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REPORT
1Rehabilitation Neuroscience Laboratory, University of Victoria, Victoria, British Columbia; and 2International Collaboration on Repair Discoveries, Vancouver, British Columbia, Canada
Submitted 19 May 2004; accepted in final form 13 August 2004
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ABSTRACT |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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; Pearson 1993). In the cat, research on the pattern of backward and forward walking support the concept that spinal CPGs may simply run in reverse when the movement direction changes (Buford and Smith 1990, 1993; Perell et al. 1993). During human locomotion, it has been shown that for some joints (especially the hip) kinematics and to a lesser extent EMG of backward walking are similar to those of forward walking (Grasso et al. 1998; Thorstensson 1986; Winter et al. 1989). However, electromyographic (EMG) amplitudes are typically higher during backward walking compared with forward walking (Duysens et al. 1996; Grasso et al. 1998; Thorstensson 1986; Winter et al. 1989). The similarities between forward and backward locomotion could reflect the activity of CPG networks running in reverse to produce backward walking. Indeed Grasso et al. (1998) suggest that their data support the activity of similar CNS mechanisms operating to regulate forward and backward walking. It has also been suggested that the same CPG mechanisms may regulate various patterns of gait in the infant (Lamb and Yang 2000).
Modulation of motor activity due to changes in peripheral feedback during rhythmic movement can be used to infer the activity of CPG circuits (Burke 1999; Burke et al. 2001; Zehr and Duysens 2004). For example, the modulation of cutaneous reflexes during rhythmic movement has been suggested to arise due to activity of a human locomotor CPG (Duysens and Tax 1994; Zehr et al. 2001), and this could explain phase- and task-dependency of reflexes via premotoneuronal gating of afferent feedback (Dietz 2002a, b; Duysens and Tax 1994; Duysens and Van de Crommert 1998; MacKay-Lyons 2002). It has been shown that cutaneous and H reflexes are phase and task dependent during arm cycling (Zehr and Chua 2000; Zehr and Kido 2001; Zehr et al. 2003). Further, reflexes evoked by stimulation of cutaneous nerves in the hand and foot are both phase and task dependently modulated in arm muscles during the natural arm swing of walking (Haridas and Zehr 2003; Zehr and Haridas 2003). These observations support the suggestion that rhythmic arm movements are to some extent regulated by CPGs just as posited for the leg (Dietz 2002a, b; Dietz et al. 2001; Zehr and Duysens 2004; E. P. Zehr, T. J. Carroll, R. Chua, D. F. Collins, A. Frigon, C. Haridas, S. R. Hundza, and A. Kido, unpublished data).
Duysens and colleagues (1996) studied cutaneous reflex modulation evoked by electrical stimulation of the sural nerve during forward and backward treadmill walking. Modulation of reflex amplitude throughout the step cycles could be generally explained by a CPG running in "reverse" when going backward. However, the pattern was not strictly simply reversed as some muscles showed minor timing differences and shifts during backward locomotion. This observation was similar to the pattern of cutaneous reflex modulation seen during forward and backward walking in the cat (Buford and Smith 1993). There it was suggested that the central control of cutaneous reflex amplitude was similar for forward and backward quadrupedal walking (Buford and Smith 1993). In this paper, we undertook to replicate this kind of experiment during arm cycling where it is relatively easy to perform a simple reversed movement during backward versus forward cycling. For example, both backward and forward leg cycling generate very similar phase-reversed patterns of muscle activity (Eisner et al. 1999; Ting et al. 1999). The purpose of the experiment described in this paper was to test the hypothesis that cutaneous reflexes evoked during backward arm cycling would show a similar but reversed pattern of modulation to that seen in forward arm cycling. Support for this hypothesis would further add to the evidence for CPG contributions to rhythmic human arm movement (Zehr and Duysens 2004) such as has already been demonstrated for the cat forelimb (Yamaguchi 2004).
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METHODS |
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Protocol
The experimental methodology and protocol are similar to that described in previous experiments involving reflex modulation during walking (Zehr and Haridas 2003) and arm cycling (Zehr and Chua 2000; Zehr and Kido 2001; Zehr et al. 2003). Thus only differences in methodology are highlighted here. Participants performed rhythmic arm cycling using a previously described arm ergometer (e.g., Zehr et al. 2003). Arm cycling was performed in a forward direction (in which clockwise movement of the right arm can be observed from the right side) and then in a backward direction in separate trials.
Nerve stimulation
Electrical stimulation was delivered pseudorandomly throughout the movement cycle to the superficial radial nerve (SR) at the wrist of the right hand with trains of 5 x 1-ms pulses at 300 Hz (Zehr and Haridas 2003; Zehr and Kido 2001) applied with a Grass S88 (Grass Instruments, AstroMed) stimulator connected in series with an SIU5 isolator and a CCU1 constant current unit. The SR nerve was stimulated at approximately twice the threshold for radiating paresthesia through bipolar surface electrodes placed just proximal to the radial styloid on the right arm. Appropriate stimulation location was verified by determining that sensation was evoked in the innervation area of the SR nerve (dorsolateral portion of the right hand).
EMG
Bilateral bipolar recordings were made from shoulder muscles anterior (AD) and posterior (PD) deltoid, elbow muscles biceps (BB) and triceps (TB) brachii, and the wrist flexor carpi radialis (FCR) muscles. EMG signals were preamplified and band-pass filtered at 100–300 Hz (P511 Grass Instruments, AstroMed).
Data acquisition and analysis
Data were sampled at 1,000 Hz with a 12-bit A/D converter connected to a computer running custom-written (Dr. Timothy Carroll, University of New South Wales, Australia) LabView (National Instruments, Austin TX) virtual instruments. Post hoc the movement cycle was divided into 12 equidistant bins or phases that represent positions on the clockface and responses to stimuli in each bin were averaged. "Control data" obtained from cycles without nerve stimulation were used to create subtracted traces (
10–20 observations per bin) of reflex EMG (Zehr and Kido 2001).
EMG analysis
Reflexes were examined at early (50–80 ms) and middle (80–120 ms) latencies. During analysis for a given subject all subtracted reflex traces for a muscle (i.e., for all 12 bins) were plotted, and the mean and SD of the prestimulus EMG was calculated as an index of subtraction error. Reflex amplitudes at each latency were considered significant and included in the analysis if they exceeded a 2 SD band calculated from this residual. To quantify the reflex amplitudes, a 10-ms window centered on the peak of each response was calculated at early and middle latency. All EMG and reflex amplitudes were normalized to the maximum control background EMG recorded during forward cycling for each muscle.
Statistics
ANOVA was used to determine main effects and statistically significant reflex amplitudes as well as phase dependency during forward and backward cycling (Statistica, Statsoft). This analysis was conducted on datasets averaged across all subjects. Tukey's HSD test was used to post hoc significant main effects (e.g., significant differences between direction). Linear regression analysis using Pearson's correlation (r) was conducted between reflex amplitudes and background control EMG for each muscle at each phase to determine the extent to which variations in reflex size were linearly related to changes in background muscle activation during forward and backward arm cycling. For this regression analysis all data from each subject were used giving 9° of freedom and yielding a critical r of 0.602 at P < 0.05. Descriptive statistics included means ± SE. Statistical significance was set at P 
0.05.
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RESULTS |
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Background rhythmic EMG amplitudes were significantly (main effect P < 0.05) modulated by phase in the movement cycle for all 10 muscles examined. The pattern of EMG activity (i.e., the amplitude of EMG activity relative to phase in the movement cycle) when examining forward and backward cycling was generally similar for most muscles (see Fig. 1). However, EMG during backward cycling was higher (main effect for direction P < 0.05) than during forward arm cycling for half of the muscles studied (iAD, iPD, iBB, cAD, and cBB; see Fig. 1). Note that in Fig. 1 EMG amplitudes are plotted such that the arm position is the same for forward and backward cycling and thus the two directions can be directly compared. To specifically contrast EMG amplitude in the two directions, amplitudes are expressed as percentages of peak EMG amplitude during forward arm cycling. Significant differences between forward and backward amplitudes at each phase (deduced from post hoc for significant interaction, P 0.05) are as indicated (*).
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Time to the peak response for the early and middle latency reflexes are shown in Table 1 for forward and backward arm cycling and did not significantly differ between the movement directions.
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Reflex amplitudes at early and middle latency were similarly modulated during forward and backward arm cycling. That is, excitatory or inhibitory reflexes were seen at comparable phases in either forward or backward cycling and were of similar amplitude and corresponding sign. Shown in Fig. 2 are reflex traces from iPD muscle for a single subject during forward (A, left) and backward (A, right) arm cycling. The numbers shown to the left of Fig. 2A indicate the phase in the movement cycle relative to the clock face. Note that the orientations are the same for forward and backward cycling allowing for direct comparison. The excitatory responses during both directions of cycling are highlighted by the gray rectangles. In Fig. 2B, reflex traces during forward and backward cycling are shown superimposed. These traces are from phases (3–4 o'clock) where background EMG levels were similar for this subject and where the arms where in similar orientations. The similarity between the responses can be seen clearly. It is also observed that the excitatory responses may persist across a greater portion of the movement cycle for backward arm cycling (from 1 to 6 o'clock) as compared with forward cycling. Note as well that the pattern of responses in PD muscle differs somewhat from the other muscles studied in that a large early latency excitatory burst dominates with only very small responses at middle latency. This can be seen in Fig. 2 for a single subject as well as in Figs. 3 and 4 described in the following text for all subjects.
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0.05) for these interactions are shown in Figs. 3 and 4 (*). Note that this analysis identifies if the reflex amplitudes during forward and backward cycling were significantly different at each movement phase. As can be seen there are few instances of significant differences between arm cycling direction at any given phase in the movement cycle at the early latency (Fig. 3) and none for middle latencies (Fig. 4).
Previously it has been shown that reflex amplitude is typically uncoupled from rhythmic background EMG amplitude during forward arm cycling (Zehr and Kido 2001). To examine the extent to which reflex modulation during backward cycling was coupled to background EMG during backward arm cycling, we examined Pearson correlations here. Across all muscles for forward and backward cycling and at early and middle latency this analysis yielded 40 comparisons. In only 1 instance was a significant relation with background EMG demonstrated (iAD at early latency during forward cycling). Thus during both forward and backward cycling, reflex amplitude was typically uncoupled from rhythmic background EMG.
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DISCUSSION |
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EMG of forward and backward arm cycling
With some subtle differences the general EMG pattern associated with forward arm cycling was maintained during backward motion. For many muscles studied, the magnitude of rhythmic EMG amplitude during backward arm cycling was significantly greater than corresponding values for forward cycling (e.g., see Fig. 1, *). This is similar to the observations reported for EMG amplitudes during forward versus backward walking (Grasso et al. 1998; Winter et al. 1989). There were some shifts in timing of peak activities of certain muscles and minor shifts in the temporal patterns within the movement cycle. This may be similar to previous documentation of EMG during leg cycling that may be due to subtle changes in the biomechanical function of the muscles during backward motion (Eisner et al. 1999; Ting et al. 1999). However, this was not explicitly evaluated in this study and cannot be definitively discussed here. In general, the pattern of EMG during backward arm cycling was similar to forward cycling (see Fig. 1).
Reflex modulation during backward arm cycling
The pattern of cutaneous reflex modulation during backward arm cycling was equivalent to that seen during forward cycling (e.g., see Figs. 2–4). Across both cycling conditions responses in contralateral muscles were typically of smaller amplitude (as seen in Figs. 3 and 4 in which responses are plotted on the same scale across the body), except for iTB and cTB. There are numerous instances of reciprocal coordination at similar latencies in contralateral muscles and in antagonist muscles (e.g., contrast AD and PD responses in Figs. 3 and 4) just as shown previously for SR nerve reflexes during arm cycling (Zehr and Haridas 2003; Zehr and Kido 2001) and walking (Zehr and Haridas 2003). There were some differences in terms of the timing in the movement cycle of maximum reflex amplitudes and the amplitudes themselves. However, the general features were very similar in that there appeared to be no drastic re-organization of the reflex control such that an entirely new pattern arose with backward cycling as compared with forward motion. That is, reflex responses were still phase-modulated and excitation or inhibition still occurred at similar phases and were not replaced by responses of opposite sign in forward versus backward arm cycling. CPG networks "running in reverse" during backward motion could explain this observation in much the same way that this has been used to explain the observed reversal in the pattern of cutaneous reflexes during backward quadrupedal (Buford and Smith 1993) and bipedal walking (Duysens et al. 1996). Buford and Smith (1993) suggested that, although they did observe some differences in the pattern of cutaneous reflex modulation during backward walking, these differences were very subtle and expressed as minor differences in reflex amplitude and general timing. This was also the case for the observations of Duysens and colleagues (1996). These earlier observations describe the current data fairly well. Here, reflex amplitudes and timings were quite similar, but there are some minor differences. For example the pattern shown for arm cycling seems close to a simple reversal that is much "cleaner" than that seen in leg muscles during walking. Perhaps this reflects the clear symmetry between directions in the arm cycling task (e.g., continuous task evenly distributed) which is not present during walking (e.g., continuous task with uneven distribution of activation for swing and stance).
It is notable that reflex amplitudes were uncoupled from background EMG irrespective of arm cycling direction. Previously it has been suggested that this is an indicator of the activity of CPG mechanisms during rhythmic movement (Haridas and Zehr 2003; Komiyama et al. 2000; Van Wezel et al. 1997; Zehr and Haridas 2003; Zehr and Kido 2001). The current data support the concept that the arms and legs are regulated by the same mechanisms during rhythmic motion that is independent of movement direction and that a portion of this control can be ascribed to CPG-like activity. Interestingly, data on human infants suggest a common CPG for walking that is independent of movement direction (Lamb and Yang 2000; Pang and Yang 2002). The current results thus extend to the human upper limb many of the features of reflex modulation observed during lower limb locomotor control and add further to the evidence suggesting similar control mechanisms (e.g., CPG contributions) to the generation of the rhythmic arm muscle activation pattern during arm cycling and walking.
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GRANTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: E. P. Zehr, Rehabilitation Neuroscience Laboratory, PO Box 3015 STN CSC, University of Victoria, Victoria, BC V8W 3P1, Canada (E-mail: pzehr{at}uvic.ca)
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REFERENCES |
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