Modulation of ipsi- and contralateral reflex responses in unrestrained walking cats

Abstract

1. The modulation of reflex responses in up to 10 simultaneously recorded hindlimb muscles was studied in unrestrained cats walking on a treadmill. Single electrical shocks of various strengths were applied to different skin areas of teh hindlimb at different times of the step cycle while the resulting EMG responses were sampled and analyzed. 2. Two excitatory response peaks (P1 and P2) at a latency of about 10 and 25 ms, respectively, were seen in all flexors examined (sartorius, semitendinosus, tibialis anterior, extensor digitorum longus). Stimulation of most skin areas was effective but responses were most easily obtained from stimuli applied to the foot or ankle. During the step cycle there was a marked modulation of the amplitudes of the responses, especially the P2 responses, which grew larger toward the end of stance when a maximum was reached, followed by a steady decline throughout swing. This pattern was very similar for various flexors, although these muscles differed considerably in their normal EMG activity pattern during walking. 3. Flexor responses were absent when the same stimuli were applied during the early stance phase. Instead, inhibition of the ongoing EMG activity was seen at a latency of 10 ms or less in all extensors examined (semimembranosus, quadriceps, soleus, gastrocnemius medialis, flexor digitorum longus). The inhibition was followed by a late excitatory peak (P3) at about 35-ms latency in all extensors except soleus. 4. Certain stimulation sites yielded exceptions to the above patterns. Stimulation of the skin area innervated by the sural nerve yielded larger and earlier MG excitatory responses as compared to stimulation of other skin areas. Activation of the plantar surface of the foot often failed to elicit P2 responses in the hip flexor sartorius, which showed inhibition instead. 5. In the hindlimb contralateral to the stimulus, excitatory responses occurred both in flexors and extensors at a latency of 20-25 ms. The pattern of modulation of these responses was similar to the ipsilateral modulation of P2 flexor and P3 extensor responses. Soleus failed to show a crossed response. 6. The data indicate that flexor and extensor responses differ both with respect to their latency and to their correlation with the ongoing EMG reactivity. It is concluded that these stimuli do not demonstrate reflex reversal in the strict sense in the normal walking cat but that there is modulation of transmission in a flexor excitatory and extensor inhibitory pathway, possibly by the flexor part of the spinal locomotor oscillator. In addition, there are some specialized flexor inhibitory and extensor excitatory pathways. The slow soleus muscle does not seem to be excited through these pathways.

Short-Latency Crossed Inhibitory Responses in Extensor Muscles During Locomotion in the Cat

“…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).…”

“…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 ϳ10 ms and 2 is ϳ25 ms. Excitatory responses in ipsilateral extensors beginning at ϳ35 ms are sometimes termed P3 (Duysens and Loeb 1980) but for simplicity will be referred here as P2.…”

“…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).…”

“…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).…”

Step Training-Dependent Plasticity in Spinal Cutaneous Pathways

“…Nervespecific reflex responses to cutaneous stimulation were previously observed during locomotion in cats (Abraham et al, 1985;Moschovakis et al, 1991;Pratt et al, 1991;LaBella et al, 1992;Degtyarenko et al, 1996) and humans (van Wezel et al, 1997) to provide location-specific information from the skin of the foot. However, a common synergy of flexor responses in the swing phase and of extensor responses in the stance phase was also observed, independent of the location of the stimulus in cats walking on a treadmill (Duysens and Stein, 1978;Duysens and Loeb, 1980;Abraham et al, 1985). Thus, during locomotion, both common and nerve-specific controls of cutaneous reflex responses were observed.…”