Intracellular analysis of reflex pathways underlying the stumbling corrective reaction during fictive locomotion in the cat

In cat and humans, contact between an obstacle and the dorsum of the foot evokes the stumbling corrective reaction (reflex) that lifts the foot to avoid falling. This reflex can also be evoked by short trains of stimuli to the cutaneous superficial peroneal (SP) nerve in decerebrate cats during the flexion phase of fictive locomotion. Here we examine intracellular events in hindlimb motoneurons accompanying stumbling correction. SP stimulation delivered during the flexion phase excites knee flexor motoneurons at short latency [minimum excitatory postsynaptic potential (EPSP) latency 1.8 ms; mean 2.7 ms]. Although a similar short latency excitation occurs in ankle extensors (mean latency, 2.8 ms), recruitment is delayed until successive shocks in the stimulus train overcome the locomotor-related hyperpolarization of ankle extensors. In ankle flexor motoneurons, SP stimulation evokes an inhibition (mean latency, 2.7 ms) that briefly reduces or stops their firing during the flexion phase. There is a phase-dependent modulation of SP-evoked EPSP amplitude as well as latency during locomotion. However, the more obvious change in SP reflex pathways with the onset of fictive locomotion is the reduced inhibition of ankle extensor motoneurons and the increased inhibition of ankle flexors. These results show that the characteristic pattern of hindlimb motoneuron activation during SP nerve-evoked stumbling correction results from 1) di- and trisynaptic excitation of knee flexor and ankle extensor motoneurons; 2) increased inhibitory postsynaptic potentials in ankle flexors and a suppression of inhibition in extensors, 3) sculpting of the short-latency SP postsynaptic effects by motoneuron membrane potential, and 4) longer latency excitatory effects that are likely evoked by lumbar interneurons involved in the generation of fictive locomotion.     

Parallel reflex pathways from flexor muscle afferents evoking resetting and flexion enhancement during fictive locomotion and scratch in the cat

Reflex actions of muscle afferents in hindlimb flexor nerves were examined on ipsilateral motoneurone activity recorded in peripheral nerves during midbrain stimulation-evoked fictive locomotion and during fictive scratch in decerebrate cats. Trains of stimuli (15–30 shocks at 200 Hz) were delivered during the flexion phase at intensities sufficient to activate both group I and II afferents (5 times threshold, T ). In many preparations tibialis anterior (TA) nerve stimulation terminated ongoing flexion and reset the locomotor cycle to extension (19/31 experiments) while extensor digitorum longus (EDL) stimulation increased and prolonged the ongoing flexor phase activity (20/33 preparations). The effects of sartorius, iliopsoas and peroneus longus muscle afferent stimulation were qualitatively similar to those of EDL nerve. Resetting to extension was seen only with higher intensity stimulation (5 T ) while ongoing flexor activity was often enhanced at group I intensity (2 T ) stimulation. The effects of flexor nerve stimulation were qualitatively similar during fictive scratch. Reflex reversals were consistently observed in some fictive locomotor preparations. In those cases, EDL stimulation produced a resetting to extension and TA stimulation prolonged the ongoing flexion phase. Occasionally reflex reversals occurred spontaneously during only one of several stimulus presentations. The variable and opposite actions of flexor afferents on the locomotor step cycle indicate the existence of parallel spinal reflex pathways. A hypothetical organization of reflex pathways from flexor muscle afferents to the spinal pattern generator networks with competing actions of group I and group II afferents on the flexor and extensor portions of this central circuitry is proposed.     

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."     

Modulation of short latency cutaneous excitation in flexor and extensor motoneurons during fictive locomotion in the cat

Summary We examined modulation of transmission in short-latency, distal hindlimb cutaneous reflex pathways during fictive locomotion in 19 decerebrate cats. Fictive stepping was produced either by electrical stimulation of the mesencephalic locomotor region (MLR) or by administration of Nialamide and 1-DOPA to acutely spinalized animals. Postsynaptic potentials (PSPs) produced by electrical stimulation of low threshold afferents (< 2.5 times threshold) in the superficial peroneal (SP), sural, saphenous or medial plantar nerves were recorded intracellularly from various extensor (n = 28) and flexor (n = 24) motoneurons and averaged throughout the step cycle, together with voltage responses to intrasomatic constant current pulses (in order to monitor relative cell input resistance). Each motoneuron studied displayed rhythmic background oscillations in membrane potential and correlated variations in input resistance. The average input resistance of extensor motoneurons was lowest during mid-flexion, when the cells were relatively hyperpolarized and silent. Conversely, average input resistance of flexor motoneurons was highest during mid-flexion, when they were depolarized and active. The amplitude of the minimum-latency excitatory components of PSPs produced by cutaneous nerve stimulation were measured from computer averaged records representing six subdivisions of the fictive step cycle. Oligosynaptic EPSP components were consistently modulated only in the superficial peroneal responses in flexor motoneurons, which exhibited enhanced amplitude during the flexion phase. With the other skin nerves tested (sural, saphenous, and plantar), no consistent patterns of modulation were observed during fictive locomotion. We conclude that transmission through some, but not all, oligosynaptic excitatory cutaneous pathways is enhanced by premotoneuronal mechanisms during the flexion phase of fictive stepping in several cat hindlimb motor nuclei. The present results suggest that the patterns of interaction between the locomotor central pattern generator and excitatory cutaneous reflex pathways depend on the source of afferent input and on the identity of the target motoneuron population.     

The role of cutaneous afferents from the distal hindlimb in the regulation of the step cycle of thalamic cats

Summary The pad and the plantar surface of the foot were stimulated electrically in thalamic cats. Weak stimulation evoked an extensor reflex in the animal at rest. The same stimuli in a spontaneously walking animal applied during the stance phase produced an increase both in amplitude and duration of the ongoing extensor activity. When given during the swing phase, the stimuli either prolonged the ongoing flexor activity and/or shortened the following extensor burst. These changes in flexor and extensor burst duration were reflected in changes in the step cycle duration.Similar results were seen with direct stimulation of the sural nerve. For the latter experiments the ipsilateral hindlimb was fixed and denervated except for the ankle extensors and flexors, which showed rhythmic contractions correlated normally with the walking movements of the three remaining limbs. At rest, threshold stimulation of the sural nerve evoked a reflex contraction in the triceps surae of the fixed leg. The same stimuli applied during the contraction phase of the fixed triceps surae during walking resulted in a larger and longer extensor contraction and a delay of the following flexion. Stimulation during the relaxation phase of the fixed triceps surae reduced the duration of the following contraction phase. The findings are discussed in relation to the possible role of cutaneous input during locomotion.     

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.     

Phase-dependent transmission in the excitatory propriospinal reflex pathway from forelimb afferents to lumbar motoneurones during fictive locomotion

In high spinal paralyzed cats the effect of forelimb nerve stimulation on hindlimb motoneurones was investigated during fictive locomotion, which was induced by injection of nialamide and L-DOPA. The EPSPs which were evoked by forelimb nerve stimulation in almost all species of hindlimb motoneurones showed a distinct dependence on the phase of the step cycle. In motoneurones to extensor they were only observed during the extension phase, in those to flexors only during the flexion phase. It is assumed that the transmission in the descending propriospinal excitatory reflex pathway is cyclically modulated at the lumbar level.     

Ia inhibitory interneurons and Renshaw cells as contributors to the spinal mechanisms of fictive locomotion

The activity of selected single alpha-motoneurons, Renshaw cells (RCs), and Ia inhibitory interneurons (IaINs) during fictive locomotion was recorded via microelectrodes in decerebrate (precollicular-postmammillary) cats in which fictive locomotion was induced by stimulation of the mesencephalic locomotor region. The interrelationships in the timing and frequency of discharge among these three interconnected cell types were determined by comparing their averaged step cycle firing histograms, which were normalized in reference to motoneuron activity recorded in ventral root filaments. Previous findings that RCs are rhythmically active during locomotion and discharge in phase with the motoneurons from which they are excited were confirmed, and further details of the phase relationships between RC and alpha-motoneuron activity during fictive locomotion were obtained. Flexor and extensor RCs became active after the onset of flexor and extensor motoneuron activity, respectively. Maximal activity in extensor RCs occurred at the end of the extension phase coincidental with the onset of hyperpolarization and a decrease in activity in extensor motoneurons. Maximal flexor RC activity occurred during middle to late flexion and was temporally related to the onset of reduced flexor motoneuron activity. The IaINs recorded in the present experiments were rhythmically active during fictive locomotion, as previously reported. The quadriceps IaINs were mainly active during the extension phase of the step cycle, along with extensor RCs. Thus the known inhibition of quadriceps IaINs by RCs coupled to quadriceps and other extensor motoneurons is obviously not sufficient to interfere with the appropriate phasing of IaIN activity and reciprocal inhibition during fictive locomotion, as had been speculated. Most of the quadriceps IaINs analyzed exhibited a decrease in discharge frequency at the end of the extension phase of the step cycle, which was coincidental with increased rates of firing in extensor RCs. These data are consistent with the possibility that extensor RCs contribute to the reduction in quadriceps IaIN discharge at the end of the extension phase of the step cycle. The possibility that IaIN rhythmicity during fictive locomotion arises from periodic inhibition, possibly from Renshaw cells, was tested by stimulating the reciprocal inhibitory pathway throughout the fictive step cycle. The amplitude of Ia inhibitory postsynaptic potentials (IPSPs) varied significantly throughout the fictive step cycle in 14 of the 17 motoneurons tested, and, in 11 of these 14 motoneurons, the Ia IPSPs were maximal during the phase of the step cycle in which the motoneuron was most     

Phasic modulation of short latency cutaneous excitation in flexor digitorum longus motoneurons during fictive locomotion

Summary We examined modulation of transmission of short-latency excitation produced by distal hindlimb cutaneous input, as well as fluctuations in motoneuron membrane potential and input resistance, in flexor digitorum longus (FDL) motoneurons during fictive locomotion. Fictive stepping was induced in unaesthetized, decerebrate cats either by repetitive stimulation of the mesencephalic locomotor region (MLR) or by administration of Nialamide and 1 DOPA after low spinal section. In the MLR preparations, brief depolarizing waves occurred in FDL cells during the early flexion phase of fictive stepping, immediately after cessation of activity in extensor muscles. In some FDL cells, plateau-like depolarizations also occurred during the extensor phase. Fictive stepping induced in acutely spinalized cats by administration of l-DOPA was slower and more variable; peak polarization in FDL motoneurons always occurred during the early flexion phase but there was usually no distinct depolarization during extension. In both types of preparation, the initial EPSP components in synaptic potentials (SP-EPSPs) produced by electrical stimulation of the cutaneous division of the superficial peroneal nerve (SP) were maximally facilitated during early flexion, coincident with the peak of background depolarization. This enhancement was manifested by an increase in the amplitude of initial SP-EPSP components or by decreased central latency of the initial EPSP components, or both. In most FDL motoneurons, input resistance decreased systematically during late flexion, coincident with relative membrane hyperpolarization. Correction of SP-EPSP amplitudes for changes in input resistance suggested that SP-EPSP facilitation persisted throughout the flexion phase These findings are discussed with reference to modulation of cutaneous reflexes during locomotion and the possibility that excitatory last-order interneurons in particular cutaneous reflex pathways may distribute excitatory drive from the central pattern generator for locomotion to FDL -motoneurons     

Proprioceptive input resets central locomotor rhythm in the spinal cat

Summary The reflex regulation of stepping is an important factor in adapting the step cycle to changes in the environment. The present experiments have examined the influence of muscle proprioceptors on centrally generated rhythmic locomotor activity in decerebrate unanesthetized cats with a spinal transection at Th12. Fictive locomotion, recorded as alternating activity in hindlimb flexor and extensor nerves, was induced by administration of nialamide (a monoamine oxidase inhibitor) and L-DOPA. Brief electrical stimulation of group I afferents from knee and ankle extensors were effective in resetting fictive locomotion in a coordinated fashion. An extensor group I volley delivered during a flexor burst would abruptly terminate the flexor activity and initiate an extensor burst. The same stimulus given during an extensor burst prolonged the extensor activity while delaying the appearance of the following flexor burst. Intracellular recordings from motoneurones revealed that these actions were mediated at premotoneuronal levels resulting from a distribution of inhibition to centres generating flexor bursts and excitation of centres generating extensor bursts. These results indicate that extensor group I afferents have access to central rhythm generators and suggest that this may be of importance in the reflex regulation of stepping. Experiments utilizing natural stimulation of muscle receptors demonstrate that the group I input to the rhythm generators arises mainly from Golgi tendon organ Ib afferents. Thus an increased load of limb extensors during the stance phase would enhance and prolong extensor activity while simultaneously delaying the transition to the swing phase of the step cycle.     

Locomotor activities in the decerebrate bird without phasic afferent input

We examined whether forelimb and hindlimb phasic afferent input is a prerequisite for the production of avian locomotor patterns. We eliminated phasic afferent feedback through paralysis of a decerebrate animal. The term "fictive" has been used to describe the neural activity associated with spontaneous or evoked motor output during neuromuscular paralysis. We observed that a paralysed decerebrate bird is capable of producing similar locomotor activity patterns as an unparalysed preparation, regardless of whether the "fictive" locomotion is generated spontaneously, or in response to focal electrical and/or neurochemical stimulation of discrete brainstem locomotor regions. Not all aspects of "fictive" locomotor patterns were identical to the locomotion elicited prior to paralysis. The stimulus current threshold necessary to evoke hindlimb locomotion increased from 69 +/- 22 mu A (mean +/- S.D.) prior to paralysis to 185 +/- 87 mu A for "fictive" stepping. For wing activity, the threshold increased from 84 +/- 46 mu A during wing flapping to 228 +/- 148 mu A for "fictive" flight. In addition, the frequency of "fictive" efferent locomotor activity from the leg nerve (1.04 +/- 0.44 Hz) decreased relative to the frequency of leg activity prior to paralysis (1.55 +/- 0.70 Hz). Similarly, the frequency of wing activity decreased from 2.73 +/- 0.73 Hz before paralysis to 1.8 +/- 0.69 Hz after paralysis. Finally flexor burst duration remained constant during treadmill and "fictive" walking while the extensor burst duration was markedly increased during "fictive" walking. Thus, the relative contributions of leg flexor activity to the overall step cycle (burst proportion = burst duration/cycle duration) decreased during evoked "fictive" stepping, while the burst proportion of the leg extensor increased. Afferent feedback therefore appears to modulate leg extensor burst duration more than leg flexor duration. For the wings, the burst proportion of the major wing depressors remained constant before and after paralysis.     

Deletions of rhythmic motoneuron activity during fictive locomotion and scratch provide clues to the organization of the mammalian central pattern generator

We examined the features of spontaneous deletions of bursts of motoneuron activity that can occur within otherwise rhythmic alternating flexor and extensor activity during fictive locomotion and scratch in adult decerebrate cats. Deletions of activity were observed both in hindlimb flexor and extensor motoneuron pools during brain stem-stimulation-evoked fictive locomotion but only in extensors during fictive scratch. Paired intracellular motoneuron recordings showed that deletions reduced the depolarization of homonymous motoneurons in qualitatively similar ways. Differences occurred in the extent to which activity in synergist motoneuron pools operating at other joints within the limb was reduced during deletions. The timing of the rhythmic activity that followed a deletion was often at an integer multiple of the preexisting locomotor or scratch cycle period. This maintenance of cycle period was also seen during deletions in which there was a complete failure of motoneuron depolarization. The activity of antagonist motoneurons was usually sustained during deletions with some rhythmic modulation at intervals of the preexisting cycle period. We discuss an organization of the central pattern generator for locomotion and scratch that functions as a single rhythm generator with separate and multiple pattern formation modules for controlling the hyper- and depolarization of subsets of motoneurons within the limb.     

Activity of interneurons within the L4 spinal segment of the cat during brainstem-evoked fictive locomotion

Summary Extracellular recordings from interneurons located in the L4 spinal segment were made during fictive locomotion produced by electrical stimulation of the mesencephalic locomotor region (MLR) in the paralysed decerebrate cat. Only interneurons within the L4 segment which received group II input from quadriceps, sartorius or the pretibial flexor muscle afferents and which had axonal projections to motor nuclei in L7 were selected for analysis. During the fictive step cycle two thirds of these interneurons fired action potentials during the time of activity in the ipsilateral hindlimb flexor neurograms. These cells were also less responsive to peripheral input during the extension phase of the fictive locomotion cycle. The remaining one third of the interneurons examined were not rhythmically active during locomotion. The possible contributions of the midlumbar interneurons to motoneuron activity during locomotion are discussed.     

Simultaneous control of two rhythmical behaviors. II. Hindlimb walking with paw-shake response in spinal cat

The simultaneous control of the hindlimb paw-shake response and hindlimb walking at slow treadmill speeds (0.2-0.4 m/s) was examined in adult cats spinalized at the T12 level, 3-6 mo earlier. Paw shaking was elicited by either 1) application of adhesive tape or 2) water to the right hindpaw. To assess intralimb and interlimb coordination of the combined behaviors, activity from selected flexor and extensor muscles at the hip, knee, and ankle was recorded, and the kinematics of these joints were determined from high-speed cinefilm. When paw shaking was combined with hindlimb walking, the response in the stimulated limb was initiated during swing (F phase) of the step cycle. The onset of knee extensor activity provided the transition from the flexor synergy of swing to the mixed synergy of paw shake. At the end of the paw shake, an extensor synergy initiated the E-1 phase of swing, and the resultant joint motion was in-phase extension at the hip, knee, and ankle to lower the paw for contact with the treadmill belt. During the rapid (81 ms) paw-shake cycles, knee extensor and ankle flexor muscles exhibited single, coactive bursts that were reciprocal with coactive hip and ankle extensor bursts. This mixed synergy was reflected in the limb coordination, as knee flexion coincided with ankle extension and knee flexion coincided with ankle extension. Phasing of hip motions was variable, reflecting the role of the proximal in stabilization during paw shake (16). Although the number of paw-shake cycles combined during swing varied greatly from 2 to 14, average cycle periods, burst durations, and intralimb synergies were similar to those previously reported for spinal cats tested under conditions in which the trunk was suspended and hindlimbs were pendent (23, 27). For step cycles during which a long paw-shake response of 8-14 cycles occurred, swing duration of the shaking limb increased by 1 s, and during this prolonged interval, the contralateral hindlimb completed two support steps. Stance duration of the support steps was also prolonged. This adjustment maximized the duration of paw-contact and minimized any period of nonsupport by the contralateral hindlimb during paw shake. Completion of the paw-shake response was followed by either an alternating, or a nonalternating, gait pattern on the recovery steps. One spinal cat combined locomotion with short two-cycle paw-shake responses, and because the shortened response was limited primarily to the time ordinarily devoted to swing, interlimb adjustments were slight.(ABSTRACT TRUNCATED AT 400 WORDS)     

Ascending long spinal actions on forelimb motoneurons in the acute spinal cat

Ascending long spinal reflex system were investigated by means of monosynaptic reflex testing in the acutely spinalized unanesthetized cat. 1.Hindlimb nerve stimulation gave bilateral facilitatory effects on the motoneuron pools of pectoralis major and physiological flexors of the forelimb such as biceps brachii, extensor carpi radialis, extensor digitorum communis, but elicited depressive effects on the physiological extensors such as triceps brachii, flexor carpi radialis, flexor digitorum profundus. 2. In the latissimus dorsi, which is the antagonist of pectoralis major, a depressive effect was elicited by the stimulation of ipsilateral hindlimb nerves, and a facilitatory effect by contralateral stimulation. 3. These effects were evoked mainly from group II afferent fibers in muscle as well as cutaneous nerves. 4. Intracellular recordings from motoneurons of extensor carpi radialis revealed EPSPs following stimulation of hindlimb nerves with time courses corresponding to those of the facilitatory effects. We failed to detect any potential changes in the motoneurons of flexor carpi radialis following stimulation of hindlimb nerves.     

Reciprocal interactions in the turtle hindlimb enlargement contribute to scratch rhythmogenesis.

We examined interactions between the spinal networks that generate right and left rostral scratch motor patterns in turtle hindlimb motoneurons before and after transecting the spinal cord within the anterior hindlimb enlargement. Our results provide evidence that reciprocal inhibition between hip circuit modules can generate hip rhythmicity during the rostral scratch reflex. "Module" refers here to the group of coactive motoneurons and interneurons that controls either flexion or extension of the hip on one side and coordinates that activity with synergist and antagonist motor pools in the same limb and in the contralateral limb. The "bilateral shared core" hypothesis states that hip flexor and extensor (HF and HE) circuit modules interact via crossed and uncrossed spinal pathways: HF modules make reciprocal inhibitory connections with contralateral HF and ipsilateral HE modules and mutual excitatory connections with contralateral HE modules. It is currently unclear how much reciprocal inhibition between modules contributes to scratch rhythmogenesis. To address this issue, fictive scratch motor patterns were recorded bilaterally as electroneurograms from HF, HE, knee extensor (KE), and respiratory (d.D8) muscle nerves in immobilized animals. D3-end (low-spinal) preparations had intact spinal cords posterior to a complete D2-D3 transection. Unilateral stimulation of rostral scratch in D3-end turtles elicited rhythmic alternation between ipsilateral HF and HE bursts in most cycles; consecutive HF bursts were separated by complete silent (HF-OFF ) periods. D3-D9 and D3-D8 preparations received a second spinal transection at the caudal end of segment D9 or D8, respectively, within the anterior hindlimb enlargement. This second transection disconnected most HE circuitry (located mainly in segments D10-S2 of the posterior enlargement) from the rostral scratch network and thereby reduced the HE-associated inhibition of HF circuitry. Unilateral stimulation of rostral scratch in most D3-D9 and D3-D8 preparations evoked rhythmic or weakly modulated ipsilateral HF discharge without HF-OFF periods between bursts and without ipsilateral HE activity in the majority of cycles. In contrast, bilateral stimulation in D3-D9 and D3-D8 preparations reconstructed the HF-OFF periods, increased HF rhythmicity (assessed by fast Fourier transform power spectra and autocorrelation analyses), and reestablished weak HE-phase motoneuron activity. We suggest that bilateral stimulation produced these effects by simultaneously activating reciprocally inhibitory hip modules on opposite sides (right and left HF) and the same side (HF and residual ipsilateral HE circuitry). Our data support the hypothesis that reciprocal inhibition can contribute to spinal rhythmogenesis during the scratch reflex.     

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)     

Adaptive control for backward quadrupedal walking. II. Hindlimb muscle synergies

1. To compare the basic hindlimb synergies for backward (BWD) and forward (FWD) walking, electromyograms (EMG) were recorded from selected flexor and extensor muscles of the hip, knee, and ankle joints from four cats trained to perform both forms of walking at a moderate walking speed (0.6 m/s). For each muscle, EMG measurements included burst duration, burst latencies referenced to the time of paw contact or paw off, and integrated burst amplitudes. To relate patterns of muscle activity to various phases of the step cycle, EMG records were synchronized with kinematic data obtained by digitizing high-speed ciné film. 2. Hindlimb EMG data indicate that BWD walking in the cat was characterized by reciprocal flexor and extensor synergies similar to those for FWD walking, with flexors active during swing and extensors active during stance. Although the underlying synergies were similar, temporal parameters (burst latencies and durations) and amplitude levels for specific muscles were different for BWD and FWD walking. 3. For both directions, iliopsoas (IP) and semitendinosus (ST) were active as the hip and knee joints flexed at the onset of swing. For BWD walking, IP activity decreased early, and ST activity continued as the hip extended and the knee flexed. For FWD walking, in contrast, ST activity ceased early, and IP activity continued as the hip flexed and the knee extended. For both directions, tibialis anterior (TA) was active throughout swing as the ankle flexed and then extended. A second ST burst occurred at the end of swing for FWD walking as hip flexion and knee extension slowed for paw contact. 4. For both directions, knee extensor (vastus lateralis, VL) activity began at paw contact. Ankle extensor (lateral gastrocnemius, LG) activity began during midswing for BWD walking but just before paw contact for FWD walking. At the ankle joint, flexion during the E2 phase (yield) of stance was minimal or absent for BWD walking, and ankle extension during BWD stance was accompanied by a ramp increase in LG-EMG activity. At the knee joint, the yield was also small (or absent) for BWD walking, and increased VL-EMG amplitudes were associated with the increased range of knee extension for BWD stance. 5. Although the uniarticular hip extensor (anterior biceps femoris, ABF) was active during stance for both directions, the hip flexed during BWD stance and extended during FWD stance.(ABSTRACT TRUNCATED AT 400 WORDS)     

Scratch responses in normal cats: hindlimb kinematics and muscle synergies

1. Scratch responses evoked by a tactile stimulus applied to the outer ear canal were characterized in nine adult cats. Chronic electromyographic (EMG) electrodes were surgically implanted in selected flexor and extensor muscles of the hip, knee, and ankle joints to determine patterns of muscle activity during scratching. In some trials EMG records were synchronized with kinematic data obtained by digitizing high-speed ciné film, and in one cat, medial gastrocnemius (MG) tendon forces were recorded along with EMG. For analysis the response was divided into three components: the approach, cyclic, and return periods. Usually scratch responses were initiated with the cat in a sitting position, but in some trials the animal initiated the response from a standing or lying posture. 2. During the approach period the hindlimb ipsilateral to the stimulated ear was lifted diagonally toward the head by a combination of hip and ankle flexion with knee extension. Hindlimb motions during the approach period were associated with sustained EMG activity in hip-flexor, knee-extensor (occasionally), and ankle-flexor muscles. Initial hindlimb motions were typically preceded by head movements toward the hindpaw, and at the end of the approach period, the head was tilted downward with the stimulated pinna lower than the contralateral ear. During the return period movements were basically the reverse of the approach period, with the hindpaw returning to the ground and the head moving away from the hindlimb. 3. During the cyclic period the number of cycles per response varied widely from 1 to 60 cycles with an average of 13 cycles, and cycle frequency ranged from 4 to 8 cycles/s, with a mean of 5.6 cycles/s. During each cycle the paw trajectory followed a fairly circular path, and the cycle was defined by three phases: precontact, contact, and postcontact. On average the contact phase occupied approximately 50% of the cycle and was characterized by extensor muscle activity and extension at the hip, knee, and ankle joints. The hindpaw contacted the pinna or neck at the base of the pinna throughout the contact phase, and paw contact typically resulted in a rostral motion of the head as the hindlimb extended. 4. The postcontact phase constituted approximately 24% of scratch cycle and was usually initiated by the onset of knee flexion. Ankle and then hip flexion followed knee flexion, and flexor muscles were active during the postcontact phase as the paw was withdrawn from the head. The precontact phase constituted approximately 26% of scratch cycle and was initiated by knee joint extension and knee-extensor activity.(ABSTRACT TRUNCATED AT 400 WORDS)     

Proprioceptive modulation of hip flexor activity during the swing phase of locomotion in decerebrate cats

This study examined the influence of proprioceptive input from hip flexor muscles on the activity in hip flexors during the swing phase of walking in the decerebrate cat. One hindlimb was partially denervated to remove cutaneous input and afferent input from most other hindlimb muscles. Perturbations to hip movement were applied either by 1) manual resistance or assistance to swing or by 2) resistance to hip flexion using a device that blocked hip flexion but allowed leg extension. Electromyographic recordings were made from the iliopsoas (IP), sartorius, and medial gastrocnemius muscles. When the hip was manually assisted into flexion, there was a reduction in hip flexor burst activity. Conversely, when hip flexion was manually resisted or mechanically blocked during swing, the duration and amplitude of hip flexor activity was increased. We also found some specificity in the role of afferents from individual hip flexor muscles in the modulation of flexor burst activity. If the IP muscle was detached from its insertion, little change in the response to blocking flexion was observed. Specific activation of IP afferent fibers by stretching the muscle also did not greatly affect flexor activity. On the other hand, if conduction in the sartorius nerves was blocked, there was a diminished response to blocking hip flexion. The increase in duration of the flexor bursts still occurred, but this increase was consistently lower than that observed when the sartorius nerves were intact. From these results we propose that during swing, feedback from hip flexor muscle afferents, particularly those from the sartorius muscles, enhances flexor activity. In addition, if we delayed the onset of flexor activity in the contralateral hindlimb, blocking hip flexion often resulted in the prolongation of ipsilateral flexor activity for long periods of time, further revealing the reinforcing effects of flexor afferent feedback on flexor activity. This effect was not seen if conduction in the sartorius nerves was blocked. In conclusion, we have found that hip flexor activity during locomotion can be strongly modulated by modifying proprioceptive feedback from the hip flexor muscles.