The Inhibition of short latency reflex linking the pretibial muscles to quadriceps motoneurones during stance to swing transition in humans.
Objective: The modulation of short latency reflex linking the pretibial to quadriceps muscle (CPQ reflex) was investigated in seven subjects during walking on a treadmill at the stance to swing transition period.
Methodology: The intensity of quadriceps (Q) EMG was increased throughout the gait cycle by using a modified knee orthosis. Pairs of spring were added to the orthosis to produce different levels of muscular activity in Q during the midstance, transition period and terminal swing phase of gait. Electrical stimulation was applied to the common peroneal nerve (CPN) at these three instants of gait.
Results: The peak to peak amplitude of CPQ reflex was significantly increased with escalation of background EMG in Q during midstance (pLess than0.015) and terminal swing (pLess than0.04). At the transition period however, despite significant increase in the Q activity no responses was evoked. Conclusions: The results were indicative of an active inhibition of the reflex pathway during transition period. This inhibition could help the unloading of the limb that is necessary for the initiation of the swing phase.
KEY WORDS: Quadriceps, Reflex, Gait, Inhibition, Swing Phase.
How to cite this article:
Kalantari KK, Baxendale RH, Rezasoltani A. The Inhibition of short latency reflex linking the pretibial muscles to quadriceps motoneurones during stance to swing transition in humans. Pak J Med Sci 2011;27(1):162-166
The spinal cord in humans1,2 contains circuitry capable of generating alternating activity for stereo- typical limb movements such as walking. While the motor output associated with human walking is thought to be largely generated by spinal centers, both supraspinal and afferent input contribute considerably to the locomotor output.3 Considerable evidence derived from both animal and human experiments suggests that specific afferent input to the spinal cord such as hip proprioceptors, Group-I muscle afferents and plantar cutaneous afferents play a significant role in modulating reflex transmission during walking and standing. One aspect of the sen- sory control of gait is the control of the transition from the stance to swing phase. Both hip and ankle affer- ents responding to stretch and load respectively reset the locomotor rhythm, signifying their impact on the walking pattern.4,5
Practically the hip joint has to reach a certain extended angle for the swing phase to be initiated,6 and the extensor muscles to be unloaded.7 In humans, evidence suggests that hip angle is critical for soleus H-reflex8 and flexion reflex9 modulation. It has been shown that the amount of load and hip extension in infants can delay the swing phase.10
There is increasing evidence that Group I and II excitatory pathways play a crucial role in the control of bipedal stance and gait. In contrast to the Group- I projections which are weak and unlikely to pro- vide strong reflex support, the Group-II excitatory pathways play a crucial role in the control of bipedal stance and gait.11 In man, stimulation of the common peroneal nerve (CPN) has been shown to evoke biphasic excitation of quadriceps (Q) motoneurones with the earlier phase attributed to non-monosyn- aptic Group-I and the later phase to Group-II affer- ents.12 It has been shown that the interneurones in this reflex pathway are the convergence point for different ascending13 and descending regulating pathways.12 The concept that this reflex pathway could be modulated by different descending and ascending inputs could suggest its important role in reflex adjustments of different sequences of normal gait or the pathological gait.14,15
It is shown that this reflex modulates profoundly during gait.16 During early stance phase it shows a very strong appearance followed by an areflexic period from midstance to the end of the swing phase. The nature of this quiescent period is unclear since Q is inactive during this period. It is known that a minimum background activity in Q is needed to re- veal the reflex.17 It is not known whether the absence of the reflex is the result disfacilitation or an active inhibition is involved. Accordingly, in the present study the intensity of activity in Q has been increased artificially to reveal the pattern of modulation of this reflex pathway during the relatively quiescent period of gait cycle.
Twelve volunteers (5 male and 7 female, age 25+-5) were studied during walking on a treadmill. None of the subjects had any history of neuromuscular injury or systemic disease. Each participant provided informed written consent, and the experimental protocol was approved by local Research Ethics committee.
Each experiment consisted of 3-5 minutes continuous Surface EMG recording from tibialis anterior (TA), vastus medialis (VM), rectus femoris (RF), of the right leg during which 40 stimuli were applied in pseudo-random sequences. A small pres- sure switch (1cm'2cm), which did not interfere with normal gait, were located on the heel of the right shoe. The trigger pulse from the heel switch passed through a digital delay width module (NL 401, Digitimer Ltd, Hertfordshire, England) in order to adjust different delays to trigger the stimulator and signal averaging.
In order to increase the knee extensor muscle activity during silent periods of gait a modified knee orthosis was used. By adding one or two pairs of springs (20N each) to a knee brace, a variable flexion moment was applied to the knee joint. Three differ- ent configurations of the knee orthosis i.e. orthosis alone and with one and two pairs of springs, were tested for each subject. The correct position of the orthosis was confirmed by obtaining a resistance-free and full range of knee flexion for each subject at the start of experiment. Two single axis electrogoniometers (Biometrics Ltd, Cwmfelinfach, Gwent) were used to signal the movement of the knee and the ankle during gait.
Enough habituation periods were provided for each subject wearing the knee orthosis, until the sub- ject felt comfortable walking on the treadmill. The speed of the treadmill was adjusted at a comfortable value (3.5- 4.5 k/h).
Electrical stimuli were applied to the CPN at caput fibulae. The intensity of stimuli was set at 2xmotor threshold in tibialis anterior. This was capable to evoke a strong Group I and II volley without inter- fering with the normal pattern of movement during walking. Three time delays from heel strike were adjusted individually to trigger the stimulation dur- ing mid stance, the transition from stance to swing and the terminal swing phase. The fine adjustment for each subject was made individually to set the stimulation near the peak of activity of RF at these three periods. A control recording was done for each knee brace configuration.
Non-rectified EMG from VM, RF and TA were analysed. Forty gait cycles were captured and aver- aged in each configuration. The magnitude of the reflex evoked by the stimulation was measured peak to peak from average of 40 non-rectified EMG samples and normalised by the RMS of maximum voluntary contraction (MVCRMS).
An ANOVA along with post hoc Bonferroni test were applied to the experimental data sets to determine if significant differences existed among the reflex amplitude at different instants of gait with different investigated configurations. This analysis was performed for VM and RF muscles separately.
The use of springs obviously increased the inten- sity of activity in RF and VM muscles through out the gait cycle. The most prominent change in muscular activity happened at the transition period from stance to swing phase. The activity of RF and VM also started earlier during the swing phase.
Three adjusted instants of stimulation were positioned at about 25% (stance), 65% (stance-swing transition) and 90% (swing) of gait cycle respectively where significant increase in muscular activity was recorded (pLess than0.006, pLess than0.003 and pLess than0.005 at midstance, transition and terminal swing respectively).
The reactions of the Q at these three periods were different (Fig-1). The reflex magnitude in RF and VM increased along with the increase in the muscular activity during midstance and terminal swing phase During the transition period however, all the subjects remained areflexic during this period despite significant increase in the EMG background activity (Fig-4). Average increase of 17% of MVC in the muscular activity occurred during this period that was above the threshold needed for the reflex.
In this study we have established that the pathway conveying signals from pretibial muscles to Q motoneurones goes under significant inhibition during the stance-swing transition period. During the early stance phase of gait a strong activity of the reflex linking the pretibial muscles to Q motoneurones is reported.16 It was suggested that this positive feedback effect could help lower limb to resist the applied load during the early stance phase. We were able to increase the activity of Q during its quiescent period of gait. Electrical stimulation at midstance, elicited reflexes which increase in mag- nitude in proportion to the background EMG. This was similar to early stance phase. It seems that the reflex pathway remains open for activation which is consistent with the necessity of stability and balance for the lower limb during the stance phase. The same reaction to the intensity of the background activity is observed during terminal swing.
The most significant discrepancy occurs during transition from stance to swing. The lack of reflex at this period could not be a simple response to disfacilitation, since the increase in the background EMG during this period was almost the same as the other two periods of gait. It is therefore concluded that an inhibitory effect is present at this period.
Given the current experimental protocol, it is difficult to identify the involved afferents that participated in the inhibition of the CPQ reflex how- ever, indirect evidence can be obtained. The knee and hip joints' position appear to show a correlation with the inhibition seen in the reflex.13 It was shown that knee flexion by 10o to 20o is capable of inhibiting the reflex significantly and the reflex was at its maximum magnitude at extended position of knee. The pattern of knee movement during gait is very consistent with the pattern of modulation of the reflex. During the stance phase knee is near full extension. The reflex must have its maximum potential for activation during this period. This positive correlation between the knee joint position and the reflex excitability could also be seen in the terminal swing phase where the knee is again extended and the reflex can be elicited.
The only period when the knee flexes rapidly and significantly during gait is from the preswing phase to the midswing phase. An average of 22o of flexion was observed in the present experiment. This was sufficient to produce a strong inhibition. This period of maximum flexion movement of the knee was when the maximum inhibition in the reflex was detected.
The hip position has also been proposed for a long time that have critical role in initiating the stance to swing transitiony.4,10 Grillner and Rossignol18 have shown that preventing hip extension in one hind leg in cats terminated stepping movement in that leg without influencing the movement of contra lateral leg. Only when the hip was allowed to extend be- yond a critical angle did stepping resume. It has been reported that stretching or vibrating a hip flexor muscle during the stance phase leads to an earlier onset of swing in walking decerebrate catsy.4 The receptors signalling hip extension are probably the primary and secondary endings of muscle spindles in the hip flexor muscles.5
Afferent actions from the lower limb are evidently switched between inhibition and facilitation depending on the position of the hip, indicating that position of the hip is a control- ling factor of spinal reflex excitability.8,9,19,20 The hip joint movement during gait was not recorded in present experiment but the normal pattern of hip movement suggests that it could participate in the inhibition of the CPQ reflex during the transition period. The hip joint is in a flexed position at heel strike and it moves gradually toward its neutral po- sition by the end of the midstance. The hip reaches its maximally extended position at the end of the stance phase where the inhibition of the CPQ reflex happens. It is plausable that the stretch receptors of the hip flexors may help the transition from stance to swing during gait in humans by boosting the inhibition of the CPQ reflex.
This strong inhibition of the reflex can suggest a functional role during the transition from stance to swing phase. During the transition period the ankle dorsiflexors showed a peak of activity. This helps the foot to clear from the ground and to start the swing phase of gait. Inhibition of CPQ reflex would help the transition from stance to swing phase by prevent- ing of any co-contraction of ankle dorsiflexors and knee extensors. This co-contraction could seriously hinder the flexion of the knee joint that is necessary for unloading and clearance of foot from the ground and start of the swing phase. The results further emphasise the importance of hip and knee proper positioning in rehabilitation of patients with neurological movement disorders.
Authors are grateful to the subjects for their will- ingness to participate on many hours of experimen- tation throughout the project. This study was sup- ported and funded by the Shahid Beheshti Univer- sity of Medical Sciences, Faculty of Rehabilitation.
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|Author:||Kalantari, Khosro K.; Baxendale, Ronald H.; Rezasoltani, Asghar|
|Publication:||Pakistan Journal of Medical Sciences|
|Article Type:||Clinical report|
|Date:||Mar 31, 2011|
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