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

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

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.     

Modulation of activity of spindle afferents recorded in trigeminal mesencephalic nucleus of rabbit during fictive mastication

1. These experiments were based on the findings that antidromic firing is observed in first-order sensory afferents during fictive locomotion and were designed to test the hypothesis that a similar central modulation of afferent discharge occurs during mastication. To do this, spindle afferents were recorded in the trigeminal mesencephalic nucleus (Mes V) of anesthetized and paralyzed rabbits during fictive mastication. The cortical masticatory area was stimulated to induce mastication, and activity of the XIIth or the Vth nerves were recorded to monitor the masticatory motor rhythm. 2. Although we could find little evidence that antidromic discharges invade the somatic region of this class of sensory afferents, we did discover a previously unrecognized type of modulation of afferent firing. 3. Of 83 slowly adapting muscle spindle afferents, 33 were modulated during fictive mastication. In 28 cases, the modulation consisted of a phasic inhibition, whereas for the remaining units it could be either a phasic excitation (n = 2) or an excitation alternating with an inhibition (n = 3). 4. Rapidly adapting units were also tested when encountered. Tonic or phasic excitation was never observed. The presence of inhibition could not be verified for this population because tonic activity could not be maintained by passive stretch. 5. The main electroneurogram (ENG) burst of the XIIth and Vth cranial nerves occurred during the opening phase of the masticatory cycle, and in all cases where the records were clear (22 out of 33), phasic inhibition of the afferents coincided with the ENG burst. 6. There was no difference in the distributions of the modulated and of the unmodulated units along the length of the Mes V nucleus. 7. Approximately 40% of trigeminal spindle afferent cell bodies have dendrites, and we suggest that these are the ones rhythmically modulated during fictive mastication. The possible role of this modulation is discussed.     

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.     

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.     

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.     

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.     

Rhythmic fluctuations of dorsal root potentials and antidromic discharges of primary afferents during fictive locomotion in the cat

1. This study examines rhythmical activity of primary afferents occurring during "fictive" locomotion in decorticate paralyzed cats. Oscillations of the dorsal root potential (DRP) at the frequency of the locomotor rhythm have been observed at the lumbosacral and cervical levels. In addition, rhythmic antidromic discharges of primary afferent units have been recorded from the proximal stumps of cut dorsal root filaments. A detailed study of the relationships between the DRP fluctuations, the antidromic discharges, and the locomotor activity monitored by recording extensor and flexor muscle nerves is presented. 2. Typical DRP recordings from both lumbosacral and cervical levels show two negative waves (N1 and N2) separated by positive troughs (P1 and P2) in each locomotor cycle. Linear regression analyses indicate that the first negative wave (which generally has the largest amplitude) is related to the flexor activity whereas the second is related to the extensor activity. The relative amplitude of the two negative waves may vary without apparent concomitant changes in the recorded flexor or extensor motor nerves. The positive troughs occur respectively close to the period of transition between flexor and extensor activities and between extensor and flexor activities. 3. DRPs of similar period and amplitude can be observed in different ipsilateral roots recorded simultaneously. The DRPs recorded bilaterally from the same segment have the same periodicity but are out-of-phase. Point-to-point variations of amplitude in bilaterally recorded roots are not correlated. This suggests that the polarization of primary afferents on one side is mainly related to the locomotor events on that side. DRPs have been recorded in cats spinalized at Th13 and injected with nialamide and l-DOPA. This suggests that although the supraspinal contribution may be important, at least part of the DRPs may result from locomotor activity within the spinal cord itself. 4. A salient finding in our experiments was that of rhythmic antidromic unit discharges in the proximal stump of cut dorsal root filaments. Of the 194 units recorded, 19% (37/194) discharged in distinct bursts occurring at fixed times in the locomotor cycle. The majority of the units discharged either one burst during the period of flexor or extensor activity or one burst during one of the two periods of transition. Three units discharged two bursts per locomotor cycle. The frequency of the antidromic discharges of some units in one limb were also found to be modulated by stimulation of the skin or passive manipulation of the limbs.(ABSTRACT TRUNCATED AT 400 WORDS)     

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.     

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.     

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.     

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.     

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     

Interneurones of the lumbar cord related to spontaneous locomotor activity in the rabbit

Summary In decorticate, unanaesthetized and curarized rabbit preparations displaying spontaneous fictive locomotor sequences, the firing pattern of neurones was recorded extracellularly in the L6-S1 spinal cord. These neurones, located in the intermediate part of the cord, were not invaded by antidromic stimulation of the hindlimb muscle nerves and thus were considered as interneurones (or propriospinal or tract cells ascending to the brain). When compared to the output from the ipsilateral muscle nerves, these neurones were classified as flexor (F INs) or extensor (E INs) according to the phase of the locomotor cycle when they displayed their maximal firing rate. Among 69 F INs, 33 maintained tonic firing during the periods between episodes of locomotor activity. Their maximal firing rate was in phase with the flexor efferent bursts of the locomotor sequence; during the extensor phase, they maintained an instantaneous frequency (i.f.) that was clearly above the resting i.f. Of these neurones, six became completely silent during the initial flexor-extensor coactivation that opened the sequence (F₁ neurones) whereas the 27 others increased their firing rate at that time (F₂ neurones). The other neurones (36 F₃) were silent between the locomotor episodes. Although most of them had a rhythmic activity limited to the flexor bursts, some fired throughout the locomotor sequence with a maximal rate during flexor bursts. All the 123 E neurones completely stopped firing during the flexor phase. As was the case for F₃- neurone firing, E₃ neurone firing (34 neurones) occurred only during periods of locomotor activity. Among the neurones that displayed tonic activity between locomotor episodes, the E₂ neurones (24 from 123) remained at this resting value during the extensor phase whereas the E₁ neurones (65 neurones) showed an increased i.f. for all or part of this phase. These data, which suggest an asymmetrical genesis of the flexor and extensor activities in locomotion, need to be supported by further analysis.     

Static fusimotor action during locomotion in the decerebrated cat revealed by cross-correlation of spindle afferent activity

Cross-correlation of the discharges of muscle spindle afferents in ankle extensor and flexor muscles has been used to reveal the activity of static gamma (gammaS) motoneurones innervating chain intrafusal muscle fibres during locomotion. In the anaesthetised cat, the cross-correlation of spindle afferents, jointly innervated by a gammaS-efferent with chain fibre contacts, showed short duration synchrony (2-8 ms) when the efferent was stimulated repetitively. In pre-mammillary decerebrated cats, the cross-correlograms of discharges of some pairs of spindle afferents showed similar short duration peaks of synchronisation and these were interpreted as being due to a common gammaS drive to chain intrafusal muscle fibres. The incidence of synchrony was low, and was similar at rest (5 % of pairs) and during treadmill locomotion (7 % of pairs). Phase dependence of synchrony was evident during locomotion in the flexor muscle. The synchrony of muscle spindle afferent discharge is discussed in relation to estimates of the numbers of spindles contacted by individual gammaS-efferents.     

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)     

Excitability changes of ankle extensor group Ia and Ib fibers during fictive locomotion in the cat

Summary The present study examines the modulation of gastrocnemius-soleus (GS) monosynaptic reflexes as well as the intraspinal threshold changes of GS group I primary afferent terminals ending in the intermediate and motor nuclei during fictive locomotion in high decerebrate cats. The amplitude of the monosynaptic reflexes (MSR's) evoked in the medial gastrocnemius by stimulation of the lateral gastrocnemius nerve was increased during the extensor (E) phase, decreased during the flexion (F) phase of the step cycle and remainded transiently increased after spontaneous episodes of fictive stepping. The intraspinal threshold of populations and of single group Ia GS afferent fibers ending in the motor pool, as well as of single Ia and Ib fibers ending in the intermediate nucleus, showed a sustained reduction during the episodes of fictive locomotion with superimposed cyclic changes in phase with the step cycle. During fictive walking and trotting the reduction of the intraspinal threshold of both Ia and Ib fiber terminals was maximal during the middle or late portion of the F-phase. During fictive gallop elicited by stimulation of the superficial peroneus nerve, the decrease in the intraspinal threshold of the Ia afferent fibers occurred however in phase with the activity of the GS motoneurons. During episodes of fictive locomotion slow, sustained negative DC potential shifts lasting tents of seconds, reflecting an increase in the extracellular potassium concentration were recorded at the base of the dorsal horn and in the intermediate nucleus. The present findings support the existence of tonic and phasic depolarization of the intraspinal terminals of GS group Ia and Ib primary afferents during spontaneous fictive locomotion. It is suggested that accumulation of potassium ions in the extracellular space contributes mainly to the sustained depolarization of group I fibers. The phasic depolarization would be mostly due to the activation of specific sets of interneurons and may, in the case of Ia fibers, contribute to the cyclic modulation of the MRS elicited during fictive locomotion.     

Discharges of single hindlimb afferents in the freely moving cat.

1. Implanted semimicroelectrodes were used to record single afferent fiber discharges from L7 dorsal roots during unrestrained walking in the conscious cat. 2. A series of tests were used to identify an afferent during a short period of anesthesia following each recording session. The majority of afferents were from muscle spindle primary endings in hindlimb muscles. 3. Ankle extensor spindle primaries generally showed their highest firing rates during that phase of stepping in which they were passively stretched. During active muscle contraction there was evidence of fusimotor drive, although this was not usually sufficient to entirely overcome the unloading effect of rapid muscle shortening. The variability of firing rate from cycle to cycle was considerably greater for the phase of active muscle contraction. The EMG response to brisk stretches of the ankle extensor muscle indicated a rapid (disynaptic or trisynaptic) reflex arc in the conscious animal. 4. Knee flexor spindle primaries showed similarly higher firing rates during passive muscle stretching in the step cycle. The shorter periods of presumed alpha-gamma coactivation corresponded to the much more phasic role of these muscles in stepping. 5. Tendon organs in the physiological extensors of the toes were mainly active during stance, although some discharges were usually seen during the swing phase. It is suggested that previous experiments on mesencephalic preparations may have led to an exaggerated view of the degree of alpha-gamma coactivation during normal stepping movements.     

Patterns of locomotor drive to motoneurons and last-order interneurons: clues to the structure of the CPG.

We have examined the linkage between patterns of activity in several hindlimb motor pools and the modulation of oligosynaptic cutaneous reflex pathways during fictive locomotion in decerebrate unanesthetized cats to assess the notion that such linkages can shed light on the structure of the central pattern generator (CPG) for locomotion. We have concentrated attention on the cutaneous reflex pathways that project to the flexor digitorum longus (FDL) motor pool because of that muscle's unique variable behavior during normal and fictive locomotion in the cat. Differential locomotor control of last-order excitatory interneurons in pathways from low-threshold cutaneous afferents in the superficial peroneal and medial plantar afferents to FDL motoneurons is fully documented for the first time. The qualitative patterns of differential control are shown to remain the same whether the FDL muscle is active in early flexion, as usually found, or during the extension phase of fictive locomotion, which is less common during fictive stepping. The patterns of motor pool activity and of reflex pathway modulation indicate that the flexion phase of fictive locomotion has distinct early versus late components. Observations during "normal" and unusual patterns of fictive stepping suggest that some aspects of locomotor pattern formation can be separated from rhythm generation, implying that these two CPG functions may be embodied, at least in part, in distinct neural organizations. The results are discussed in relation to a provisional circuit diagram that could explain the experimental findings.     

Fictive locomotor patterns generated by tetraethylammonium application to the neonatal rat spinal cord in vitro

Intrinsic spinal networks generate a locomotor rhythm characterized by alternating electrical discharges from flexor and extensor motor pools. Because this process is preserved in the rat isolated spinal cord, this preparation in vitro may be a useful model to explore methods to reactivate locomotor networks damaged by spinal injury. The present electrophysiological investigation examined whether the broad spectrum potassium channel blocker tetraethylammonium could generate locomotor-like patterns. Low (50-500 microM) concentrations of tetraethylammonium induced irregular, synchronous discharges incompatible with locomotion. Higher concentrations (1-10 mM) evoked alternating discharges between flexor and extensor motor pools, plus large depolarization of motoneurons with spike broadening. The alternating discharges were superimposed on slow, shallow waves of synchronous depolarization. Rhythmic alternating patterns were suppressed by blockers of glutamate, GABA(A) and glycine receptors, disclosing a background of depolarizing bursts inhibited by antagonism of group I metabotropic glutamate receptors. Furthermore, tetraethylammonium also evoked irregular discharges on dorsal roots. Rhythmic alternating patterns elicited by tetraethylammonium on ventral roots were relatively stereotypic, had limited synergy with fictive locomotion induced by dorsal root stimuli, and were not accelerated by 4-aminopyridine. Horizontal section of the spinal cord preserved irregular ventral root discharges and dorsal root discharges, demonstrating that the action of tetraethylammonium on spinal networks was fundamentally different from that of 4-aminopyridine. These results show that a potassium channel blocker such as tetraethylammonium could activate fictive locomotion in the rat isolated spinal cord, although the pattern quality lacked certain features like frequency modulation and strong synergy with other inputs to locomotor networks.