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INTRODUCTION |
Short-latency stretch reflex responses are mediated primarily by muscle spindle feedback and have been shown to scale with velocity of stretch (Gottlieb and Agarwal 1979
; Lee and Tatton 1982
; Tatton and Bawa 1979
) over broad ranges of stretch velocity ranges [e.g., a range from 30 to 150°/s was used in Lee and Tatton (1982)
Fig. 4]. Such data concur with findings that muscle spindles are sensitive to muscle stretch velocity and to some extent amplitude in cats (Loeb et al. 1985
; Prochazka et al. 1979
) as well as in humans (Vallbo et al. 1979
).
We have examined the relationship between stretch input and reflex output from a different approach. We hypothesized that traditionally measured inputs to the system (e.g., the velocity of an external movement or whole muscle velocity) may not accurately represent the mechanical input to the muscle spindles, especially when the background forces are small. Previous investigations have suggested that the length changes imposed upon muscle spindles during locomotion are not simply related to changes in the parent muscle length (Hoffer et al. 1989
, 1992
). During active movements, extrafusal fibers can shorten while the muscle is lengthening and vice-versa, and thus muscle spindle lengths cannot be expected to mirror the whole muscle length profile. The pinnation angle of local fibers, the compliance of aponeurotic tissues, and location of a spindle within the muscle also contribute to the spindle response.
Unlike other studies, we did not vary the external perturbation. Instead, we compared the actual changes in cat medial gastrocnemius (MG) muscle length and muscle fiber length at two locations in response to similar ankle rotations. The actual extent of the muscle stretch varied slightly from trial to trial because of variations in posture and in levels of muscle activation. We examined the relationship between local fiber stretch velocity (input variable) and the corresponding local reflex electromyographic (EMG) amplitude (a measure of the neural output) to determine how muscle spindle feedback participates in postural control. Preliminary findings appeared in abstract form (Eng et al. 1996
).
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METHODS |
Three adult male cats (mean mass: 6 kg) were trained to stand unaided on four circular pedestals (50 mm diam) and to maintain a desired force level with the left hindlimb before and after 10° rotations about the left ankle joint (causing a 11-mm displacement of the central foot pad with a rise time of 30 ms) (see Sinkjaer and Hoffer 1987
, 1990
for detailed apparatus and training protocol). The cats were cared for in accordance with Canadian Council for Animal Care and American Physiological Society guidelines, and the experimental procedures were approved by the Simon Fraser University Animal Care Committee. Once the cats were proficient at this task, the following transducers were surgically implanted in the left hindlimb (see Fig. 1): a muscle length gauge that spanned from origin to insertion of the MG muscle, a tendon force transducer, thermistor, pairs of piezoelectric crystals to measure MG fiber length based on ultrasound transit-time (Sonomicrometer 120, Triton Technology), and closely spaced bipolar stainless steel electrodes (Cooner Wire Company, AS 631) to record local EMG activity (see Caputi et al. 1992
; Hoffer 1990
; Weytjens et al. 1992
for further description of these devices). EMG electrodes and crystals measured MG muscle activity and fiber length, respectively, both in a proximal region and a distal region (Fig. 1). Surgical anesthesia was maintained with Halothane and oxygen and an analgesic/sedative was administered for a minimum of 24 h postoperatively.

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| FIG. 1.
Illustration of implanted devices in cat hindlimb. ···, location of proximal medial gastrocnemius (MG) muscle fibers (at 30-35% of total length of MG muscle belly) and distal muscle fibers (at 70-80%) recorded using sonomicrometry.
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Data collection began 1 wk postsurgery to allow for encapsulation of crystals by connective tissue and intimate attachment to the aponeuroses. The cat stood quietly on the pedestals while perturbations of random direction (lengthening or shortening) were presented 100 ms after the pedestal force had remained within a prescribed window. Pedestal force, pedestal position, a time code, EMG, length, tendon force, and crystal signals were recorded on 20 channels of FM tape (DC
10 kHz per channel). Fifteen to 20 lengthening trials were collected for each cat, depending on his ability to maintain the desired posture and background force.
Signals were digitized off-line at 1 kHz per channel. Rectified EMG, fiber, and muscle length signals were processed through second-order, 0 lag, 100 Hz low-pass filters followed by differentiation of the latter two signals to obtain velocity profiles. The peak fiber or muscle velocity was defined as the first peak value after the perturbation. The onset of the reflex EMG burst was defined as the time when the signal amplitude rose above the background level (measured in a 50-ms window before the perturbation) and the end of the burst was defined as the time when the signal returned to baseline without further activity in the next 3 ms. The amplitude of the EMG burst was computed as the area of the burst from onset to end of the burst.
Linear regression and Pearson product moment correlations were tested between peak muscle velocity and peak fiber velocity and mechanical input (peak fiber velocity or peak muscle velocity) and the reflex output (EMG amplitude within the same muscle region or across regions). As multiple correlations were tested, an alpha of 0.02 was used to minimize Type I errors. Preliminary analyses used variants of the measures including the mean value of the EMG burst, the slope of the muscle or fiber velocity profile, and the initial muscle or fiber velocity (10 ms after the first detectable rise in velocity). Similar relationships were found using these variables.
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RESULTS |
Responses to muscle stretch
Normal variations in standing posture resulted in slight deviations in initial muscle and fiber lengths from trial to trial. Initial lengths ranged within ±2 mm for the muscle and ±1 mm for the fibers. Activation of the MG muscle was generally modest during quiet standing. Baseline MG tendon forces ranged from 3 to 5 N, about 30% of the peak forces reached during moderately paced locomotion. A typical trial is shown in Fig. 2. Simultaneous with the pedestal rotation, the MG tendon force and muscle velocity both rose. The tendon force typically doubled its original value within 20 ms. Within 1-2 ms of the start of rise in muscle velocity, the velocity of the proximal and distal fibers also started to increase and reached the first peak value 10-15 ms later. The stretch amplitude ranged from 1 to 3 mm for the muscle and 1-2 mm for the fibers. EMG reflex bursts started 6-8 ms after the rise of the corresponding local fiber velocity and lasted 20-30 ms.

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| FIG. 2.
Pedestal movement (a), tendon force (uncalibrated) (b), muscle length (c), local fiber length (d and e), muscle velocity (f), local fibre velocity (g and h), and local reflex EMG (i and j; cat 2) recorded during a typical trial.
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Local fiber velocity does not represent the whole muscle velocity during the postural task
The peak local fiber velocity (distal or proximal) was not significantly correlated with the whole muscle velocity in any of the cats (Table 1). Although the pedestal rotation was similar across trials, the velocity of stretch of the MG muscle and its fibers tended to vary from trial to trial. This variability could depend on various initial factors including fibre pinnation angles, muscle and fiber lengths, levels of activation of MG and other muscles, intrinsic properties of the active fibers (stiffness of the active cross bridges), and viscoelastic properties.
Reflex EMG responses correlate with local fiber velocity but not muscle velocity
Correlations of the peak local fiber velocity with the corresponding local reflex EMG response were evaluated. R values ranged from 0.51 to 0.82, indicating that
67% of the variability in the local reflex EMG was accounted for by the corresponding local fibre velocity (Fig. 3). Correlations for the distal muscle region were somewhat lower than those in the proximal region (Fig. 3) but were still significant (P < 0.02).

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| FIG. 3.
Local electromyogram (integrated area of reflex burst) plotted against peak velocity of stretch of corresponding local fibers. All correlations were significant (P < 0.02).
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In contrast, correlations between the peak stretch velocity of the MG muscle and EMG reflex responses (proximal or distal) were not significantly different from 0 (P > 0.05). Thus the reflex activation of the MG muscle did not scale with the length changes in the parent muscle.
Evidence of regionalization of the stretch reflex
In cats 1 and 3, the reflex EMG burst area depended on the velocity of stretch of local fibers (Fig. 3). In contrast, fiber stretch velocity in the proximal region and reflex EMG area in the distal region were not significantly correlated (Table 1). The same was found for the distal fiber velocity and proximal reflex EMG area. Correlations between the proximal and distal reflex EMG activity and between the proximal and distal peak velocity were assessed and shown to be nonsignificant (Table 1). This further supported the notion that the stretch reflex amplitude is regulated locally.
In cat 2, the local EMG response also depended on the local fibre stretch velocity (Fig. 3). However, fiber stretch velocities in the proximal and distal regions tended to be closely correlated in this cat, as were the EMG response amplitudes in the proximal and distal regions (Table 1), masking any possible regional specificities. As a result, cross-correlations of the proximal input with the distal output and distal input with the proximal output were significant in cat 2.
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DISCUSSION |
Muscle spindles monitor local fiber length
The lack of correlation between moment-to-moment muscle stretch and muscle fiber stretch found during this postural task concurs with the earlier finding of disparate, site-specific fiber movements within the MG muscle during locomotion (Hoffer et al. 1992
). Furthermore, the lack of correlation between muscle stretch and reflex EMG suggests that muscle length is not a globally monitored variable during active posture. On the other hand, the significant correlations found between local fiber length changes and corresponding reflex EMG amplitudes indicate that during postural tasks, muscle spindles monitor changes in local fiber length.
It is expected that if the pedestal rotations had comprised a broad range of velocities, a relation between whole muscle velocity and EMG output would have emerged (see Gottlieb and Agarwal 1979
; Lee and Tatton 1982
; Tatton and Bawa 1979
). However, by using the same external perturbation for all trials, the muscle velocity was constrained purposely within a narrow range in this study. What was interesting in this study was that inherent differences in fiber stretch velocity in response to matched external perturbations had a direct effect on the amplitude of the neurally mediated reflex output. This effect reveals the very fine, localized control of muscle fiber lengths and the segmental regulatory role played by muscle spindle feedback.
These results may have been enhanced by the relatively low forces and muscle activation levels required during this postural task. It remains possible that at higher forces, the muscle fiber and whole muscle profiles would become more alike as all structures become more rigidly linked within a stiffer muscle.
Reasons for variability in reflex responses
Up to 67% of the variability in the neural output (reflex EMG response amplitude) could be explained by changes in local fiber length. What factors might comprise the rest of the variability during this task? Projections from muscle spindles located in remote parts of the muscle or in synergist muscles could account for some of the variability. Descending drive to the motoneurons and/or fusimotor set (Prochazka et al. 1988
) could be distributed unevenly through the muscle. Cutaneous and proprioceptive feedback from the foot can have substantial contributions in generating reflex EMG in the cat (Bonasera and Nichols 1994
; Nichols 1989
; Sinkjaer and Hoffer 1990
) that also may be selectively distributed. Last, some variability may have been a result of measurement errors (e.g., EMG amplitude) or the selection of the most appropriate input (peak velocity) or output variables (EMG burst area).
Stretch reflex action is localized within the muscle
Site-specific fiber length changes and their corresponding reflex EMG demonstrate that stretch reflex action is localized within the muscle. The relationship can be somewhat surprising in light of the known neuronal divergence of Ia-afferent projections that are distributed to all the motoneurons that innervate the homonymous muscle as well as to synergist motoneurons (Mendell and Henneman 1971
). These present results suggest the presence of spatial weighting of the projection strength of Ia afferents onto the motoneurons, with those motor units in closest proximity to the receptor having the greatest effect. This regionalization is further supported by the lack of correlation found between proximal and distal regions in cats 1 and 3.
The local action of muscle spindle feedback within the receptive field concurs with earlier evidence that stretch sensitivity of afferents is dependent on their location within a muscle (Meyer-Lohmann et al. 1974
; Stuart et al. 1988
). The demonstration of a relationship between local fiber velocity and corresponding reflex EMG in awake cats supports the hypothesis of local reflex circuits proposed by Windhorst et al. (1989)
; this hypothesis, until now, had only been supported by limited data from reduced preparations.
The proximal and distal regions of the MG muscle differ in architectural and mechanical factors such as relative movement at the knee and ankle joints, site-specific muscle fiber lengths and pinnation angles (Hoffer et al. 1992
), and complex patterns of aponeurotic movement (Qi et al. 1994
). There is debate as to whether such factors necessitate regional control or in contrast, perhaps, regional stretch sensitivity is an outcome of these factors (Windhorst et al. 1989
). Regionalization could explain the large variability of afferent activity profiles that have been reported within individual muscles (Loeb et al. 1985
; Prochazka et al. 1989
).
In conclusion, direct recordings with sonomicrometry used in this study have shown that muscle fiber lengths are controlled regionally during postural tasks. These findings extend the findings of Hoffer et al. (1992)
, who reported regional fiber length changes in the MG muscle during cat locomotion. Muscle spindle feedback appears to participate importantly at the segmental level, and its impact is greatest in the reflex regulation of nearby muscle fibers.