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Groupe de Recherche sur le Système Nerveux Central, Department of Physiology, Faculty of Medicine, Université de Montréal, Montreal, Canada
Submitted 29 February 2008; accepted in final form 7 July 2008
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ABSTRACT |
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INTRODUCTION |
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). Moreover, contacting the foot dorsum during the swing phase of locomotion in spinal cats generates a coordinated reflex response that allows the leg to overcome the obstacle (Forssberg 1979; Forssberg et al. 1975). This shows that the spinal cord can process sensory inputs from the hindlimbs to meet the demands of the environment during locomotion (Rossignol et al. 2006).
The spinal cord can also adapt to changes induced in its internal environment. For instance, lesioning the mixed peripheral nerve that innervates the lateral-gastrocnemius-soleus (LGS) in already spinal cats (i.e., after spinalization) produced an increased ankle yield during early stance, although with time this deficit disappeared (Bouyer et al. 2001), as is the case after a similar denervation in otherwise intact cats (Pearson et al. 1999). However, the spinal cord has a limited ability to adapt to changes induced in its internal environment because plantar paw placement was permanently lost after a complete cutaneous denervation of the hindpaws in a spinal cat (Bouyer and Rossignol 2003b), whereas in intact cats plantigrade placement can recover following the same denervation (Bouyer and Rossignol 2003a). This suggests that with an intact spinal cord the spinal central pattern generator (CPG) for locomotion can make use of other inputs to properly place the paw, whereas after a complete spinalization the spinal CPG requires at least a modicum of input from the skin for plantigrade placement of the paw. Therefore although intrinsic spinal mechanisms can offset to a certain extent the loss of sensory and/or motor innervations and produce changes leading to the functional recovery of locomotion, the isolated spinal cord has limitations.
In a recent study, reflex responses evoked by stimulating the tibial (Tib) nerve at the ankle, which is primarily cutaneous, were increased in the days following a unilateral LGS neurectomy in otherwise intact cats, suggesting that remaining cutaneous inputs can be increased following the loss of proprioceptive information in cats with an intact spinal cord (Frigon and Rossignol 2007). Whether cutaneous reflexes are modified and participate in the locomotor compensation following a similar denervation in chronic spinal cats is unknown. Supraspinal inputs could be required to evoke changes in reflex pathways following a muscle denervation. In addition, in chronic spinal cats (Bouyer et al. 2001) and otherwise intact cats (Pearson et al. 1999) functional recovery following partial denervation of ankle extensors was attributed to large increases in the burst activity of remaining synergists, such as the medial gastrocnemius (MG). However, in a more recent study it was shown that the activity of several leg muscles increased bilaterally following LGS denervation in otherwise intact cats (Frigon and Rossignol 2007). Whether a similar increase in multiple muscles occurs following a muscle denervation in chronic spinal cats is unclear.
The purpose of the present study was therefore 1) to determine whether Tib nerve reflexes and burst activity of several hindlimb muscles are modified after LGS neurectomy in chronic spinal cats and 2) to assess whether these changes are similar to those observed in otherwise intact cats by comparing the present results with those previously obtained (Frigon and Rossignol 2007). Similar adaptive changes in cats with intact and transected spinal cord would indicate that the spinal cord is strongly involved in mediating these changes after muscle denervation.
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METHODS |
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Animals and general procedures
Three adult cats (two males, one female), weighing between 3.5 and 5.0 kg, were first selected based on their ability to walk for prolonged periods on a treadmill and trained for a few weeks at their preferred speed (0.35–0.5 m/s). Cats were then chronically implanted with electrodes for EMG recordings and nerve stimulation, allowed to recover from the implantation, and then values of EMGs and reflexes were recorded. A complete transection of the spinal cord was then made at the 13th thoracic segment (T13). Once a stable spinal locomotion was achieved, after a period of 26–41 days of treadmill training, control values were obtained for a few weeks followed by a denervation of the left LGS. Recordings resumed the day after the denervation, for 
31 days. Two of these cats were used to describe changes in Tib nerve reflexes after spinalization (Frigon and Rossignol 2008a).
Implantation of electromyographic electrodes, recording, and processing
Chronic electromyographic (EMG) electrodes were implanted bilaterally in the following hindlimb muscles: 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), medial gastrocnemius (MG: ankle extensor/knee flexor), and tibialis anterior (TA: ankle flexor). 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, Pointe-Claire, Canada) and sown into the belly of each muscle for bipolar EMG recordings. The tips of the electrode wires were exposed for 2–4 mm. EMG recordings were band-pass filtered (100–3,000 Hz) and amplified (gains of 0.5–10K) using two Lynx-8 amplifiers (Neuralynx, Tucson, AZ). EMG data were digitized (5,000 Hz) using custom-made acquisition software. The duration, mean amplitude, and timing of the EMG bursts during locomotion relative to onsets of left St bursts were calculated using custom software. Mean amplitude was defined as the area under the rectified EMG burst divided by its duration and expressed as a percentage of the averaged control value (i.e., pooled data from three predenervation sessions). Over the course of the study some EMG recordings were lost in each cat, as determined by the disappearance of EMG signals.
Tibial nerve stimulation and reflexes
A chronic stimulating electrode composed of bipolar wires (AS633; Cooner Wire) embedded in a polymer (Denstply International, Milford, DE) cuff (Julien and Rossignol 1982) was placed around the intact left Tib nerve at the ankle adjacent to the Achilles’ tendon. The Tib nerve was stimulated (Grass S88 stimulator) at different intensities during locomotion with a single 1-ms pulse at a constant time (100 ms after onset of St burst) to determine the threshold for obtaining small, yet consistent short-latency (
10 ms) responses in the left TA. The current delivered was controlled and monitored using a custom-made constant-current generator set to 1.2-fold the threshold. Once reflex responses were qualitatively and quantitatively reproducible from one session to another for a few weeks (
22 days), the same current was used before and after denervation. In all testing sessions, a stimulus was given once every three cycles at pseudorandom times within the step cycle to elicit about 10 responses in the different parts of the step cycle divided in 10 equal parts for a total of approximately 120–200 stimuli. After the initial implantation substantive scar tissue forms around the stimulating electrode and stabilizes it and it is thus improbable that the afferent volley evoked at the stimulating electrode changed over time.
Reflexes were measured as detailed previously (Frigon and Rossignol 2008a,b). 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. Averaged responses of EMGs with stimulation were separated into these 10 bins according to the time they were evoked in the cycle. An average of 50 control cycles provided a template of baseline locomotor EMG (blEMG) during the step cycle. Onsets and terminations of responses, denoted as prominent negative or positive deflections 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), such as N1 or P1 (8–10 ms) and P2 (25 ms), where "P" denotes positive (excitatory) responses. Short-latency excitatory reflex responses (P1) from the ipsilateral (i.e., side of stimulation and denervation) St and TA as well as the longer-latency excitatory response (P2) from the ipsilateral VL were analyzed after denervating the left LGS. These muscles were chosen because reflex changes were notable in the ipsilateral St and TA in our previous study and the VL is a muscle that frequently displays increased activity after denervating the ipsilateral LGS. For P1 responses of the ipsilateral St and TA the same windows were used pre- and postneurectomy (St: 10–25 ms; TA: 10–30 ms). Longer-latency excitatory responses (P2) were not measured in St or TA because these responses are either absent or reduced following spinalization (Frigon and Rossignol 2008a). For the ipsilateral VL, response onsets and terminations were manually determined because P2 onsets differ slightly throughout the stance phase due to varying durations of the short-latency inhibitory response. Short-latency inhibition (N1) in VL was not quantified because this response is reduced after spinalization (Frigon and Rossignol 2008a).
To measure reflexes, the stimulated and nonstimulated EMGs within the determined window were integrated. The nonstimulated integrated EMG within the same window was then subtracted from the integrated stimulated value. Because reflex amplitude is known to scale (i.e., automatic gain control) with the level of EMG activity (Matthews 1986), the subtracted value was then divided by a fixed 15-ms block of blEMG in the same phase (for an example, see Fig. 1 of Frigon and Rossignol 2008b), thus giving a reflex amplitude normalized to the level of baseline locomotor activity. For St and TA, reflex responses evoked during swing (data points at phases 0.05 to 0.35) and those evoked during stance (data points at phases 0.45 to 0.85) were averaged together to provide an average reflex response during swing and stance, respectively. Reflex responses of the ipsilateral VL were analyzed only during stance (i.e., data points at 0.45–0.85). These reflex responses were then expressed as a function of the average control value (i.e., pooled data from three predenervation sessions).
Spinalization and training
Spinalization procedures were identical to those of previous studies (Bélanger et al. 1996; Frigon and Rossignol 2008a). In the early days after spinalization, training consisted of having two experimenters move the hindlimbs over the motorized treadmill to simulate locomotion while the forelimbs were positioned on a fixed platform located about 3 cm above the belt. The skin of the perineal region was stimulated to facilitate stepping movements. A Plexiglas separator was placed between the limbs to prevent them from impeding each other because of increased adduction. Initially, the experimenter supported the hindquarters by lifting the tail. After spinalization, recording sessions resumed once a steady locomotor pattern was attained, with the experimenter providing equilibrium by gently holding the tail (Barbeau and Rossignol 1987; Bélanger et al. 1996). This occurred after 26–41 days.
Neurectomy
The left LGS nerve was cut by carefully separating the nerve from its surrounding tissue in the popliteal fossa and the proximal end was capped with flexible vinyl polysiloxane (Reprosil; Dentsply International) to prevent nerve regeneration (Frigon and Rossignol 2007). The anesthesia and surgery for the neurectomy lasted <1 h and cats were tested the next day to allow sufficient recovery from surgery. Postmortem analyses confirmed that the LGS nerve was cut and did not regenerate in each cat.
Statistics
To determine statistical differences for locomotor EMG bursts, data from the last three sessions recorded before denervation (control) were averaged and compared with each day postdenervation using a one-way ANOVA. A Dunnett's post hoc test for many comparisons against a control group was performed if significant changes were detected by the ANOVA (Bouyer and Rossignol 2003b; Bouyer et al. 2001). Reflexes were analyzed identically except that each reflex response in swing or stance was treated independently. For example, the average reflex response during swing in the left St in the control state was compared against the average reflex response during swing in the left St for all days after the neurectomy.
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RESULTS |
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), there was little change in the quality of locomotion. Spinal cats had no difficulty in maintaining the same treadmill speed as that before denervation the day following the neurectomy. There were, however, several changes in locomotor EMG bursts in multiple hindlimb muscles in the days following denervation. Moreover, reflex responses during locomotion were altered in some muscles after denervating the left LGS. Changes in locomotor EMG bursts after denervation
The EMG bursts in several hindlimb muscles were investigated during locomotion before and after denervating the left LGS in chronic spinal cats to determine whether the neurectomy produced changes in multiple muscles, as is the case in otherwise intact cats (Frigon and Rossignol 2007). Figure 1 shows EMG bursts for selected muscles before (left) and 2 days after (right) denervating the left LGS in cat 1. The burst magnitude and/or duration of several muscles, particularly Srt bilaterally and the right VL, were altered 2 days postneurectomy in this cat. Before the neurectomy the Srt burst discharged during the swing phase but, by 2 days postdenervation, there was a large burst during stance as well.
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22 days postdenervation. Each colored line illustrates a different muscle. In all cats there was an increase in the mean EMG burst amplitude of some muscles of both hindlimbs following denervation. For instance, in cat 1 (Fig. 2, top), muscles of the right leg (Srt, VL, LG), contralateral to the neurectomy, and the left VL showed large increases in the first few days postdenervation. In cat 2 (Fig. 2, middle) the left MG had a considerable increase postdenervation that remained so for the rest of the study, whereas the EMG activity of other muscles (left and right Srt, right LG) increased in the first few days postneurectomy. In cat 3 (Fig. 2, bottom), the mean EMG burst amplitude of the left Srt, left VL, right MG, and right LG increased in the days following denervation. Therefore as in otherwise intact cats (Frigon and Rossignol 2007), denervating the left LGS in chronic spinal cats produced changes in the activity of multiple muscles bilaterally and the amount of changes in specific subsets of muscles could differ from one cat to another.
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The Tib nerve was stimulated before and after denervating the left LGS to determine whether reflex responses are altered following denervation in chronic spinal cats, as is the case in otherwise intact cats (Frigon and Rossignol 2007). Figure 3 shows responses in the left St evoked by stimulating the left Tib nerve in cat 1 (Fig. 3A) and cat 2 (Fig. 3B) in 10 bins of the step cycle before and at 1 and 10 days postdenervation. In cat 1 (Fig. 3A), P1 responses either decreased or were unchanged 1 day after denervation and returned to predenervation values at 10 days (phases 0.05 and 0.25) or could be increased (phase 0.15). P2 responses were mostly absent throughout the step cycle except for phase 0.05 and were not greatly affected by the neurectomy. However, in cat 2 (Fig. 3B), P1 responses increased throughout the step cycle 1 day postdenervation, particularly during the stance phase (i.e., hatched responses in phases 0.45–0.85). At 10 days postdenervation responses during stance remained elevated, albeit reduced compared with 1 day. Changes in reflex responses in cat 3 resembled those of cat 1 and are not illustrated.
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) and will be briefly reiterated in the appropriate sections to put the current data into context.
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). Over time these responses tended to return toward predenervation values. In the present study, P1 responses of the ipsilateral St were altered after denervating the left LGS (Fig. 4), particularly in cats 2 and 3. In these two cats changes were much greater during stance than during swing. For example, in cat 2 P1 responses during stance increased to about 1,400% of the control value 2 days postdenervation before gradually returning to control values. During swing, P1 responses increased more gradually, reaching a peak at 7 days, before returning to control values. In cat 3, P1 responses during swing and stance increased over time, although increases were much greater during stance. In cat 1 increased P1 responses during swing and stance followed a similar pattern of change and were significantly increased only at 13 days postdenervation. Thus in intact and spinal animals denervating the left LGS produces changes in Tib nerve reflexes in the ipsilateral St, which are most evident during stance.
In two intact cats P1 responses in the ipsilateral TA, evoked by stimulating the left Tib nerve, tended to increase over time and after a few weeks they returned toward predenervation values (Frigon and Rossignol 2007). In one cat, P1 responses increased over time and remained increased after several weeks. In all cats, prominent changes were found equally during swing and during stance. In the present study, P1 responses of the ipsilateral TA were modified in all cats after denervation (Fig. 5). Cats 1 and 3 had a similar pattern of reflex change during swing and stance. During swing, responses tended to increase over time, except for the large increase at 2 days postdenervation in cat 3, whereas during stance, responses were generally decreased postdenervation. Responses during swing remained elevated 3 wk postdenervation in cats 1 and 3. In cat 2, reflex responses during swing and stance increased in the days postdenervation before gradually returning to control values. Thus as is the case in the otherwise intact cats, P1 responses of the ipsilateral TA can increase over time and remain elevated (cats 1 and 3) or increase gradually and return to predenervation values (cat 2).
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Therefore reflex responses in some muscles were modified after denervation of the left LGS in chronic spinal cats. Reflex responses evoked during stance and swing in ipsilateral flexors could change in parallel (e.g., ipsilateral St of all cats) or independently (e.g., ipsilateral TA of cats 1 and 3). Large changes in reflex responses were observed in the ipsilateral St and TA, even though these muscles showed little change in mean EMG burst amplitude postdenervation. In contrast, reflex responses in the ipsilateral VL were unchanged postdenervation, even though this muscle could undergo changes in mean EMG burst amplitude after denervation. This clearly shows that changes in reflex responses dissociate from those of the underlying background level of EMG.
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DISCUSSION |
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), a clear demonstration that the spinal cord can compensate for the motor and/or sensory loss. Whereas Bouyer et al. (2001) investigated changes in kinematics of the denervated hindlimb and in the activity of close remaining synergists, such as MG and plantaris, we evaluated changes in locomotor bursts and reflex responses evoked by Tib nerve stimulation of several muscles of both hindlimbs.
Overall, there were some changes in step cycle duration and burst onsets after denervation (see Table 1), but these were relatively small compared with the large modifications in locomotor EMG bursts and reflexes. Changes in the mean amplitude of locomotor bursts of multiple muscles bilaterally were found in the days following the denervation (Figs. 1 and 2), as is the case in otherwise intact cats (Frigon and Rossignol 2007). Moreover, there were several changes in reflexes after denervating the left LGS, as shown previously in otherwise intact cats. The results indicate that intrinsic spinal mechanisms are involved in increasing muscle activity in multiple hindlimb muscles bilaterally and in effecting reflex changes following a partial denervation of ankle extensors, although supraspinal and/or propriospinal inputs most certainly also contribute after a muscle denervation in cats with an intact spinal cord.
Postdenervation changes in EMG bursts
Data presented here and elsewhere (Bouyer et al. 2001; Bretzner and Drew 2005a; Frigon and Rossignol 2007) indicate that changes in the activity of multiple muscles of both hindlimbs mediate functional recovery following muscle or cutaneous denervations, although large changes are evident and most prominent in synergists following lesions of muscle nerves in otherwise intact (Pearson et al. 1999; Tachibana et al. 2006) or chronic spinal (Bouyer et al. 2001) cats. Modified activity in several muscles could reduce the demand for increased force generation imposed on remaining synergists, some of them by providing simple biomechanical advantages, until more long-term adaptive mechanisms develop (Bouyer et al. 2001), such as muscular hypertrophy (Walsh Jr et al. 1978; Whelan and Pearson 1997). As in otherwise intact cats (Frigon and Rossignol 2007), the subset of muscles showing increased activity following the denervation in chronic spinal cats could vary from one cat to another. Therefore even though walking is somewhat different in intact and spinal cats (Bélanger et al. 1996), an increase in the activity of multiple muscles appears to mediate the functional recovery after partially denervating ankle extensors.
Changes in reflex pathways following denervation
Postdenervation, reflex pathways from the Tib nerve were altered in the ipislateral St and TA (Figs. 4 and 5), but not in the ipsilateral VL (Fig. 6). Some of the reflex changes described here were similar to those of our previous study in intact cats (Frigon and Rossignol 2007). For instance, we showed previously that P1 responses in the ipsilateral St were increased during stance in the first few days postdenervation in intact cats, which were also observed in cat 2 of the present study. Moreover, following denervation in intact cats, P1 responses of the ipsilateral TA during swing and stance tended to increase gradually over time and returned to control values, or remained elevated. In the present study, changes in P1 responses of the ipsilateral TA followed a similar time course during swing (i.e., increase over time that was maintained or returned to predenervation values) but, during stance, responses were decreased postdenervation in cats 1 and 3. Thus despite some similarities in reflex changes between intact and chronic spinal cats there are also some differences. Similarities in reflex changes following denervation in intact and chronic spinal cats suggest that spinal mechanisms are involved in mediating changes in cutaneous reflex pathways following a muscle denervation.
On the other hand, differences in reflex changes after denervation in intact and spinal cats suggest that different mechanisms also subserve reflex changes when the spinal cord is intact. Descending supraspinal inputs are known to influence the excitability in cutaneous reflex pathways in anesthetized cats (Fleshman et al. 1988) and during intact locomotion (Bretzner and Drew 2005b) and could influence changes in reflex pathways following LGS denervation. One study showed that corticospinal efficacy increased after a cutaneous denervation of the hindpaw in the cat during locomotion (Bretzner and Drew 2005a), suggesting that descending inputs from cortical areas are involved in functional recovery by increasing the excitability in spinal circuits. Although these studies have not directly shown that supraspinal inputs are involved in modifying cutaneous reflex pathways following a muscle or cutaneous denervation it was demonstrated that the corticospinal tract is required in operant conditioning of the soleus H-reflex in rats (Chen and Wolpaw 1997; Chen et al. 2006). Thus supraspinal structures are most likely involved in mediating some of the changes in reflex pathways following LGS denervation in cats with an intact spinal cord.
In the present study, reflex responses during swing and stance could change in parallel, albeit with different magnitude, after denervation. This is most evident in the ipsilateral St of all cats (Fig. 4) and in the ipsilateral TA of cat 2 (Fig. 5B). It is possible that sensory inputs from the LGS nerve, which are normally evoked during stance, are important for the phase-dependent modulation of cutaneous reflex pathways from the Tib nerve. Consequently, sectioning the LGS nerve could remove part of this phase-dependent modulation and reflexes during swing and stance change in parallel.
Variability in reflex changes
Cutaneous reflexes, evoked by stimulating a given cutaneous nerve, in otherwise intact or chronic spinal cats can differ from one individual or animal to another during locomotion (Frigon and Rossignol 2008a; Loeb 1993; Zehr et al. 1997). This interanimal variability in reflex pathways indicates that spinal sensorimotor circuits are shaped by experience and training. Consequently, it is not surprising that an identical nerve lesion produced different patterns of changes in reflexes (see Figs. 4 and 5) and in locomotor EMG bursts (see Fig. 3) because the spinal circuitry is inherently different from one animal to another, even though the locomotor adaptation is similar. It is important to note that despite different adaptive changes in reflex pathways and locomotor EMG bursts all cats offset the loss of two ankle extensors. In other words it appears that the spinal circuitry is "programmed" to produce an appropriate locomotion in a number of ways after a muscle denervation. On the other hand, that reflex pathways and locomotor EMG bursts are modified in intact and chronic spinal cats suggest that there is a propensity for the spinal cord to adapt locomotion via set mechanisms.
Mechanisms of recovery
Although reflex responses could be increased or decreased in the ipsilateral St (Fig. 4) or TA (Fig. 5) the mean amplitude of the locomotor EMG burst of these muscles was relatively unchanged after denervation (Fig. 2). Moreover, reflex responses in the ipsilateral VL were unchanged after denervation (Fig. 6), even though mean amplitude of this muscle is generally increased postneurectomy (Fig. 2). This clearly shows that changes in reflex pathways from the Tib nerve dissociate from those occurring at the motoneurons, inferred by EMG recordings, indicating that premotoneuronal mechanisms must be involved in mediating reflex changes after LGS denervation.
However, this does not exclude that other reflex pathways mediate increased activity in hindlimb muscles. Pearson and colleagues (1999) hypothesized that group I afferents from remaining synergists (i.e., MG) could mediate increased homonymous burst activity because the MG muscle is more stretched and must produce more force after denervating the LGS. However, changes in muscle length following denervation of the left LGS in chronic spinal cats did not parallel changes in the activity of the left MG (Bouyer et al. 2001) and, in another study, stretch reflexes evoked in MG following denervation of synergistic ankle extensors in otherwise intact cats simply scaled with the underlying muscle activity, demonstrating that the gain of MG group Ia pathways was unchanged (Gritsenko et al. 2001). Therefore it is not likely that increased muscular activity is directly mediated by changes in reflex pathways.
The most likely explanation for the increased muscle activity is an enhanced central drive from the spinal CPG (Frigon and Rossignol 2007; Gritsenko et al. 2001; Pearson et al. 1999), which can simultaneously mediate increases to multiple muscles. Changes in reflex pathways, including those from the Tib nerve, could provide important signals to the spinal CPG because sensory feedback from large-diameter afferents is required for functional recovery following partial denervation of ankle extensors (Pearson et al. 2003). Proprioceptive inputs from the LGS nerve normally project to several interneuronal targets within the spinal cord and influence the excitability of other proprioceptive and cutaneous pathways (McCrea 2001; Rossignol et al. 2006). Consequently, the loss of LGS proprioceptive inputs changes the excitability of reflex pathways from other sources, thus modifying signals that project to the spinal CPG and other interneurons. These altered inputs could be sufficient to signal the CPG that changes in muscle activity are required to compensate for the loss of two ankle extensors.
Locomotor adaptation following denervation of the left LGS in intact cats no doubt results from the interplay between spinal and supraspinal mechanisms, although the present results suggest that the spinal cord contributes strongly because adaptive mechanisms (i.e., changes in EMG bursts and reflexes) were similar in chronic spinal cats. Changes in sensory inputs could provide an important signal to the spinal CPG to effect changes in multiple hindlimb muscles because cutaneous reflex pathways from the Tib nerve are altered after denervation.
The present results clearly demonstrate that the spinal cord, in the absence of supraspinal inputs, can adapt to further challenges, such as a peripheral nerve lesion, and that reflex pathways can be modified at the spinal level after a complete spinal cord transection. This reinforces the idea that reflex pathways can be targeted to strengthen the locomotor circuitry after spinal cord injury (Barbeau et al. 1999). For example, reflex pathways after spinal cord injury could be further modified via training and pharmacological and electrical stimulation. As a result, because the spinal cord possesses a rich and complex adaptive circuitry, promoting appropriate changes within reflex pathways could facilitate the recovery of motor functions following lesions to the spinal cord or to peripheral nerves.
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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, Department of Physiology, Groupe de Recherche sur le Système Nerveux Central, Faculty of Medicine, Université de Montréal, P.O. Box 6128, Station Centre-Ville, Montreal, Quebec, Canada H3C 3J7 (E-mail: serge.rossignol{at}umontreal.ca)
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