Effects of Skin in Triceps
Cooling on Stretch Reflex Activity Surae of the Decerebrate Cat
STEVEN L. WOLF AND EVERT KNUTSSON Department
The effects of selective skin stimulation by cooling on the stretch reflexes in triceps surae were studied in the midcollicularly decerebrated cat. Stretch reflexes were elicited with a muscle puller allowing the determination of responses to dynamic and static stretch. The skin overlying the lateral gastrocnemius was freed into a flap, and 8.6 cm2 of this cooled with a thermoelectric cooling module. Lowering temperature to 10 f 2 C produced an 11% decrease in the tonic component of the triceps surae stretch reflex, without significantly altering the amplitude of the phasic component. Cooling by applying ice cubes to the skin flap, a procedure involving mechanical stimulation, augmented both the tonic (11%) and the phasic (15%) stretch responses. The removal of the ice cubes depressed both responses for 30 sec. It is concluded that selective cooling of the skin receptors can depress tonic stretch reflexes of underlying muscle in the decerebrated cat. This effect differs from the facilitatory effect on phasic and tonic stretch reflexes characteristic of less selective forms of cutaneous stimulation.
INTRODUCTION As several studies have shown, local cooling over spastic muscles may result in a lowering of muscular hypertonus (13, 22, 25, 26). Since the effect is transitory, cooling can be used to improve the long-term value of therapeutic exercises (21) and may also be of importance in differentiating types of muscular hypertonus that respond differently to antispastic medication (18, 19). In part, the reduction of exaggerated stretch reflexes should be the result of temperature effects on the muscle spindles and their nerves, since 1 This work was supported by a postdoctoral fellowship from the Muscular Dystrophy Associations of America, Inc. awarded to Dr. Wolf, and by the Swedish Medical Research Council. We wish to thank Docent L. Haapanen for his valuable technical advice. Dr. Wolf’s present address is : Neurophysiology Laboratory, Road, N.E., Atlanta, Georgia Georiga Mental Health Institute, 1256 Briarcliff 30306. 22 Copyright All rights
0 1975 by Academic Press, Inc. of reproduction in any form reserved.
a lowering of the temperature within the muscle will alter the response characteristics of muscle spindles (9, 23, 29). Changes in the contractile properties of skeletal muscles, though present, do not explain the reflex changes (20, 27) and the spinal transmission of H reflexes does not diminish (20, 27, 33, 34). Consequently, the refles depression during cooling may be ascribed to a lowered inflow from the muscle spindles in response to stretch. Reflex changes are, however, prominent before the intramuscular temperature has been significantly altered (13, 20, 25) and, thus, at least the early stretch reflex depression in response to cooling has been suggested as arising from an altered inflow in cutaneous afferents
(13, 17, 25). In view of these findings and of recent reports suggesting that skin heating or cooling can alter motor responses in lightly anesthetized or decerebrate and decerebrate-spinal cat preparations (32, 35)) we have studied the effects that a comparatively innocuous cooling stimulus, applied to skin freed from underIying muscle, has upon the stretch reflex of the cat triceps surae musculature. Reflex testing, allowing the estimation of effects on tonic and phasic components of the stretch reflex, was employed, and a specific thermal stimulus was delivered by a thermoelectric cooling module which was positioned beneath the outer surface of a skin flap overlying the lateral gastrocnemius muscle several minutes prior to its activation. This study was undertaken in order to determine: (a) whether thermal activation of a cutaneous area isolated from underlying muscle is capable of altering reflex activity, (b) whether there is a differential effect upon static and dynamic motoneuron populations when skin cooling is instituted, and (c) whether this form of thermal stimulation evokes responses differing from those produced by a more nociceptive (pinch) or a nonspecific (icing) input. METHODS The data presented in this study were obtained from ten cats of both sexes, weighing 2.2-3.7 kg. Szrrgical Procedure. Decerebration at the intercollicular midbrain level was performed under ether anesthesia. The recording sessions began no earlier than 1 hour following decerebration. Rectal temperature was maintained at 3639 C by an infrared heating lamp and room temperature ranged from 22-24 C. The left hind limb was shaved and pinned through the femoral condyles for limb stabilization. A longitudinal incision was made 1 cm medial to the posterior midline extending from the inferior border of the popliteal fossa to the calcaneous. Care was taken in dissecting skin from underlying tissue so that blood supply and innervation to the skin and triceps surae
musculature underwent minimal trauma and disruption. Incisions perpendicular to that described above were made at the proximal and distal limits SO that the resulting skin flap, which would have lain over the lateral gastrocnemius, could be deflected laterally on to the cooling device. The exposed triceps surae were covered with several layers of warm salinesoaked tissue paper replenished repeatedly throughout each experiment, This procedure helped to maintain limb temperature at appropriate levels and ensured the insulation of the underlying muscle group from skin cooling effects. Mounting. The triceps surae tendon and a small piece of calcaneus bone were severed, and the most distal 334 cm were separated gently from surrounding tissue. The tendon was attached to a muscle puller using polyester fiber string (Johnson and Johnson, Mersilene 1) so that minimal tension (2Og) was exerted at resting length. The pin through the femoral condyles was secured with the knee in approximately 20” of flexion. In some experiments, attempts were made to separate the lateral gastrocnemius muscle and its tendon from the remaining triceps surae in order to evaluate the effects of skin-flap cooling on the stretch reflex components of this muscle. Hind limb muscle nerves were not disrupted since this procedure presumably alters the central excitatory state ( 1, 16, 28, 31) . Recording. The phasic and tonic components of the stretch reflex were recorded at each muscle stretch. The muscle puller employed (Wilhelm Nass, Hanover, Germany, Type 250561302, 3.3 kp) was converted from an electromagnetic reflex hammer whose rate of pull during maximal excursion (8.3 mm) was calculated as approximately 600 mm/set at midrange with a rise time of 16 msec. A force transducer (four-armed bonded resistance strain gauge, Flygtekniska Forsoksanstalten, Stockholm), with a linear output within the range used at a sensitivity of 2.4 mV/kg, recorded the tension increase during stretch. A linear potentiometer transducer (Swema, Stockholm, RLP25) registered the length excursion of the puller. The degree of stretch could be varied between 5.3 and 8.3 mm, the rate of stretch being constant. The excursion of the puller was adjusted so that the muscle was stretched lO-15% of the in viva resting length. A Grass C4 kymograph camera triggered a Grass S4 stimulator delivering 50 v over a duration of 650 msec at 0.5 cycles/set. The stimulator triggered a relay activating the pulling magnet with a 24 v dc source. The stretches thus obtained in most cats were sufficient to elicit both the phasic and tonic stretch reflexes which add to the tension obtained from the visco-elastic properties of the muscle. The outputs from the length and tension recording transducers were displayed on a Tektronix 502 dual beam oscilloscope. Changes in the phasic reflexes were determined from the peak tension at the early part of the stretch. Tonic stretch reflexes were estimated from the tension level sustained after peak tension. The
recordings include the passive tension resulting from v&o-elastic properties of the muscle. They can be regarded as constant and their inclusion in the determinations will underestimate relative tension changes. E.rperimental Procedure. The skin flap was placed on an 8.6 cm? thermoelectric cooling module (2, 36). By placing the skin in contact with the cold plate several minutes prior to recording sessions,it was hoped that mechanoreceptor activation would reach a steady state, and that only thermosensitive cutaneous receptor activity would be effected by the cooling, Muscle stretch responses during control, cooling, and postcooling periods were recorded at 5 set intervals. The temperature of the skin area cooled was usually lowered to 10 2 2 C from 32 * 1 C, the rate of cooling being approximately 1 C/set. The duration of the cooling varied in different trials, but never exceeded 3 min. In several experiments, two ice cubes 2 x 2 x 1 cm were placed adjacently, and the skin flap was laid over the cubes and held to simulate a skin cooling period. Consecutive cooling, or icing trials, were always separated by at least 15 min intervals in order to ensure a skin temperature return to control levels. In other trials, the effect of gentle manipulation of the skin flap on stretch reflex activity was studied. In each experiment, the effects of a cutaneous nociceptive input on the stretch reflexes was assessedby a gentle squeezing of the skin flap, using a pair of forceps. The pinching force used, when tested on the human hand, was found painful. Pinch began immediately before muscle stretch, and covered the period of stretch. Observation of the contraction of the hind limb musculature in response to this stimulus was used to establish the presence of intact reflex paths. Excessive dessication of the skin flap, a failure to evoke an excitatory response by skin pinch, loss of rigidity, and repeated excessive movements during cooling trials were all factors limiting the number of repeated cooling trials. As a result, five to ten successfultrials were obtained from each preparation. RESULTS Effects of Skin Flap Cooling. The tonic and phasic components of the triceps surae stretch reflex were examined cluring cooling trials using a thermoelectric cooling module over which the deflected hind limb skin flap was placed. Reflex responseswere evoked at 5 set intervals during each trial. Figure 1 illustrates typical responseswhen the skin flap was pinched (A) and cooled (B). In most preparations, skin flap cooling resulted in an inhibition of the tonic response (Fig. 1, B2). This was most prominent during the first four intervals (20 set) following activation of the cooling device. In the first measured response following cooling, a slight faciIitation of the tonic component could be discerned (Fig. 1, B3). Figure 2 shows compiled data from 26 cooling trials in six animals. All these trials were obtained when animaIs displayed a rigid, stable posture,
B FIG. 1. The effect of skin flap pinch (A) and cooling of skin flap (B) on the triceps surae stretch reflex. 1, 2, and 3 are control, stimulus, and post-stimulus tension records respectively. Bl : 5 sec. prior to skin cooling (skin-cold plate interface temperature : 34 C) ; B2: 15 set after initiation of skin cooling (skin-cold plate interface temperature: 12 C) ; B3: 5 set after termination of skin flap cooling (skincold plate interface temperature: 18 C), Triceps surae stretched 1.5% of resting length. Records taken from the same animal. Rising time in BZ is retouched slightly. Calibration : 2OOg, 100 msec.
flexion withdrawal, or pinna reflexes could when crossed extensor, be elicited. As is seen, the tonic component of the triceps surae stretch reflex was initially reduced by 11 + 2.6%, while the phasic component showed a slight elevation, 3.7 * 2.9%. The effects of cooling lasted approximately 30 set for the tonic reflex, and 10 set for the phasic. These effects may partly be caused by cold receptor discharge in response to the change in temperature gradient lasting approximately 22 set, and indicates that tonic members of the triceps surae motor nuclei were more responsive to this thermal input than were phasic motoneurons. After termination of skin flap cooling, the tonic reflex responsewas increased 1.9 + 3.6% above control levels and by 5.9% above the mean amplitude during the last 30 set of cooling. The phasic reflex amplitude was reduced by 6.5 + 2.5% from control level, and by 3.17%from the mean amplitude during the last 30 set of cooling. These findings indicate that tonic and phasic motoneurons respond differently within a 5 set interval following the termination of skin flap cooling, and that for both reflexes the responseswere inverse to those observed at the beginning of cooling, thus indicating a rather small variability in the different trials. Efiects of Skin Flap Icing. When the skin flaps were held over two adjacent ice cubes while reflexes were elicited, an entirely different responsewas obtained. Figure 3 shows that both tonic and phasic amplitudes and
five secondsafter the removal of the icing stimulus, both reflexes had returned to control levels (B3). Figure 4 shows data taken within 5 hours following decerebration from ten icing trials in five preparations. It can
be seen that the influence on tonic and phasic responses tended to run parallel to one another. Five seconds after ice application, the mean tonic reflex amplitude was 8.6 f 3.2% above controls, and the phasic 10.5 -+ 3.6% above control values. These reflex amplitudes remained elevated for more than 1 min, falling below control amplitudes when the skin flap was removed from the ice cubes. After withdrawal of the stimulus, both reflex components remained slightly depressed for 15-30 sec. Standard
1 Cold, off ’
25 50 PHASIC
I IO FIG. 2.
Mean values (*SD) for tonic (upper) and phasic (lower) components of triceps surae stretch reflex as seen for 26 cooling trials in six cats. Ordinates: percentage of control, abscissa; time in 5 set intervals. Gap indicates interval ranging from O-60 set of cooling. Data points following removal of stimulus indicated by open circles. Increasing phasic responses are shown as downward. All data contributing to graph were taken within 5 hr following decerebration.
FIG. 3. Triceps surae stretch reflex responses to skin flap pinch (A) and icing (B). 1, 2, and 3 are control, stimulus and post-stimulus records respectively. Upper traces: length records; lower traces: tension records. Triceps surae stretched 15% of resting length. Records taken from same animal. Calibration for lower tracts: 2OOg, 100 msec. See text for further description.
deviations ranged from 1.1-5.6s thus suggesting slight variation in the effects. Effects of Nociceptive Skin Flap Stimulation. When the skin flap was squeezed responsessimilar to those seen in Fig. 1 (A2) were observed. Both the phasic and tonic responses were increased more by nociceptive stimulation than by skin flap icing or manipulation. Occasionally, an animal responded to a nociceptive stimulus with rapid ankle extensor contractions, as illustrated in Fig. 3 (A2). Eflects of Skin Flap Manipulation. In order to determine whether only holding the skin flap could affect tonic and phasic reflex amplitudes, a series of reflexes were evoked when the skin was held as in icing trials. The results from one trial are shown in Fig. 5. The phasic reflex amplitude was increased substantially, while the tonic component was increased only slightly. However, in other trials both reflexes were increased markedly. In most cats, the responsesto skin flap manipulation were not as large as when the skin flap was iced. Consequently, skin flap icing in these experiments must be viewed as a nonspecific input, since quantitatively it is possible that varying numbers of pressoreceptors and mechanoreceptors as well as thermoreceptors and thermosensitive pressoreceptors contribute to reflex responses. Effects on Lateral Gastrocnemizts Stretch Reflex. In several experiments, the lateral gastrocnemius muscle was separated from the remaining triceps surae at the calcaneal insertion and freed from other ankle ex-
tensors as far proximally as possible. This was undertaken to gain information concerning the relationship of skin stimulation to muscle activity in the specific underlying muscle. Figure 6 illustrates that skin flap icing produced a larger increase in tonic and phasic reflex amplitudes (A2) than did skin flap manipulation (B2). Thus, the reflex changes observed with these applied stimuli ran parallel to those seen when the entire triceps
1 100 3 SE 2 90 s
-II T cem
120 4. Mean values (*SD) for tonic (upper) and phasic (lower) components of triceps surae stretch reflex as seen for ten icing trials in five cats. Ordinates: percentage of control, abscissa: time in 5 SW intervals. Gap indicates intervals ranging from O-60 set of skin flap icing. Data points following removal of stimulus indicated by open circles. Increasing phasic responses are shown as downward. All data contributing to graph were taken within 5 hr following decerebration. FIG.
FIG. 5. The effect of skin flap manipulation on triceps surae stretch reflex. 1, 2, and 3 are stretch reflexes elicited before, during, and following manipulation respectively. Upper traces : length records ; lower traces : tension records. Muscles stretched to 15% of resting length. All records taken from the same animal. Calibration for lower traces : ZOOg, 100 msec.
surae reflex was evoked by the same stimuli. However, these experiments were discontinued becauseit was felt that the lateral gastrocnemius muscle had not been sufficiently separated. It is believed that the contractions observed in the entire triceps surae complex while lateral gastrocnemius was being pulled could have been contributory to lateral gastrocnemius responsesby continuous action proximally and consequently, it cannot be said that lateral gastrocnemius was truly “separated.” DISCUSSION The results of this study suggest that while decerebrate cats maintain a rigid extensor posture, a cutaneous stimulus, capable of specifically 1
FIG. 6. The effect of skin lateral gastrocnemius stretch during, and after application lower traces: tension records. taken from the same animal.
flap icing (A) and skin flap manipulation (B) on the reflex. 1, 2, and 3 are stretch reflexes elicited before, of stimuli respectively. Upper traces: length records ; Muscle stretched to 15% of resting length. All records Calibration for lower traces: 2OOg, 100 msec.
activating thermosensitive receptors without effectively altering the thermal environment of subcutaneous structures, can produce opposite responses in tonic and phasic motor cells of nuclei comprising the triceps surae complex. Utilizing the stretch reflex, it was possible to demonstrate that the tonic component, which presumably is a measure of tonic motoneuron activity, was depressed most noticeably during the 20 set interval after skin cooling was begun; while the phasic response, an index of phasic motoneuron activity, appeared slightly elevated for approximately 10 sec. The contributions made by each member of the triceps surae complex, however, could not be assessed by the present experimental design ; yet it can be assumed that, in accordance with Burke’s physiological classification of triceps surae motoneurons, a large percentage of the tonic response was provided from soleus motoneurons (4). With respect to the present results, it should be noted that Creed et al. (6) observed that electrical stimulation of hindlimb cutaneous nerves in decerebrate cats produced an inhibition of the slow soleus and a simultaneous increase of the fast gastrocnemius muscle when tension was measured during superimposed stretch of triceps surae. The predominating inhibitory response to skin flap cooling complements findings from studies of decerebrate cats in which reductions in medial gastrocnemius electromyographic activity and hyperpolarization of triceps surae motoneurons were observed when the same thermal stimulus was employed (35, 37). That the effects can be attributed to the thermal stimulus and not to spontaneous variation in the central excitatory state of rigid preparations is a plausible conclusion since (a) tonic and phasic responses were of an opposite nature immediately following cold plate activation, and (b) within the first 5 set after the termination of skin flap cooling phasic and tonic reflex responses showed an “off” or “rebound” effect indicated by their reversed behavior with respect to activity at the beginning of cooling. The latter response is analogous to the rebound phenomenon described by Wolf (35) using more precise measuring techniques. On the other hand, when thermal stimulation was not specific (icing)because the skin flap had to be manipulated or when nociceptive and mechanical stimuli were applied-both tonic and phasic reflexes were augmented. The phasic response to skin flap icing was always greater than the tonic, which implies that input other than specific cooling appears to be processed in such a way as to enhance preferentially phasic motoneuron responses. However, at present, no systematic evaluation has been made to support this contention. Similarly while the abrupt withdrawal of all cutaneous input might have contributed to the prolonged reduction (20 set) in tonic and phasic responses following removal of the skin flap from the icing stimulation, a precise explanation for this finding cannot be offered at this time.
3% increased reflex responses which were noted during skin flap icing, pinching, and manipulation generally conform to the observations made by Sherrington (30), and elaborated upon by Hagbarth (12), and Eldred and Hagbarth, (8) in that skin stimulation above ankle extensors facilitated activity in these muscles. Additionally, it has been shown that natural cutaneous stimuli including touch or pressure (3, 15), ear twist (IO), and head movements (7, 11) are all capable of producing increased gamma activity in decerebrate or spinal animals. The effects imposed on motor cells responding to cutaneous cooling through the gamma Ioop must be considered. However, no attempt was made in the present study to evaluate these effects. It should be noted that in formulating the size principle of spinal motoneurons, Henneman, Somjen, and Carpenter (14) did not observe a change in the recruitment order of first tonic and second phasic motoneurons by disrupting the gamma loop while evoking triceps surae stretch responses in decerebrate cats. Furthermore, in previous studies (35) monosynaptic reflex amplitudes were reduced during skin cooling using a cold plate and these responses were recorded from the proximal end of the cut L7 or Sl ventral roots. The concept that spin& motor c+.%s which can be differentiated physiologically respond in a unique manner to an afferent input is not novel. As noted previously, Creed et al. (6) reported differing responses in the soleus and gastrocnemius muscles of the decerebrate cat during electrical stimulation of cutaneous nerves. In contrast to the present study, Megirian (24) observed opposite responses from motor tibers innervating triceps surae musculature when cutaneous pain or pressure stimuli was applied over the ankle estensors. These differences may be reconciled, in part, by the fact that Megirian examined spinalized and immobilized preparations and administered more localized stimuli to undissected skin areas. Burke, Jankowska, and ten Bruggencate (5) have shown that in lightly anesthetized cats, electrical stimulation of cutaneous nerves, at stimulus strengths which activate predominantly myelinated afferent axons, can produce inhibitory postsynaptic potentials in fast triceps surae motoneurons. Their study, thus, also suggests qualitative differences with respect to excitatory and inhibitory inputs from cutaneous afferents to triceps surae motor cells. The data provided from this lend further support to this notion with respect to qualitative behavior of triceps surae motoneurons receiving input elicited by a natural stimulus (skin flap coaling). Comparison of the effects of skin cooling in the decerebrate cat with reflex effects in spastic man must be made with great caution. The mechanisms involved in spastic conditions are not very well understood and they most probably include highly different disturbances of the reflex control in different subjects. Thus, the only conclusion that justly can be made with relevance to cryotechniques in human spasticity seems to be that the
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