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Groupe de Recherche sur le Système Nerveux Central, Department of Physiology, Faculty of Medicine, Université de Montréal, Montreal, Quebec, Canada
Submitted 20 November 2007; accepted in final form 19 December 2007
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ABSTRACT |
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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 (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. |
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INTRODUCTION |
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; McCrea 2001; Rossignol et al. 2006; Zehr and Stein 1999). For instance, mechanical stimulation of the foot dorsum during the swing phase of locomotion generates a coordinated reflex, the stumbling corrective reaction, in several leg muscles bilaterally allowing the perturbed limb to progress over the obstacle (Buford and Smith 1993; Forssberg 1979; Prochazka et al. 1978; Wand et al. 1980; Zehr and Stein 1999). In the stumbling corrective reaction, the ipsilateral leg is lifted over the obstacle while the contralateral leg supports the stimulated limb (i.e., crossed extensor reflex). The locomotor program must be capable of adjusting both hindlimbs when one limb is perturbed so that progression and equilibrium are preserved (Saltiel and Rossignol 2004b) but pathways involved in this bilateral coupling are unclear. Recent work in cats has delineated interneuronal spinal pathways involved in stumbling corrective reactions in the ipsilateral limb during fictive locomotion (Quevedo et al. 2005a,b), but pathways to the contralateral leg were not studied.
Electrically stimulating cutaneous afferents from the foot has been used as an alternative to mechanical stimulation to evaluate responses in several leg muscles (Abraham et al. 1985; Buford and Smith 1993; Duysens 1977; Duysens and Loeb 1980; Duysens and Pearson 1976; Loeb 1993; Pratt et al. 1991). During swing, electrical stimulation of cutaneous afferents from the paw evokes, in the ipsilateral limb, short (P1)- and longer (P2)-latency excitatory responses in flexors in the swing phase whereas during stance, flexors are typically silent, and responses in extensors are characterized by short-latency inhibition (N1) followed by longer-latency (P2–P3) excitation (Abraham et al. 1985; Duysens and Loeb 1980; Loeb 1993; Pratt et al. 1991). Similar responses are also evoked in the forelimbs during locomotion (Drew and Rossignol 1987; Zehr and Duysens 2004). In the contralateral hindlimb, excitatory responses (P2) are observed in extensors at a latency of 20–25 ms (Duysens and Loeb 1980), and it was proposed that crossed excitatory pathways coordinate activity between limbs during locomotion (Gauthier and Rossignol 1981; Lundberg 1979; Lundberg et al. 1987; Rossignol et al. 2006; Sherrington 1910a).
However, by conditioning monosynaptic reflexes to examine motoneuron excitability, it was shown that crossed inhibitory pathways also exist (Curtis et al. 1958; Holmqvist and Lundberg 1959; Lloyd 1944). In another study, inhibitory postsynaptic potentials mediated by a disynaptic pathway were recorded in motoneurons of the sacral cord following stimulation of low-threshold fibers of the contralateral dorsal root of the same segment (Curtis et al. 1958). Crossed disynaptic inhibition of sacral motoneurons was shown to be mediated by group Ia muscle spindle afferents (Jankowska et al. 1978). Stimulation of group II or cutaneous afferents in nonlocomotor anesthetized cats also evokes short-latency inhibition in contralateral ankle extensor motoneurons (Aggelopoulos et al. 1996; Arya et al. 1991; Edgley and Aggelopoulos 2006). During locomotion, inhibition of contralateral extensors while the ipsilateral limb is perturbed during swing would tend to destabilize the animal. Reflex pathways during locomotion are often thought as adjusting phase onset and offset by terminating stance and initiating swing, for example, but rarely within the context of adjusting the coordination between limbs.
A few studies have suggested that probably several interlimb coordination mechanisms exist (Forssberg et al. 1980; Saltiel and Rossignol 2004a,b), and it is possible that crossed inhibition plays a critical role. Therefore because crossed inhibitory responses are elicited by stimulating group II or cutaneous afferents in reduced nonlocomotor preparations (Aggelopoulos et al. 1996; Arya et al. 1991; Edgley and Aggelopoulos 2006), we hypothesized that these responses could also be present in walking cats.
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METHODS |
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Data were obtained from seven adult cats (6 males, 1 female) weighing between 3.0 and 7.0 kg. Cats in the present study were used in other experiments (Frigon and Rossignol 2007), but specific observations have not been published previously. Cats were first selected based on their ability to walk for prolonged periods on a treadmill and trained for 2 wk at their preferred speed (0.3–0.5 m/s). Cats were subsequently implanted with chronic electrodes for EMG recordings and nerve stimulation and allowed to recover from the implantation, and baseline values of EMGs and reflexes were recorded for 33–60 days.
The experimental protocol was in accordance with the guidelines of the animal Ethics Committee of the Université de Montréal. All surgical procedures were performed under general anesthesia and aseptic conditions. Prior to surgery, cats were injected with an analgesic (Anafen 2 mg/kg sc) and premedicated (Atravet 0.1 mg/kg, glycopyrrolate 0.01 mg/kg, ketamine 0.01 mg/kg im). Cats were then intubated and maintained under gaseous anesthesia (isoflurane 2%) while heart rate and respiration were monitored. After surgery, an analgesic (Buprenorphine 0.01 mg/kg) was administered subcutaneously. An oral antibiotic (cephatab or apo-cephalex, 100 mg/d) was given for 10 days following surgery.
EMG
Chronic electromyographic (EMG) electrodes were implanted bilaterally in the following hindlimb muscles for all cats: semitendinosus (St: knee flexor/hip extensor), anterior part of sartorius (Srt: hip flexor/knee extensor), vastus lateralis (VL: knee extensor), lateral gastrocnemius (LG: ankle extensor/knee flexor), and tibialis anterior (TA: ankle flexor). The medial gastrocnemius (MG: ankle extensor/knee flexor), soleus (Sol: ankle extensor), and gluteus medius (GM: hip extensor) were also implanted in five, three, and two cats, respectively. A pair of Teflon-insulated multistrain fine wires (AS633; Cooner Wire, Chatsworth, CA) was directed subcutaneously from head-mounted 15 pin connectors (Cinch Connectors; TTI) and sewn into the belly of each muscle for bipolar EMG recordings. EMG recordings were band-pass filtered (100-3,000 Hz) and amplified (gains of 0.5–50,000) using two Lynx-8 amplifiers (Neuralynx, Tucson, AZ). EMG data were digitized (5,000 Hz) using custom-made acquisition software.
Step cycle duration was measured as the time between two successive Srt bursts. Burst duration was determined as the time from onset to offset. The effects of tibial (Tib) nerve stimulation, evoked at different phases of the step cycle, on durations of the step cycle and selected EMG bursts (Srt and ankle extensors bilaterally) were assessed in five cats and expressed as the difference from the control (i.e., nonstimulated) values in ms. Stimulated cycles were grouped in 1 of 10 bins according to the time stimulation was delivered during the step cycle while nonstimulated cycles were averaged to provide control values. The mean control value was then subtracted from the mean stimulated values in each of the 10 bins providing a difference from control in milliseconds in each phase. Correlation coefficients (r) were calculated (Sigmaplot 9.0) to determine the strength of the linear association between burst durations of the left Srt and right ankle extensors and between the right Srt and left ankle extensors with Tib nerve stimulation during different phases of the step cycle.
Nerve stimulation
A chronic stimulating electrode composed of bipolar wires (AS633; Cooner Wire) embedded in a polymer (Denstply International) cuff (Julien and Rossignol 1982) was placed around the left Tib nerve at the ankle adjacent to the Achilles' tendon in five cats and around the left superficial peroneal (SP) on the dorsum of the foot in two cats. Both nerves were stimulated (Grass S88 stimulator) at varying intensities during locomotion with a single 1-ms pulse at a constant time (100 ms after onset of left St burst) to determine the threshold for obtaining a small yet consistent short-latency (10 ms) response in TA. Stimulation current was then set at 1.2–1.5 times this threshold. During testing sessions, stimuli were given once every three cycles. The time of the stimulus was varied pseudorandomly to evoke responses at different times during the step cycle for a total of 120–200 stimulations. In one session, left SP nerve stimulation was triggered at 100 ms for 100 stimulations following left St burst onset.
Reflexes were measured as detailed previously (Frigon and Rossignol 2007), and only responses evoked in extensors bilaterally will be described. Figure 1 provides a detailed description of the methodology used to quantify reflex responses. Briefly, the EMGs were grouped into stimulated or control (nonstimulated) trials. The step cycle was divided into 10 phases by synchronizing the cycle to the onset of the left St burst. At least 50 control cycles (i.e., without stimulation) were averaged and separated into these 10 bins according to the time they were evoked in the cycle to provide a template of baseline locomotor EMG (blEMG) during the step cycle (dotted line in Fig. 3). From the 120–200 stimulations, 10–20 reflex responses were grouped in each of the 10 bins superimposed on the blEMG for that bin. Onset and offset of reflexes in extensors, delineated as a prominent negative or positive deflection away from the blEMG, were determined manually using predefined latencies as guidelines (Abraham et al. 1985; Duysens and Stein 1978; Loeb 1993; Pratt et al. 1991). We used previously described nomenclature (Duysens and Loeb 1980) where N and P, respectively, denote negative (inhibitory) and positive (excitatory) responses. The numbered suffix indicates response onset where 1 is 10 ms and 2 is 25 ms. Excitatory responses in ipsilateral extensors beginning at 35 ms are sometimes termed P3 (Duysens and Loeb 1980) but for simplicity will be referred here as P2. EMG from onset to offset was rectified and integrated and the blEMG was subtracted from this value. The subtracted value was then divided by a 10-ms portion of the blEMG in the corresponding bin to provide a measure of reflex amplitude. Correlation coefficients (r) were calculated (Sigmaplot 9.0) to determine the strength of the linear association between the amplitude of N1 and P2 in ankle extensors of the same limb evoked by Tib nerve stimulation during the step cycle.
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A one-way ANOVA was used to determine the effects of Tib nerve stimulation when given at different times during the step cycle on the duration of the step cycle and selected EMG bursts across five cats. If significant, a Dunnet's post hoc test was performed against control (nonstimulated) values. An ANOVA was also used to determine significant differences between the latency and duration of ipsi- and contralateral responses of the same nature (e.g., inhibition or excitation) evoked by Tib nerve stimulation across five cats. The duration and latency of inhibitory and excitatory responses in extensors on the ipsi- and contralateral sides were grouped separately to evaluate differences between both hindlimbs. For example, inhibitory responses in extensors of the ipsilateral limb were compared with inhibitory responses in extensors of the contralateral limb. Significance level was set at P 
0.05. Descriptive statistics are means ± SE.
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RESULTS |
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Short-latency inhibitory responses were observed in extensors of the left leg during stance of the left leg and in the right leg during stance of the right leg with stimulation of the Tib or SP nerves of the left leg, which were followed in both cases by longer-latency excitatory responses. For instance, Fig. 2 shows the effects of Tib nerve stimulation on selected EMG bursts (Srt and triceps surae muscles bilaterally) during locomotion in one cat. In the same session but at different times, the left Tib nerve was stimulated during stance of the left (Fig. 2A) and stance of the right (Fig. 2B) leg. In both instances, stimulation evoked a very brief period of silence, or inhibition, of the ongoing EMG in ankle extensors of both legs. A closer examination in the right LG clearly shows that stimulating the left Tib nerve during stance of the right leg produces a period of inhibition starting 12 ms following the stimulus (Fig. 2C).
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100 times in one cat while the right hindlimb was in the latter half of stance. A short-latency crossed inhibition at 13 ms of the ongoing EMG lasting for 14 ms is observed (
) followed by a longer-latency excitatory response at 26 ms (), which lasts for 14 ms. Crossed inhibitory responses were consistently observed in ankle and hip extensors but not in vastus lateralis, a knee extensor. Although preliminary results showed that Tib nerve stimulation evoked short-latency inhibitory responses during the hip flexor burst of the contralateral Srt, a bifunctional muscle, the presence of crossed inhibition in flexors and other muscles requires further investigation before a conclusive statement can be made.
To compare reflex responses evoked in extensors of the left and right leg, muscles were recorded bilaterally and stimulation was evoked at different times during the step cycle. Figure 4 shows the average of 10 responses in each of the 10 phases of the step cycle, synchronized to the left St burst, to stimulation of the left Tib nerve in the left (A) and right (B) MG of the same cat. Stimulation of the left Tib nerve evoked a short-latency inhibition (10 ms) and a longer-latency excitation (35–40 ms) in the left MG. Stimulation of the same nerve likewise evoked a short-latency inhibition (13 ms) and longer-latency excitation (25 ms) in the right MG during locomotion. As can be seen, inhibitory responses in the right MG appear at a slightly longer latency and are of shorter duration than responses in the left MG. Response amplitudes in MG of both hindlimbs were modulated according to the phase of the step cycle. The background locomotor EMG is given on the far right for each muscle to illustrate the activity of these muscles during the step cycle. Responses were qualitatively similar in LG, soleus, and GM (not shown).
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To assess the relationship between the amplitude of short-latency inhibition with the amplitude of longer-latency excitation, N1 and P2 responses were plotted and correlations were made. Figure 5, top, shows group data of N1 and P2 responses evoked in ankle extensors of the left (A) and right (B) hindlimbs with stimulation of the left Tib nerve at different times during the step cycle for five cats. Response amplitude was modulated throughout the step cycle. Bottom panels show by regression analyses that N1 and P2 amplitudes correlated strongly (r = –0.85) on the right side (D) but that there was no correlation (r = –0.22) on the left side (C). In other words, a large N1 amplitude will be associated with a large P2 amplitude and vice versa in contralateral ankle extensors.
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The effects of stimulating the Tib nerve on selected EMG bursts were assessed in 5 cats to determine if nerve stimulation produced concomitant increases in muscle bursts that are simultaneously active bilaterally. Across five cats (Fig. 6), stimulation of the left Tib nerve prolonged the burst durations of the left Srt and right ankle extensors in phases 0.15 and 0.25, when these muscles were both active (A). The burst durations of ankle extensors of the right leg were unchanged from phases 0.75–0.95, when these muscles are active but the left Srt is silent. Thus prolongation of the burst in ankle extensors of the right leg occurs only in phases where the burst or activity of the left Srt is also increased. There was no effect of Tib nerve stimulation on burst durations of the right Srt and left ankle extensors at any point during the step cycle (Fig. 6B). For the group, there was a strong correlation (r = 0.91) between the durations of the left Srt and right ankle extensors with Tib nerve stimulation at different times during the step cycle (Fig. 6C), whereas for the right Srt and left ankle extensors (Fig. 6D) the correlation was less strong (r = 0.65).
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0.05). However, there were significant shifts in the onset and offset of certain muscles relative to the onset of the left Srt but only in two specific parts of the step cycle with the first and second parts corresponding to phases 0.15–0.35 (e.g., mid- to late flexion of the left leg) and 0.85 (early extension of the right leg), respectively (not shown). For instance, the left Srt burst had a delayed offset (16–44 ms) during phases 0.15–0.35 due to the increased burst duration of this muscle, which was accompanied by a delayed offset (17–22 ms) of right ankle extensors in the same phases. Onsets of left ankle extensors and right Srt were also delayed (4–10 ms) in phases 0.15–0.25 but their offsets were unchanged in these phases. In phase 0.85, the offset (28 ms) and onset (24 ms) of left and right ankle extensors, respectively, occurred earlier. The right Srt burst also finished earlier (3 ms). Therefore stimulation can influence the timing and durations of hip flexors and ankle extensors bilaterally in specific phases of the step cycle. |
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DISCUSSION |
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; Curtis et al. 1958; Edgley and Aggelopoulos 2006) operate during normal locomotion. Duysens and Loeb (1980) described in detail responses evoked in contralateral muscles by stimulating cutaneous nerves of the foot during locomotion in the cat. The reason for the absence of crossed inhibition in that paper is unclear, but an inspection of their Fig. 3 would seem to indicate that a period of inhibition precedes the excitatory response in the contralateral MG. The lack of a template of background locomotor activity (e.g., nonstimulated trials) probably prevented a clear distinction of the crossed inhibition that was observed in the present study. The crossed pathways responsible for these responses and their putative functions during locomotion are discussed. Afferents mediating the responses
Stimulation of both SP and Tib nerves just above motor threshold evoked qualitatively similar short-latency crossed inhibitory responses in extensors indicating that some of these effects were mediated by large diameter cutaneous afferents. Although the Tib nerve innervates intrinsic muscles of the foot and contains group I and II muscle afferents the SP nerve at the level of the ankle is entirely cutaneous. Stimulating the Tib nerve at an intensity of 1.2–1.5 times the threshold for evoking small but consistent short-latency responses in the ipsilateral TA could have recruited group I muscle afferents and group II muscle and cutaneous afferents. Edgley and Aggelopoulos (2006) reported that inhibitory postsynaptic potentials (IPSPs) in contralateral extensor motoneurons evoked by stimulating SP or sural nerves appeared near the threshold of the most excitable fibers, suggesting that large-diameter Aβ fibers, most likely mechanoreceptor afferents, were responsible. Smaller-diameter afferents can also contribute to responses because increasing stimulus intensity evoked larger crossed inhibitory responses in anesthetized cats, indicating a convergence between large and small diameter afferents (Edgley and Aggelopoulos 2006). Irrespective of which afferent type mediated responses, it is clear that crossed inhibition can be evoked in the intact cat during locomotion and forms part of the crossed pathway (i.e., inhibition followed by excitation) for certain muscles.
Central pathways
The differences in latencies of inhibitory responses on the left and right sides were similar to those following stimulation of cutaneous afferents in anesthetized cats (Edgley and Aggelopoulos 2006). For instance, contralateral inhibition of EMG on average started 2 ms later than ipsilateral inhibitory responses, whereas Edgley and Aggelopoulos (2006) reported a difference of 1 ms. The small difference between the two preparations could simply be due to the conduction distance from the spinal cord to recording sites and because in the present study we recorded EMG activity, whereas Edgley and Aggelopoulos (2006) recorded postsynaptic potentials in motoneurons.
Central pathways responsible for crossed inhibitory responses are probably the same described for anesthetized preparations (Bannatyne et al. 2006; Edgley and Aggelopoulos 2006; Jankowska et al. 2005b). For example, inhibitory interneurons in the dorsal horn of mid-lumbar spinal segments have wide ranging ipsi- and contralateral projections to many regions of the spinal gray matter including connections with large cholinergic neurons in the ventral horn, most likely motoneurons (Bannatyne et al. 2006). Excitatory connections from primary cutaneous afferents to these inhibitory interneurons in the dorsal horn could mediate crossed inhibition during locomotion. Another pathway mediating crossed inhibition in anesthetized cats includes activation of contralateral Ia inhibitory interneurons by excitatory commissural interneurons (Jankowska et al. 2005b). Commissural interneurons, inhibitory and excitatory, can be excited by various afferents, including group II and cutaneous afferents (Edgley and Aggelopoulos 2006; Jankowska 2007; Jankowska et al. 2005a,b).
Short-latency crossed inhibition was not present in the right VL following stimulation of the SP or Tib nerves of the left leg. The absence of crossed inhibition in VL could be due to the fact that motor pools of VL are located at L5–L6, whereas those of glutei and triceps surae muscles, which exhibited crossed inhibition, are found at L7–S1 (Vanderhorst and Holstege 1997; Yakovenko et al. 2002). This could suggest that relay neurons in the crossed inhibitory pathway observed in the present study are located more caudally within the spinal cord.
The strong correlation between the amplitude of crossed inhibition and excitation (Fig. 5) could mean that the short-latency inhibition controls the excitability of the longer-latency excitatory pathway without requiring inputs from supraspinal levels. It is likely that part of the excitatory response is mediated by postinhibitory rebound (Abraham et al. 1985). However, because short- and longer-latency excitatory responses can be evoked during the swing phase of locomotion in ipsilateral ankle extensors without preceding inhibition, a longer latency reflex pathway must also be involved (Duysens and Loeb 1980). Therefore excitatory responses are probably mediated by reflex pathways, which can be supplemented via postinhibitory rebound.
Effects of stimulation and bilateral cycle adjustments
During fictive locomotion, stimulating the Tib nerve during ipsilateral stance increased the duration of the activity of ipsilateral extensors, whereas stimulation during the ipsilateral flexion phase terminated flexion and initiated extension (Guertin et al. 1995). In intact cats, stimulation can advance or delay phases but abrupt terminations and initiations are rarely observed because this would disrupt ongoing locomotion. Instead, the activation of sensory pathways ensures proper interlimb coordination by adjusting the timing and durations of specific bursts. In a situation where speed is enforced by the treadmill, step cycle duration remains largely unaffected, although sub-components of the step cycle can be altered. For example, as shown previously (Duysens and Stein 1978), and in this study stimulating the Tib nerve during ipsilateral flexion prolonged ipsilateral hip flexor and contralateral ankle extensor bursts, whereas stimulation during ipsilateral stance had little or variable (Duysens and Stein 1978) effect. Crossed pathways coupling both hindlimbs from cutaneous or muscle afferents could ensure that step cycle duration remains constant while at the same time varying the sub-phases (e.g., flexion and extension phases bilaterally) to ensure proper interlimb coordination.
It was also reported that most timing adjustments occurred around mid- or late swing (Forssberg et al. 1980), which in our preparation corresponds approximately to phases 0.25–0.35 where effects of stimulation on locomotor bursts were most evident. For example, stimulation of the left Tib nerve delivered during phases 0.25–0.35 delayed the offset of the left Srt and of right ankle extensors. The onsets of left ankle extensors and of the right Srt were also delayed. Thus there are critical points during locomotion in which peripheral inputs can influence the step cycle, as shown previously during fictive locomotion (Saltiel and Rossignol 2004a,b). Additionally, when the cat was in a double support phase stimulation of the left Tib nerve did not increase the burst duration of ankle extensors of the right leg, most likely because the left leg was also being supported. Therefore biomechanical events can modify or "override" some bilateral cycle adjustments (Saltiel and Rossignol 2004a,b). In a functional context during locomotion, a prolongation of swing of the left leg during a perturbation would require a concomitant increase in stance of the right leg so that progression and equilibrium are maintained.
Functional considerations
It has been proposed that decomposing the step cycle into several subphases, with each requiring the activation of a specific set of modules would simplify how descending systems modify limb activity (Grillner 1981; Grillner and Wallen 1985; Ivanenko et al. 2007; Krouchev et al. 2006; Lafreniere-Roula and McCrea 2005; Stein and Smith 1997). Although only a concept, these modules would undoubtedly be coupled by feedback from the periphery through various ipsilateral and crossed pathways. As such, inhibition in addition to excitation would provide more flexibility to this system. The burst durations of the left Srt and right ankle extensors (Fig. 6) were strongly correlated with stimulation of the left Tib nerve while these muscles were active suggesting that crossed pathways interconnect left hip flexor and right ankle extensor "modules."
Sherrington (1910b, 1913) long ago suggested that inhibition in reflex pathways is an integral component of various reflex pathways in several behaviors, including locomotion, but the precise function of inhibition remains poorly understood. In particular, crossed inhibition of extensors while the ipsilateral leg is in flexion would tend to destabilize the animal during walking. Although we can only speculate as to the function of crossed inhibition during locomotion, when considered during the forward progression of stepping, crossed inhibition may serve to temporarily and very briefly "halt" or slow down forward progression. After all, crossed extension is only going to be useful if the ipsilateral flexion actually frees the limb from the perturbation. Moreover, short-latency inhibition of extensors, ipsilaterally or contralaterally, could serve to delay the onset of excitatory responses to enable supraspinal structures sufficient time to influence these pathways. Therefore even though the precise function of short-latency inhibition of contralateral extensors remains unclear, what is certain is that crossed extensor reflexes are more complex than originally thought.
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GRANTS |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: S. Rossignol, Dept. of Physiology, Groupe de Recherche sur le Système Nerveux Central, Faculty of Medicine, Université de Montréal, P. O. Box 6128, Station Centre-Ville, Montréal, Québec H3C 3J7, Canada (E-mail: serge.rossignol{at}umontreal.ca)
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