of five patients implanted with chronic stimulators for pain control. Interstimulus intervals of 1, 1.2, 1.4 and 2 ms were used to investigate the first peak of facilitation. Enhanced EMG responses occurred after pairs of stimuli at 1, 1.2 and 1.4 ms, and these were accompanied by larger and more numerous descending volleys than expected from the sum of each stimulus alone. We conclude that facilitatory interaction between the stimuli can occur within the cerebral cortex. This may involve elements that produce repetitive I-wave activity in response to a single stimulus.     

Phase-dependent reversal of reflexly induced movements during human gait

Summary To investigate whether phase-dependent reversals in reflex responses on electromyography (EMG) are accompanied by movement reversals, a series of human volunteers were studied for their behavioural responses to sural nerve stimulation during running or walking on a treadmill. Low-intensity stimulation (< 2.5 x perception threshold, T) of the sural nerve yielded facilitatory responses in the tibialis anterior muscle (TA), correlated with an induced ankle dorsiflexion (mean maximum 4°) in early swing. The same stimuli yielded primarily TA suppression and weak ankle plantar flexion (mean maximum 1°) at end swing. The correlated induced knee angle changes did not precede the ankle changes, and they were relatively small. Mean maximum flexion in early swing was 6.2°, while mean maximum extension was 3.7°. High-intensity stimulation of the sural nerve (> 2.5 x T) always gave rise to suppression of the ongoing activity. This resulted in a second type of movement reversal. During late stance and early swing the responses in TA were suppressive (i.e. below background activity) and related to ankle plantar flexion. In contrast, the responses during early and middle stance consisted of suppression in extensor activity (gastrocnemius medialis and soleus) and ankle dorsiflexion.The data are discussed in terms of a new hypothesis, which states that the responses to electrical stimulation of cutaneous nerves during locomotion do not correspond directly to corrections for stumbling following mechanical perturbations during the step cycle. Instead, the data invite a reinterpretation in terms of the opening and closing of reflex pathways, presumably by a central pattern generator for locomotion.     

Reflex responses in active muscles elicited by stimulation of low-threshold afferents from the human foot.

1. Reflex responses were elicited in muscles that act at the ankle by electrical stimulation of low-threshold afferents from the foot in human subjects who were reclining supine. During steady voluntary contractions, stimulus trains (5 pulses at 300 Hz) were delivered at two intensities to the sural nerve (1.2-4.0 times sensory threshold) or to the posterior tibial nerve (1.1-3.0 times motor threshold for the intrinsic muscles of the foot). Electromyographic (EMG) recordings were made from tibialis anterior (TA), peroneus longus (PL), soleus (SOL), medial gastrocnemius (MG), and lateral gastrocnemius (LG) muscles by the use of intramuscular wire electrodes. 2. As assessed by averages of rectified EMG, stimulation of the sural or posterior tibial nerves at nonpainful levels evoked a complex oscillation with onset latencies as early as 40 ms and lasting up to 200 ms in each muscle. The most common initial responses in TA were a decrease in EMG activity at an onset latency of 54 ms for sural stimuli, and an increase at an onset latency of 49 ms for posterior tibial stimuli. The response of PL to stimulation of the two nerves began with a strong facilitation of 44 ms (sural) and 49 ms (posterior tibial). With SOL, stimulation of both nerves produced early inhibition beginning at 45 and 50 ms, respectively. With both LG and MG, sural stimuli produced an early facilitation at 52-53 ms. However, posterior tibial stimuli produced different initial responses in these two muscles: facilitation in LG at 50 ms and inhibition in MG at 51 ms. 3. Perstimulus time histograms of the discharge of 61 single motor units revealed generally similar reflex responses as in multiunit EMG. However, different reflex components were not equally apparent in the responses of different single motor units: an individual motor unit could respond slightly differently with a change in stimulus intensity or background contraction level. The multiunit EMG record represents a global average that does not necessarily depict the precise pattern of all motor units contributing to the average. 4. When subjects stood erect without support and with eyes closed, reflex patterns were seen only in active muscles, and the patterns were similar to those in the reclining posture. 5. It is concluded that afferents from mechanoreceptors in the sole of the foot have multisynaptic reflex connections with the motoneuron pools innervating the muscles that act at the ankle. When the muscles are active in standing or walking, cutaneous feedback may play a role in modulating motoneuron output and thereby contribute to stabilization of stance and gait.     

Study of cutaneous reflex compensation during locomotion after nerve section in the cat

In the cat, section of all cutaneous nerves of the hindfeet except the tibial (Tib) nerve supplying the plantar surface results in a long-lasting decrease in the intensity of Tib stimulation needed for a threshold response in flexor muscles and an increase in the amplitude of the phase-dependent responses recorded in various muscles during locomotion. Stimulating through chronically implanted nerve cuffs ensured a stable stimulation over time. The increase in reflex amplitude was well above the small increase in the amplitude of the locomotor bursts themselves that results from the denervation. Short latency responses (P1) were seen in flexor muscles, especially at the knee (semitendinosus) and ankle (tibialis anterior and extensor digitorum longus), with stimuli applied in the swing phase and also to a lesser degree in the later part of the cycle. Longer latency responses (P2) were increased in hip, knee, and ankle flexors, as well as in a contralateral extensor (vastus lateralis) when applied in late stance. Responses evoked from stimulating the proximal end of sectioned nerves were not larger than before neurectomy. This suggests that the increased responsiveness to Tib stimulation is not simply caused by an increase in motoneuron excitability, because this would have resulted in a nonspecific increase of responses to stimulation of any nerve. It is concluded that the adult locomotor system is capable of central reorganization to enhance specific remaining cutaneous reflex pathways after a partial cutaneous denervation of the paw.     

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.     

Motor functions in rat hindlimb muscles following neonatal sciatic nerve crush.

The sciatic nerve was crushed in the right hindlimb in newborn (3-8 h old) rats. Two to four months later, electromyographic activity was recorded from both the control and reinnervated ankle extensor muscles soleus or lateral gastrocnemius and from the ankle flexor muscle tibialis anterior. Tonic postural activity was present in the extensor muscles on both sides during quiet stance. The control flexor muscles were usually silent in this situation, but the reinnervated flexors exhibited abnormal sustained activity. During locomotion, the control extensors were activated during the stance phase and their mean burst made up 61.5% of the step cycle. The control tibialis anterior muscle fired only during the swing phase, with the burst lasting 18.1% of the step cycle. In the reinnervated extensor muscles, the mean burst duration was decreased (46% of the cycle) but the basic locomotor pattern was not impaired. The reinnervated tibialis muscle, however, was activated abnormally, with one appropriate flexor burst during the swing phase and an "extensor-like" burst during the stance phase of the step. Reflex responses to stretch were weak or absent on the operated side. Histological examination showed that the reinnervated soleus and tibialis muscles were almost devoid of muscle spindles. The motor unit mean firing rates in the reinnervated soleus (22 imp/s) and lateral gastrocnemius (45 imp/s) matched those of the control muscles (25 and 42 imp/s, respectively). In contrast to the phasic, high-frequency firing (52-80 imp/s) in the control tibialis, the reinnervated tibialis motor units fired at significantly lower rates (22-56 imp/s).(ABSTRACT TRUNCATED AT 250 WORDS)     

Cutaneous reflexes evoked during human walking are reduced when self-induced

Reflex responses are often less pronounced when they are self-induced, but this question has barely been investigated quantitatively. The issue is particularly relevant for locomotion since it has been shown that reflexes elicited during normal gait are important for the regulation of locomotion. The cortex is thought to be involved in the control of reflexes during gait, but it is unclear whether it plays a role in the modulation of these reflexes during the step cycle. During gait, weak electrical stimulation of the sural nerve elicits reflexes in various leg muscles. Are these reflexes different when subjects themselves trigger the stimuli instead of being randomly released by the computer? Cutaneous reflexes were elicited by sural nerve stimulation in 16 phases of the gait cycle in healthy subjects. The stimuli were triggered either by computer or by the subjects themselves. In 6 out of 7 subjects it was observed that the facilitatory responses in leg muscles were smaller and the suppressive responses were more suppressive following self-generated stimuli. In some muscles such as tibialis anterior (TA) both effects were seen (reduced facilitation at end stance and exaggerated suppression at end swing). In all subjects the modulation of anticipatory influences was muscle specific. In the main group of six subjects, the mean reduction in reflex responses was strongest in the TA (max. 30.7%; mean over 16 phases was 12.5%) and weakest in peroneus longus (PL, max. 10.1%; mean over 16 phases was 2.6%). The observation that facilitation is reduced and suppression enhanced in several muscles is taken as evidence that anticipation of self-induced reflex responses reduces the excitatory drive to motoneurones, for example through presynaptic inhibition of facilitatory reflex pathways.     

Stumbling corrective reaction: a phase-dependent compensatory reaction during locomotion.

1. Tactile stimuli to the paw consisting of a stick making contact or an air puff aimed at the dorsum were used to study the phasic influence of locomotor activity on the reflex pattern elicited in extensor and flexor muscles and on the induced compensatory movements in intact cats. The resulting movements and reflex pattern are called "stumbling corrective reactions." 2. The basic reflex pattern and movements of the stumbling corrective reaction are: a) if the stimulus occurs during the swing phase, a short-latency activation of the flexor muscles, which induces an additional flexion of the limb lifting the paw over the obstacle; b) if the stimulus occurs during the support phase, an inhibition followed by an excitation of the extensor muscles, which neither increase nor decrease the extension. However, the stimulus evokes an increased flexor activity in the succeeding swing phase, which induces a brisker flexion. 3. Tactile stimuli to the proximal part of the limb or to the belly in front of the knee evoked the same type of phase-dependent compensatory reactions. Such reactions would presumably be beneficial for the animal to avoid high obstacles that impede movement. 4. A nonnoxious electrical stimulus (typically 2 mA; 1 ms) applied to the dorsum of the paw was used to study systematically the reflex pattern of the stumbling corrective reaction. Two pathways were defined to the knee flexor (semitendinosus). One early burst was evoked at about 10 ms and one later at about 25 ms after the stimulus. Short inhibitory pathways and longer excitatory pathways (20-50 ms) projected to the extensor nuclei. A short-latency (10 ms) excitatory pathway to the ankle extensor (lateral gastrocnemius) was also activated. 5. A painful electrical stimulus applied to the dorsum of the paw evoked large flexor responses during the whole step cycle. During the support phase the locomotion was disrupted as the supporting limb was withdrawn. 6. The results demonstrate that intact cats are able to compensate rapidly for unpredicted perturbations and that the reflex pattern and the induced corrective movements are adapted to the locomotor activity so that functionally meaningful movements are evoked in each phase of the step cycle. 7. The evoked reflexes and their modulation are consistent with those previously found in chronic spinal cats during walking and in paralyzed spinal cats performing "fictive locomotion." It is suggested that the same spinal pathways are used, and that they are controlled by the spinal "locomotor generator."