Corticospinal control of locomotor pathways generating extensor activities in the cat

Interneuronal convergence of corticospinal and segmental pathways involved with the generation of extensor activities during locomotion was investigated in decerebrate and partially spinalized cats. L-dihydroxyphenylalanine (L-DOPA) was slowly injected until long-latency, long-lasting discharges could be evoked by the stimulation of contralateral flexor reflex afferents (coFRA) and the group I autogenetic inhibition was reversed to polysynaptic excitation in extensor motoneurons. Under these conditions, we stimulated in alternation the contralateral pyramidal tract (PT), group I afferents from knee and ankle extensor muscles, and both stimuli together. We did the same for the stimulation of PT and of coFRA. Clear polysynaptic EPSPs could be evoked from all three sources in 32 extensor motoneurons. Convergence was inferred from spatial facilitation, which occurred when the amplitude of the EPSPs evoked by the combined stimuli was notably larger than the algebraic sum of the EPSPs evoked by individual stimulation. Spatial facilitation was found between PT and extensor group I inputs in 30/59 tests (51%) in 20 motoneurons and in all cases (6/6) between PT and coFRA in six motoneurons. When fictive locomotion was induced with further injection of L-DOPA, PT descending volleys from the same stimulating site could reset the stepping rhythm by initiating bursts of activity in all extensors. These results indicate that at least some of the corticospinal fibers project onto interneurons shared by the coFRA and the polysynaptic excitatory group I pathways to extensors. The implications of such convergence patterns on the organization of the extensor "half-center" for locomotion are discussed.     

Entrainment of the locomotor rhythm by group Ib afferents from ankle extensor muscles in spinal cats

Summary 1. Previous studies have concluded that the timing of the locomotor rhythm can be strongly influenced by input from group Ib afferents from leg extensor muscles (Duysens and Pearson 1980; Conway et al. 1987). The main objective of the present study was to obtain additional evidence for this conclusion by examining the characteristics of entrainment of the locomotor rhythm by rhythmic stimulation of group I afferents and by rhythmic force pulses in the ankle extensor muscles. 2. A reduced, non-immobilized preparation was developed in spinal cats that allowed isometric contractions of ankle extensor muscles to be elicited by ventral root stimulation during the expression of locomotor activity. The same preparation was used to examine the influence of electrically stimulating group I afferents from the ankle extensors and the effect of rhythmically stretching these muscles. The locomotor rhythm was initiated by sustained mechanical stimulation of the perineum following the administration of Clonidine and, in some preparations, Naloxone. 3. The timing of the onset of flexor burst activity was examined during entrainment with saw-tooth and ramp-and-hold stretches of the ankle extensor muscles. Flexor bursts were initiated about 200 ms following the release from the stretch, and this latency was independent of the entrainment frequency. 4. The locomotor rhythm was readily entrained by rhythmic contractions of the ankle extensor muscles produced by ventral root stimulation provided the magnitude of the contractions was greater than about 10N. Repetitive stimulation of group I muscle afferents from the ankle extensors also entrained the locomotor rhythm, with the timing of motor activity being similar to that during entrainment with rhythmic muscle contractions. Burst activity in the ipsilateral extensors was coincident with the stimulus trains in both cases. This similarity argues for entrainment being produced mainly by input from group Ib afferents. 5. The functional implication of the results of this and previous studies is that input from group Ib afferents during the stance phase of walking acts to inhibit generation of flexor burst activity and to promote extensor activity. The proposal that a decline in Ib activity near the end of the stance phase is involved in regulating the stance to swing transition is discussed.CRSN, Physiologie, Faculte de Medecine, C.P. 6128, succursal A, Montréal, Quebec, Canada, H3C 3J7     

Modelling spinal circuitry involved in locomotor pattern generation: insights from the effects of afferent stimulation

A computational model of the mammalian spinal cord circuitry incorporating a two-level central pattern generator (CPG) with separate half-centre rhythm generator (RG) and pattern formation (PF) networks has been developed from observations obtained during fictive locomotion in decerebrate cats. Sensory afferents have been incorporated in the model to study the effects of afferent stimulation on locomotor phase switching and step cycle period and on the firing patterns of flexor and extensor motoneurones. Here we show that this CPG structure can be integrated with reflex circuits to reproduce the reorganization of group I reflex pathways occurring during locomotion. During the extensor phase of fictive locomotion, activation of extensor muscle group I afferents increases extensor motoneurone activity and prolongs the extensor phase. This extensor phase prolongation may occur with or without a resetting of the locomotor cycle, which (according to the model) depends on the degree to which sensory input affects the RG and PF circuits, respectively. The same stimulation delivered during flexion produces a temporary resetting to extension without changing the timing of following locomotor cycles. The model reproduces this behaviour by suggesting that this sensory input influences the PF network without affecting the RG. The model also suggests that the different effects of flexor muscle nerve afferent stimulation observed experimentally (phase prolongation versus resetting) result from opposing influences of flexor group I and II afferents on the PF and RG circuits controlling the activity of flexor and extensor motoneurones. The results of modelling provide insights into proprioceptive control of locomotion.     

Transmission in a locomotor-related group Ib pathway from hindlimb extensor muscles in the cat

It has been previously shown that phasic stimulation of group I afferents from ankle and knee extensor muscles may entrain and/or reset the intrinsic locomotor rhythm; these afferents are thus acting on motoneurones through the spinal rhythm generators. It was also concluded that the major part of these effects originates from Golgi tendon organ Ib afferents. Transmission in this pathway to lumbar motoneurones has now been investigated during fictive locomotion in spinal cats injected with nialamide and l-DOPA, and in decerebrate cats with stimulation of the mesencephalic locomotor region. In spinal cats injected with nialamide and l-DOPA, it was possible to evoke long-latency, long-lasting reflexes upon stimulation of high threshold afferents before spontaneous fictive locomotion commenced. During that period, stimulation of ankle and knee extensor group I afferents evoked oligosynaptic excitation of extensor motoneurones, rather than the classical Ib inhibition. Furthermore, a premotoneuronal convergence (spatial facilitation) between this group I excitation and the crossed extensor reflex was established. During fictive locomotion, in both preparations, the transmission in these group I pathways was phasically modulated within the step cycle. During the flexor phase, the group I input cut the depolarised (active) phase in flexor motoneurones and evoked EPSPs in extensor motoneurones; during the extensor phase, the group I input evoked smaller EPSPs in extensor motoneurones and had virtually no effect on flexor motoneurones. The above results suggest that the group I input from extensor muscles is transmitted through the spinal rhythm generator and more particularly, through the extensor half-centre. The locomotor-related group I excitation had a central latency of 3.5–4.0 ms. The excitation from ankle extensors to ankle extensors remained after a spinal transection at the caudal part of L6 segment; the interneurones must therefore be located in the L7 and S1 spinal segments. Candidate interneurones for mediating these actions were recorded extracellularly in lamina VII of the 7th lumbar segment. Responses to different peripheral nerve stimulation (high threshold afferents and group I afferents bilaterally) were in concordance with the convergence studies in motoneurones. The interneurones were rhythmically active in the appropriate phases of the fictive locomotor cycle, as predicted by their response patterns. The synaptic input to, and the projection of these candidate interneurones must be fully identified before their possible role as components of the spinal locomotor network can be evaluated.     

Flexor reflex afferents reset the step cycle during fictive locomotion in the cat

 The generation of locomotor-like spinal rhythms has been proposed to involve two neural centres with mutual reciprocal inhibition (Graham Brown’s ”half-centre” hypothesis). Much later a particular set of segmental flexor reflex pathways were described as being organized in accordance with this half-centre hypothesis. As these pathways became operative following injection of monoaminoxidase inhibitors and l-3,4-dihydroxyphenylalanine (l-dopa), i.e. under the same conditions under which a spontaneous locomotor activity may develop, it was assumed that these particular pathways and spinal rhythm generators involve the same neuronal networks. In order to give further evidence to this hypothesis, we investigated whether short trains to ”flexor reflex afferents” (FRA) reset the spinal locomotor rhythm, i.e. shorten or lengthen the stimulated cycle after which the regular rhythm is resumed with step cycles of the original duration. The experiments were performed in anaemically decapitated, high-spinal curarized cats. A steady locomotor rhythm was induced by injection of nialamide and l-dopa and the influence of electrical stimulation (trains of 50–1000 ms) of FRA (joint, cutaneous, and group II and III muscle afferents) onto this rhythm was tested. Stimulation of FRA induced a clear resetting of the locomotor rhythm, which was mainly characterized by a flexion reflex pattern: during the extension phase the extensor activity was interrupted and a flexion phase was initiated; during the late flexion phase mainly a prolongation of that phase with a variable change of the following extension phase was induced. In addition to this prevailing pattern, stimulation of some nerves (in particular nerves to more distal extensors and the sural nerve) could often prolong extension, when stimulated during the late extension, or terminate the flexor burst and initiate a new extension phase, when stimulated during the late flexion phase. This pattern is probably due to the concomitant stimulation of group I afferents in the case of the muscle nerves and to separate non-FRA pathways in the case of the sural nerve. The results demonstrate that the interneurones of the FRA pathways, which are operative during l-dopa-induced locomotion in spinal animals, can be considered as neuronal elements of the rhythm-generating network for locomotion. Received: 25 June 1996 / Accepted: 27 April 1998     

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.     

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.     

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.     

Toe flexor muscle spindle discharge and stretch modulation during locomotor activity in the decerebrate cat

In order to investigate the nature (i.e. static or dynamic) of fusimotor drive to the flexor hallucis longus (FHL) and flexor digitorum longus (FDL) muscles during locomotion we recorded Ia and group II muscle spindle afferent responses to sinusoidal stretch (0.25 and 1 mm amplitude, respectively, 4–5 Hz) in a decerebrate cat preparation. FHL Ia and group II afferents generally had increased discharge rates and decreased modulation to stretch throughout the step cycle, compared to rest, suggesting raised static γ drive at all locomotor phases. Although the modulation of Ia afferents was reduced during locomotion, most (13 of 18) showed a clear increasing trend during homonymous muscle activity (extension). This was consistent with phasic dynamic γ drive to FHL spindles linked with α drive. In agreement with previous reports, FHL gave a single burst of EMG activity during the step cycle while FDL α drive had two components. One was related to extension while the other comprised a brief burst around the end of this phase. Typically FDL Ia and group II afferents also had elevated firing rates and reduced modulation at all locomotor phases, again implicating static γ drive. Half the afferents (seven Ia, three group II) showed increased discharge during extension, suggesting phasic static γ drive. There was no γ drive associated with the late FDL α burst. In conclusion, the γ drives to FHL and FDL differed during locomotion. FHL, which has the α drive of a classic extensor, received γ drive that closely resembled other extensors. The γ drive of FDL, which exhibits both extensor and flexor α synergies, did not match either muscle type. These observations are compatible with the view that fusimotor drive varies in different muscles during locomotion according to the prevailing sensorimotor requirements.     

Peripheral control of the cat's step cycle

Acute low spinal and curarized cats injected with noradrenergic agonists i.v. can elicit an efferent burst pattern which can be recorded in muscle nerve filaments and can be referred to as “fictive locomotion”. This study investigates the effect that feedback, arising from movements in the hip joint, can exert on the central network generating fictive locomotion. The central network is uncoupled from generating any active movements by curarization. The motor pattern could be entrained by applying sinusoidal hip movements, even when a very extensive denervation of the leg had been performed leaving only some of the muscles around the hip and the hip joint innervated. During flexion movements, efferents to different flexor muscles became active and during movements in the reverse direction (extension), efferents to extensors were active. With an increasing movement frequency the onsets of both flexor and extensor bursts were delayed in the movement cycle. The duration of the extensor bursts varied markedly with the movement cycle, whereas pure flexors changed less in burst duration. The frequency range within which the efferent burst activity was entrained in a strict 1:1 relation to the movement varied between 5 to 70% above and below the resting burst period. In preparations with a narrow 1:1 range, a “relative coordination” was encountered outside this range. The flexor burst duration was in these cases dependent on where in the hip movement cycle the bursts appeared.     

Peripheral control of the cat's step cycle. II. Entrainment of the central pattern generators for locomotion by sinusoidal hip movements during "fictive locomotion."

Acute low spinal and curarized cats injected with noradrenergic agonists i.v. can elicit an efferent burst pattern which can be recorded in muscle nerve filaments and can be referred to as "fictive locomotion". This study investigates the effect that feedback, arising from movements in the hip joint, can exert on the central network generating fictive locomotion. The central network is uncoupled from generating any active movements by curarization. The motor pattern could be entrained by applying sinusoidal hip movements, even when a very extensive denervation of the leg had been performed leaving only some of the muscles around the hip and the hip joint innervated. During flexion movements, efferents to different flexor muscles became active and during movements in the reverse direction (extension), efferents to extensors were active. With an increasing movement frequency the onsets of both flexor and extensor bursts were delayed in the movement cycle. The duration of the extensor bursts varied markedly with the movement cycle, whereas pure flexors changed less in burst duration. The frequency within which the efferent burst activity was entrained in a strict 1:1 relation to the movement varied between 5 to 70% above and below the resting burst period. In preparations with a narrow 1:1 range, a "relative coordination" was encountered outside this range. The flexor burst duration was in these cases dependent on where in the hip movement cycle the bursts appeared.     

Development in neonatal rats of the sensory resetting of the locomotor rhythm induced by NMDA and 5-HT

 Developmental changes in the effects of quadriceps (Q) nerve stimulation on the locomotor rhythm induced by a mixture of N-methyl-d-aspartic acid and 5-hydroxytryptamine were examined using in vitro preparations from neonatal rats at postnatal days (P) 1–6. The effects of such stimulation on the rhythm were dependent both on stimulus strength and on the age of the animal. Low-intensity stimulation (≤3.0×T, where T=threshold for the monosynaptic reflex) during the flexor phase reset the rhythm via a prolongation of the flexor burst in most rats at P1–3, but via flexor burst truncation at P4–6. At any age, low-intensity stimulation during the extensor phase had no consistent effect on the ongoing rhythm. Activation of muscle afferents evoked via isometric contraction of the Q muscle caused effects similar to those obtained on low-intensity electrical stimulation in all age groups. In all age groups, high-intensity stimulation (≥5.0×T) caused resetting when delivered during the flexor phase via a prolongation of the flexor burst and during the extensor phase via a truncation of the extensor burst. These results suggest that the type of resetting evoked from low-threshold muscle afferents changes drastically during postnatal week1, while effects evoked from high-threshold afferents remain unchanged. Received: 13 May 1996 / Accepted: 17 September 1996     

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.     

Stretch and H reflexes in triceps surae are similar during tonic and rhythmic contractions in high decerebrate cats

During locomotion in decerebrate and spinal cats the group Ia afferents from hind leg muscles are depolarized rhythmically. An earlier study concluded that this locomotor-related primary afferent depolarization (PAD) does not contribute to modulation of monosynaptic reflex pathways during locomotion. This finding indicated that the neural network generating the locomotor rhythm, the central pattern generator (CPG), does not presynaptically inhibit monosynaptic reflexes. In this investigation we tested this prediction in decerebrate cats by measuring the magnitude of reflexes evoked in ankle extensor muscles during periods of tonic contractions and during sequences of rhythmic contractions. The latter occurred when the animal was induced to walk on a treadmill. At the similar levels of activity in the soleus muscle there was no significant difference in the magnitude of the soleus H reflex in these two behavioral situations. Similar results were obtained for reflexes evoked by brief stretches of the soleus muscle. We also examined the reflexes evoked by ramp-and-hold stretches during periods of rhythmic and tonic activity of the isolated medial gastrocnemius (MG) muscle. At similar levels of background activity, the reflexes evoked in the MG muscle were the same during rhythmic and tonic contractions. Our failure to observe a reduction in the magnitude of H reflexes and stretch reflexes during rhythmic contractions, compared with reflexes evoked at the same level of background activity during tonic contractions, is consistent with the notion that the CPG for stepping does not presynaptically inhibit monosynaptic reflexes during the extension phase of locomotor activity. Our results indicate that presynaptic inhibition of the monosynaptic reflex associated with normal locomotion in cats or humans arises from sources other than the extensor burst generating system of the central pattern generator.     

Reflexes induced by nerve stimulation in walking cats with implanted cuff electrodes

Summary Neural cuffs, implanted around various hindlimb nerves (sural, common peroneal, posterior tibial), were used to deliver brief stimulus trains to unrestrained cats walking on a treadmill. The resulting perturbations of the step cycle were evaluated by analyzing the EMG bursts recorded from the ankle extensors and by high speed cinematography. It was found that relatively weak stimulation (1.4 to 2 X T) of the posterior tibial nerve was very effective in eliciting a prolongation of the flexion phase provided the stimuli were applied just prior to the expected onset of the ankle extensor EMG burst. This ipsilateral hyperflexion was correlated with a prolongation of the contralateral extension. The same stimuli applied during stance usually evoked a yielding of the stimulated leg and a prolongation of the ongoing contralateral stance. In addition to these flexor and extensor reflex effects, it was found that low threshold stimulation of the sural and common peroneal nerves resulted in a powerful reflex activation of the ankle extensors. In contrast, stimulation of the gastrocnemius-soleus nerve (a muscle nerve) produced no discernible behavioral effects, even for stimuli at 3 X T, indicating that the observed reflexes are probably mediated by cutaneous afferents. The results were largely confirmed in experiments using the same cuffs implanted in spontaneously walking premammillary cats.     

Supraspinal and segmental signals can be transmitted through separate spinal cord pathways to enhance locomotor activity in extensor muscles in the cat

 The fine control of locomotion results from a complex interaction between descending signals from supraspinal structures and sensory feedback from the limbs. In this report, we studied the interaction between vestibulospinal volleys descending from Deiters’ nucleus and group I afferent input from extensor muscles. It has been shown that both pathways can exert powerful control over the amplitude and the timing of muscle bursting activity in the different phases of the step cycle. The effects of stimulating these pathways on the fictive locomotor rhythm were compared in decerebrate, partially spinal cats (ipsilateral ventral quadrant intact) injected with nialamide and l-dopa. As reported before, stimulation of both Deiters’ nucleus and group I fibres from ankle extensor muscles, when given during the flexor phase, stopped the flexor activity and initiated activity in extensors. When applied during the extensor phase, the same stimulation prolonged the extensor activity and therefore delayed the onset of flexor activity. This similarity suggests that the two pathways might converge on common spinal interneurones. This possibility was tested with the spatial facilitation technique in lumbosacral motoneurones. Deiters’ nucleus and group I fibres from extensor muscles were stimulated with different intensities and with several different coupling intervals. Motoneurones showing clear di- and/or polysynaptic excitation from both pathways were retained for analysis. Surprisingly, in all cases, there were no signs of spatial facilitation, but a simple algebraic sum of the two excitatory postsynaptic potentials. This result indicates that each input acts on the rhythm generator through separate interneuronal pathways. Received: 20 August 1996 / Accepted: 14 November 1996     

An intracellular study of muscle primary afferents during fictive locomotion in the cat

1. Presynaptic activity of identified primary afferents from flexor, extensor, and bifunctional hindlimb muscles was studied with intra-axonal recordings during fictive locomotion. Fictive locomotion appeared spontaneously in decorticate cats (n = 9), with stimulation of the mesencephalic locomotor region (n = 4), and in spinal cats injected with clonidine or nialamide and L-DOPA (n = 4). Representative flexor and extensor muscle nerves, recorded to monitor the locomotor pattern and dorsal rootlets of the sixth and seventh lumbar segments, were recorded simultaneously to monitor dorsal root potentials (DRPs). 2. From responses to muscle stretches and, in some instances, twitch contractions of the parent muscle, 75% of the single units examined were putatively identified as spindle afferents (40/53). On the basis of conduction velocity and stimulation threshold, 73% of these were further classified as group I fibers (29/40), the rest as group II fibers. 3. All units (n = 53 with resting potential more negative than -45 mV) showed fluctuations of their membrane potential (up to 1.5 mV) at the rhythm of the fictive locomotion. Subsequent averaging of these fluctuations over several cycles revealed that 89% of all units displayed a predominant wave of depolarization during the flexor phase, followed by a trough of repolarization. In 79% of the units, there was also a second, usually smaller, depolarization during the extensor phase. The relative size of each wave of depolarization could vary with different episodes of fictive locomotion in the same unit and among various afferents from the same muscle in the same experiment. 4. The firing frequency of some afferents from the ankle flexor tibialis anterior (5/16) and the bifunctional muscle posterior biceps-semitendinosus (4/15) was phasically modulated along the fictive step cycle. The maximum frequency always occurred during the flexor phase, i.e., during the largest depolarization of the unit. Because of the absence of phasic sensory input in the curarized animal, we assume that the phasic discharges were generated within the spinal cord and antidromically propagated. Phasic firing was never encountered in afferents from extensor muscles such as triceps surae (0/15) and vastus lateralis (0/4). 5. The results demonstrate that the pattern of rhythmic depolarization accompanying fictive locomotion is similar for the majority of flexor, extensor, and bifunctional group I (and possibly group II) muscle spindle primary afferents. They further indicate that there is a specific phasic modulation of antidromic firing for some flexor and bifunctional muscle spindle afferents.(ABSTRACT TRUNCATED AT 400 WORDS)     

Sartorius muscle afferents influence the amplitude and timing of flexor activity in walking decerebrate cats

Recent investigations have demonstrated that afferent signals from hindlimb flexor muscles can strongly influence flexor burst activity during walking and during fictive locomotion in decerebrate cats. We have reported previously that modifying afferent feedback from the sartorius (Sart) muscles by assisting or resisting hip flexion has a marked effect on the magnitude and duration of activity in iliopsoas (IP) as well as the sartorius muscles. The objective of the present investigation was to identify the afferents responsible for these effects by examining, in walking decerebrate cats, the influence of electrically stimulating sartorius afferents on burst activity in the IP and tibialis anterior (TA) muscles. Stimulation of the sartorius nerve at group I strength resulted in an increase in the duration of IP and TA bursts and an increase in the magnitude of IP bursts. The effect on burst durations was only observed at stimulus strengths of 1.6 T and higher. At lower stimulus strengths, there was a strong excitatory effect on IP bursts but no effect on TA bursts. Stimulation of the sartorius nerve at group II strength yielded variable results. When group II stimulation was delivered repeatedly during a walking sequence, the initial response was usually a strong inhibition of burst activity in IP and TA followed by a progressive reduction in inhibition and the emergence in IP of an excitatory response. This observation, together with findings of previous studies, suggests the existence of parallel excitatory and inhibitory pathways from sartorius group II afferents to flexor motoneurons. Taken together, these results support an earlier speculation that feedback from large afferents from the sartorius muscles has a strong influence on the generation of flexor burst activity in walking cats. Electronic Publication     

Characterization of hindlimb muscle afferents involved in ventilatory effects observed in decerebrate and spinal preparations

Summary Neurogenic changes of phrenic activity have previously been observed during periodic passive motions of one hindlimb in decorticate, unanaesthetized and curarized rabbit preparations before and after high spinal transection (Palisses et al. 1988). In decerebrate and spinal preparations, we aimed to determine, through rhythmic electrical stimulation of hindlimb muscle nerves, which muscle afferents are involved in these effects. In decerebrate preparations, these electrical stimulations (trains of shocks at 80 Hz for 300 ms every second for 20 s) produced ventilatory effects when group I+II afferent fibres of either flexor or extensor nerves were stimulated together and more powerful changes as soon as group III fibres were recruited. Stimulation of group I fibres alone induced no such effects. When present, these changes in respiratory activity consisted of a maintained decrease of the respiratory period due to both inspiratory and expiratory time shortening; in addition, the amplitude of the phrenic bursts greatly increased at the onset of electrical stimulation. After spinal transection at C2 level and pharmacological activation by nialamide and DOPA, only short-lasting phrenic bursts developed spontaneously; the electrical stimulation of group II and mainly group III flexor afferent fibres induced large amplitude phrenic activity whereas the stimulation of the same extensor afferents was relatively ineffective. The activation of phrenic motoneurones during group III flexor afferent stimulation was closely linked to each 300 ms period of stimulation. While the phrenic effects obtained in the spinal preparations by natural and by electrical periodic stimulation are quite similar to each other, those produced in decerebrate preparations differ substantially. It is concluded that the regulation of phrenic activity in decerebrate and spinal rabbit preparations by hindlimb proprioceptive afferents involves different muscle receptors; perhaps joint proprioceptors for the medullary resetting and muscle receptors connected to group III afferent fibres for the spinal reflex activation of phrenic motoneurones.     

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.