Can. J. Physiol. Pharmacol. Downloaded from www.nrcresearchpress.com by McMaster University on 12/22/14 For personal use only.
The effects of cold-induced muscle spindle secondary activity on monosynaptic and stretch reflexes in the decerebrate cat
Received August 17, 1978
CHAPMAN, C , E., MICHALSKI, W.J., and S ~ ~ G UJI.NJ., 1979. The effects of ctsld-il-aduced rs~usclespiildle secorldnry activity on rnonosyl~apticamtl stretch reflexes in the decerebrate cat. Can. J. Physiol. Pkarnnacol. 57, 606-613. The effects of muscle spindle secondary ending activity on the stretch retlex were studied in unanesthetized clecerebrate cats. Activation of seconciary endings was accor-e~plishedby reducing the ~nuscletemperature. This has been shown to cause a sustained asynchronous discharge from secondary endings. Cooling of the rneciial gastrocnen~iusor lateral gastrocnemius--soleus lnusclcs caused an increase in the phasic and tonic components of their stretch reflexes. Cooling of thc relaxed snedial gastrocnemiras mrascle caused similar increases in the components of the stretch reflex of the synergistic lateral gastrocnen~ius-soleras m~uscleand an increase in its ~-r~onosynaptic reflex. It was coa-acludedthat thc facilitatory autogenetic and synergistic efTects of muscle cooling on the stretch and naonosynaptic reflexes were brought about by activity in group l1 afferents from muscle spindle secondary endings ant1 could not be ascribed to any other type of muscle receptor. These results support the concept of an excitatory role for the secoradary endings of the lnuscle spindle in the stretch reflex of the decerebrate cat. CHAPMAN, C . E., MICHALSKI, W. J . , et S~CXJIN, J. J. 1979. 'Fhe effects of cold-induced muscle spindle secondary activity on monosynaptic and stretch reflexes in the decerebrate cat. Can. J. Physiol. ItPharrnacol.54, 606-614. On a ktudi6 ckez des chats ddckrkbr6s raon-anesthksi6s les efTets de l'activite des terminaisons secoiadaires des fr~sea~ax proproceptifs ma~sculairessur le rkflexe rnyotatiyue. L'activation des terminaisons seconctaires est rkale'ske par une diminution de la tetnperature du muscle. I1 a kt6 naontr6 que ceci cause une dkharge soutemue asyr~chronedes terminaisons secondaires. 12e refroidissement du triceps ra~edianoal des muscles triceps lat6al-soleaire cause une augnrentation des composai-atcsphasique et toniyue de leurs r6ilexes myotaticlaaes. 1.e refroidissement du triceps median rel2chC cause des augmentations siinilaires des cornposanstes du refexe myotaticgue des muscles synergistes triceps lateral-solkaire, ainsi qu'une augmentation du r6Aexe monosynaptique. Oia co~nclutque les efTcts autogGn6tiques facilitateurs et synergistes du refroidissement musculaia.~ sur les r6flexes myotatiques et rnonosynaptiqtaes sont produits par l'activite des atTQences dc groupe II des termir~aisonssecondaires des fuseaux proprioceptifs rnusculaires et qu9ils ne peuvelnt Stre attribuks 3i des rkcepteurs rnusculaires d'un autse type. Ces rdsultats supportent le concept d'un r61e excitateur ctes tcrnlinaisons secondaires des filseaux proprioceptifs ~nusculairesdams le retlexe l-alyotatique c h e ~Be chat dk6rkbrk. [Traduit par le journal]
arad Kato and Fukushima (6976). Mattlaews has postulated an autogenetic excitatory role for secThe role of muscle spi~ldlesecondary endings inn ondaries in the tonic stretch reflex of the decerebrate spinal reflex activity is still controversial. In the past, cat (Matthcws 1969, 1970a, %970b, 1972, 1973; group IT nauscle affer-c~ntswere classified as nonh1cGrath and Matthews 1973). Ira recent years this specific " B ~ c x o ~ reflex affercnts," and their dlsclnarge hypothesis has received strong support from the was thought to produce an excitation of ipsilateral work of Kirkwood and Sears (1974, 1975) and flexor motoneurones arad an inhibition of ilpsilateral Stauffcr et a/. (1976). They showed that a stretchextensor motoneurones, regardless of their muscle evoked discllarge of spimcile secondary afferents from of origin (Eccles and Lundberg d 959a; Holmqvist the triceps surae and MG ~nusclesof the cat proet wl. 1960). Exceptions to this reflex pattern have duced autogenetic rne~aaosynapticexcitation of mstobee11 repc~rted,however, by Escles and Lundberg neuroaaes. 6 1959a), Wslmqvist and Lumdberg ( 1961 ) , l&'ilson Iravestigations of the functional role of seccmlary and Kato 6 %9651, Luwdbcrg et a?. 1975: 3 977). activity have been hampered by the lack of a suitA n ~ n ~ , v ~ A T ~MG, I o N mrdiai s: LGS, lateral able means for selectively stimulating these endings. However, in 1975 Michalski and S@guinreported gastrocnemius-soleras; MSK, monosynaptic reflex.
IntrsdncQion
3 1979 National
0008-4212/79 l060606-09$01.00/0 Research Council of Canada/&'onsei%national de recherches du Canada
Can. J. Physiol. Pharmacol. Downloaded from www.nrcresearchpress.com by McMaster University on 12/22/14 For personal use only.
CHAPMAN ET AL.
that cooling of the relaxed, deefferented MG muscilc of the cat elicited a sustained, asynchronous discharge in 65% of thc anuscle spindle secondary endings. They suggested that anuscle cooling could provide a means for testing the ci'fects of secondary activity in spinal reflexes, Consequently, the aim of the present investigation was to examine the effects of cold-induced secondary activity on tlac stretch reflex in the decerebrate cat. The results showed that muscle cooling had an excitatory eff'ect on stretch reflex and MSR in ankle extensor muscles, and it is suggested that a large part of the group I1 afferents from secondary eradings of the muscle spindle play an excitatory role i1.a the phasic and tonic components of the stretch reflex.
Methods Gener~11 Preparations Experiment, were carried out on cats (2-4 kg) following preparation and decerebration at the intercollicular level under ether ane\thesia. Both hind lirmbs. incliading the hips, were denervated except for the R.fG and 1-GS ankle extensor muscles on the left side. Denervation of the left leg and hip included section of the following nerves: femoral, obturator. caudal femoral cutaneous, cauclal cutaneous sural, lateral cutaneous of the thigh, superior and inferior gluteal, hamstring, peroneal, and tibial except for its branches to the triceps surae. The contralateral hind limb was completely denervated. The head, pelvi6. and left leg were rigidly fixed in a heavy nletal frame. During recordings of the monosynaptic reflex, the spine was rzlso fixed and the I-GS denervated. Rectal temperature avas continuously monitored and maintained at between 37 and 38°C by means of an automatically regi~latedheating pad under the abdonaen. Recordings were begun 3-4 h after cessatio~r of anesthe\ia. At this time all animals showed good decerebrnte rigidity, eye blink, pinna, and stretch reflexes. Stretch Repflex The autogenetic effects s f cooling the I,GS or the M G on their stretch reflexes were ia~vestigated in six cats. The effects of cooling the relaxed MG on the stretch reflex of its synergist, the LGS, were tested in 13 other a~rimals.In preparation for recording of the stretch reflex, the left MG and LGS muscles were separated annder warm oil from currounding tissue. The muscle in which the stretch reflex was to be tested was left attached to the calc,aneum. D m ing autogenetic testing the other muscle was denervated and cut free at its insertion. For synergistic testing, the innervated MG was freed at its insertion and allowed to relax. The left tibia was rigidly fixed t s thc frame by means of a heavy pin in each end of the bone so that the %cgformed angles of 90" at the hip and knee. The maxin~alp h y s i s logical extension of the n~uscle (ankle fully dorsiflexed) was measilred before detaching the tendon ~ i t ha chip of bone from the calcaneum. The muscle was then attached to a mechanical stretcher by mean\ of a rigid brass rod clanlped to the chip of bone. The mtiscle was adjusted to an initial length s~achthat the response to a 10-mnl stretch was approximately 7 %of the maxinlal reflex response. The muscle was left rat this initial length between stretches and was recorded as the number s f millimetres less than max-
607
imal physiological extension. Recordings were made with the minscle kept at a tsrnperatiare of 37-38°C and the reflex was slicited repeatedly irntil a stable response was obtained. The rnuccle was then cooled and the stretch reflex and muscle temperatures were recorded during each stretch. The stretcher provided a linear, constant-amplitude ramp stretch of 2-20 rnm at velocities of up to 140 mrnis. 'Tension and length measurements were made through transd~acersincorporated in the stretcher. The stretch applied to the n~ilscle was 10 Inm at l O rnmis beginning from an initial length of 10-17 mm less than maximum. Each stretch was maintained for 10-20 s and applied at 1-min intervals. The rewlts were analyzed in terms of active tension of the reflex rcspsnse. Active tcnsion was calculated by subtractii~g the passive tension (determined at the end of each experiment in the denervated nauscle) from the total response to stretch. The phasic compor-eent of the reflex was taken as the peak response occurring at the end of the dynamic phase of the stretch. A measurement of the response at 4 s after the end of the ramp stretch was considered to be representative of the tonic ccsmponent. In order to facilitate comparison of the results obtained in the varioi~spreparations, the response was expressed in t e r ~ n sof the mean control value (taken as 100%). All means are expressed with the SEM. ,44c~rrohy n(lpticb Testing.
The effects of hllG cooling trn the nflonosynaptic reflex elicited in the 1,CS were studied in 12 decercbrate cats. Spinal segments 1 3 to S% were exposed by laaninectomy and ventral roots 1*6 to $I on the left side were cut along with all the dorsal roots below S f . The exposed cord was covered with warm mineral oil and maintained at 37°C by meails of a heat lamp. Nerves to the triceps surae were maintained at 37°C by means of a small oil pool and heating coil in the popliteal fossa. Single test shocks were delivered to the central end of tkc LGS nsrve through bipolar silver - silver chloride electrode\ and stimr~li (intewsity 0.08- 0.3 V; 0. I ms duration) were applied at a frequency of 0.5 Hz. The test shock was just sufficient to elicit a maxirnal MSR which was recorded Prom k 7 or S1 ventral roots using col~ventionalelectrsphysio%ogicaItechniques. Pw the graphs, each pcsint is the anzeanr value of 20 responses, expressed as a percentage of the mean control response. In every experiment, the latter was obtained after the reflex had stabilized, and represents the average of valiaes recorded during a 10- to 20-min control period before muscle cooling began. Alnsclc Cooling and Merrsurenlon: o f iA4ltsc.Ee Te~iizperararres The method of muscle cooling was sirrailar to that described by Michalski and Siguin (1975) and cooling plates were applied to the skin as shown in Fig. 1 . Ibliascle temperatures were measured by means of disc thermistors at the outer sirrface crf the n~uscleand needle thermistors at the inner surface of the muscle. All anzr~scletemperatures referred to in the text represent the temperature of the muscle surface furthest away from the cooling pl:ite. When cooling the MG, measurenaents were made at points 1 and 2 (Fig. 1 ) and in some experiments at 3 and 4 as well. When cooling the LGS, measurements were made at points 3 and 4. In experiments where the effects of M G cooling on the LGS stretch reflex were examined, the following precautions were taken to rniiaimize the spread of cooling to the LGS: the outer (lateral) surface of the I,GS was kept warm (above 36°C) by means of a heat lamp and insulation was some-
608
C A N . J. PHYSHBL. P I l A.RMACC>&. VOL. 57. 1979
Can. J. Physiol. Pharmacol. Downloaded from www.nrcresearchpress.com by McMaster University on 12/22/14 For personal use only.
B
H 5 crn FIG. 1. This figure illustrates the placement of thermistors used for monitoring muscle temperatures in various experiments. ( A ) Semidiagrammatic cross section of the leg (looking caudally) illlastrates the major muscles and positions of the cooling plates (CP) during coc~lingof the MI
The effects of cold-induced muscle spindle secondary activity on monosynaptic and stretch reflexes in the decerebrate cat
Received August 17, 1978
CHAPMAN, C , E., MICHALSKI, W.J., and S ~ ~ G UJI.NJ., 1979. The effects of ctsld-il-aduced rs~usclespiildle secorldnry activity on rnonosyl~apticamtl stretch reflexes in the decerebrate cat. Can. J. Physiol. Pkarnnacol. 57, 606-613. The effects of muscle spindle secondary ending activity on the stretch retlex were studied in unanesthetized clecerebrate cats. Activation of seconciary endings was accor-e~plishedby reducing the ~nuscletemperature. This has been shown to cause a sustained asynchronous discharge from secondary endings. Cooling of the rneciial gastrocnen~iusor lateral gastrocnemius--soleus lnusclcs caused an increase in the phasic and tonic components of their stretch reflexes. Cooling of thc relaxed snedial gastrocnemiras mrascle caused similar increases in the components of the stretch reflex of the synergistic lateral gastrocnen~ius-soleras m~uscleand an increase in its ~-r~onosynaptic reflex. It was coa-acludedthat thc facilitatory autogenetic and synergistic efTects of muscle cooling on the stretch and naonosynaptic reflexes were brought about by activity in group l1 afferents from muscle spindle secondary endings ant1 could not be ascribed to any other type of muscle receptor. These results support the concept of an excitatory role for the secoradary endings of the lnuscle spindle in the stretch reflex of the decerebrate cat. CHAPMAN, C . E., MICHALSKI, W. J . , et S~CXJIN, J. J. 1979. 'Fhe effects of cold-induced muscle spindle secondary activity on monosynaptic and stretch reflexes in the decerebrate cat. Can. J. Physiol. ItPharrnacol.54, 606-614. On a ktudi6 ckez des chats ddckrkbr6s raon-anesthksi6s les efTets de l'activite des terminaisons secoiadaires des fr~sea~ax proproceptifs ma~sculairessur le rkflexe rnyotatiyue. L'activation des terminaisons seconctaires est rkale'ske par une diminution de la tetnperature du muscle. I1 a kt6 naontr6 que ceci cause une dkharge soutemue asyr~chronedes terminaisons secondaires. 12e refroidissement du triceps ra~edianoal des muscles triceps lat6al-soleaire cause une augnrentation des composai-atcsphasique et toniyue de leurs r6ilexes myotaticlaaes. 1.e refroidissement du triceps median rel2chC cause des augmentations siinilaires des cornposanstes du refexe myotaticgue des muscles synergistes triceps lateral-solkaire, ainsi qu'une augmentation du r6Aexe monosynaptique. Oia co~nclutque les efTcts autogGn6tiques facilitateurs et synergistes du refroidissement musculaia.~ sur les r6flexes myotatiques et rnonosynaptiqtaes sont produits par l'activite des atTQences dc groupe II des termir~aisonssecondaires des fuseaux proprioceptifs rnusculaires et qu9ils ne peuvelnt Stre attribuks 3i des rkcepteurs rnusculaires d'un autse type. Ces rdsultats supportent le concept d'un r61e excitateur ctes tcrnlinaisons secondaires des filseaux proprioceptifs ~nusculairesdams le retlexe l-alyotatique c h e ~Be chat dk6rkbrk. [Traduit par le journal]
arad Kato and Fukushima (6976). Mattlaews has postulated an autogenetic excitatory role for secThe role of muscle spi~ldlesecondary endings inn ondaries in the tonic stretch reflex of the decerebrate spinal reflex activity is still controversial. In the past, cat (Matthcws 1969, 1970a, %970b, 1972, 1973; group IT nauscle affer-c~ntswere classified as nonh1cGrath and Matthews 1973). Ira recent years this specific " B ~ c x o ~ reflex affercnts," and their dlsclnarge hypothesis has received strong support from the was thought to produce an excitation of ipsilateral work of Kirkwood and Sears (1974, 1975) and flexor motoneurones arad an inhibition of ilpsilateral Stauffcr et a/. (1976). They showed that a stretchextensor motoneurones, regardless of their muscle evoked discllarge of spimcile secondary afferents from of origin (Eccles and Lundberg d 959a; Holmqvist the triceps surae and MG ~nusclesof the cat proet wl. 1960). Exceptions to this reflex pattern have duced autogenetic rne~aaosynapticexcitation of mstobee11 repc~rted,however, by Escles and Lundberg neuroaaes. 6 1959a), Wslmqvist and Lumdberg ( 1961 ) , l&'ilson Iravestigations of the functional role of seccmlary and Kato 6 %9651, Luwdbcrg et a?. 1975: 3 977). activity have been hampered by the lack of a suitA n ~ n ~ , v ~ A T ~MG, I o N mrdiai s: LGS, lateral able means for selectively stimulating these endings. However, in 1975 Michalski and S@guinreported gastrocnemius-soleras; MSK, monosynaptic reflex.
IntrsdncQion
3 1979 National
0008-4212/79 l060606-09$01.00/0 Research Council of Canada/&'onsei%national de recherches du Canada
Can. J. Physiol. Pharmacol. Downloaded from www.nrcresearchpress.com by McMaster University on 12/22/14 For personal use only.
CHAPMAN ET AL.
that cooling of the relaxed, deefferented MG muscilc of the cat elicited a sustained, asynchronous discharge in 65% of thc anuscle spindle secondary endings. They suggested that anuscle cooling could provide a means for testing the ci'fects of secondary activity in spinal reflexes, Consequently, the aim of the present investigation was to examine the effects of cold-induced secondary activity on tlac stretch reflex in the decerebrate cat. The results showed that muscle cooling had an excitatory eff'ect on stretch reflex and MSR in ankle extensor muscles, and it is suggested that a large part of the group I1 afferents from secondary eradings of the muscle spindle play an excitatory role i1.a the phasic and tonic components of the stretch reflex.
Methods Gener~11 Preparations Experiment, were carried out on cats (2-4 kg) following preparation and decerebration at the intercollicular level under ether ane\thesia. Both hind lirmbs. incliading the hips, were denervated except for the R.fG and 1-GS ankle extensor muscles on the left side. Denervation of the left leg and hip included section of the following nerves: femoral, obturator. caudal femoral cutaneous, cauclal cutaneous sural, lateral cutaneous of the thigh, superior and inferior gluteal, hamstring, peroneal, and tibial except for its branches to the triceps surae. The contralateral hind limb was completely denervated. The head, pelvi6. and left leg were rigidly fixed in a heavy nletal frame. During recordings of the monosynaptic reflex, the spine was rzlso fixed and the I-GS denervated. Rectal temperature avas continuously monitored and maintained at between 37 and 38°C by means of an automatically regi~latedheating pad under the abdonaen. Recordings were begun 3-4 h after cessatio~r of anesthe\ia. At this time all animals showed good decerebrnte rigidity, eye blink, pinna, and stretch reflexes. Stretch Repflex The autogenetic effects s f cooling the I,GS or the M G on their stretch reflexes were ia~vestigated in six cats. The effects of cooling the relaxed MG on the stretch reflex of its synergist, the LGS, were tested in 13 other a~rimals.In preparation for recording of the stretch reflex, the left MG and LGS muscles were separated annder warm oil from currounding tissue. The muscle in which the stretch reflex was to be tested was left attached to the calc,aneum. D m ing autogenetic testing the other muscle was denervated and cut free at its insertion. For synergistic testing, the innervated MG was freed at its insertion and allowed to relax. The left tibia was rigidly fixed t s thc frame by means of a heavy pin in each end of the bone so that the %cgformed angles of 90" at the hip and knee. The maxin~alp h y s i s logical extension of the n~uscle (ankle fully dorsiflexed) was measilred before detaching the tendon ~ i t ha chip of bone from the calcaneum. The muscle was then attached to a mechanical stretcher by mean\ of a rigid brass rod clanlped to the chip of bone. The mtiscle was adjusted to an initial length s~achthat the response to a 10-mnl stretch was approximately 7 %of the maxinlal reflex response. The muscle was left rat this initial length between stretches and was recorded as the number s f millimetres less than max-
607
imal physiological extension. Recordings were made with the minscle kept at a tsrnperatiare of 37-38°C and the reflex was slicited repeatedly irntil a stable response was obtained. The rnuccle was then cooled and the stretch reflex and muscle temperatures were recorded during each stretch. The stretcher provided a linear, constant-amplitude ramp stretch of 2-20 rnm at velocities of up to 140 mrnis. 'Tension and length measurements were made through transd~acersincorporated in the stretcher. The stretch applied to the n~ilscle was 10 Inm at l O rnmis beginning from an initial length of 10-17 mm less than maximum. Each stretch was maintained for 10-20 s and applied at 1-min intervals. The rewlts were analyzed in terms of active tension of the reflex rcspsnse. Active tcnsion was calculated by subtractii~g the passive tension (determined at the end of each experiment in the denervated nauscle) from the total response to stretch. The phasic compor-eent of the reflex was taken as the peak response occurring at the end of the dynamic phase of the stretch. A measurement of the response at 4 s after the end of the ramp stretch was considered to be representative of the tonic ccsmponent. In order to facilitate comparison of the results obtained in the varioi~spreparations, the response was expressed in t e r ~ n sof the mean control value (taken as 100%). All means are expressed with the SEM. ,44c~rrohy n(lpticb Testing.
The effects of hllG cooling trn the nflonosynaptic reflex elicited in the 1,CS were studied in 12 decercbrate cats. Spinal segments 1 3 to S% were exposed by laaninectomy and ventral roots 1*6 to $I on the left side were cut along with all the dorsal roots below S f . The exposed cord was covered with warm mineral oil and maintained at 37°C by meails of a heat lamp. Nerves to the triceps surae were maintained at 37°C by means of a small oil pool and heating coil in the popliteal fossa. Single test shocks were delivered to the central end of tkc LGS nsrve through bipolar silver - silver chloride electrode\ and stimr~li (intewsity 0.08- 0.3 V; 0. I ms duration) were applied at a frequency of 0.5 Hz. The test shock was just sufficient to elicit a maxirnal MSR which was recorded Prom k 7 or S1 ventral roots using col~ventionalelectrsphysio%ogicaItechniques. Pw the graphs, each pcsint is the anzeanr value of 20 responses, expressed as a percentage of the mean control response. In every experiment, the latter was obtained after the reflex had stabilized, and represents the average of valiaes recorded during a 10- to 20-min control period before muscle cooling began. Alnsclc Cooling and Merrsurenlon: o f iA4ltsc.Ee Te~iizperararres The method of muscle cooling was sirrailar to that described by Michalski and Siguin (1975) and cooling plates were applied to the skin as shown in Fig. 1 . Ibliascle temperatures were measured by means of disc thermistors at the outer sirrface crf the n~uscleand needle thermistors at the inner surface of the muscle. All anzr~scletemperatures referred to in the text represent the temperature of the muscle surface furthest away from the cooling pl:ite. When cooling the MG, measurenaents were made at points 1 and 2 (Fig. 1 ) and in some experiments at 3 and 4 as well. When cooling the LGS, measurements were made at points 3 and 4. In experiments where the effects of M G cooling on the LGS stretch reflex were examined, the following precautions were taken to rniiaimize the spread of cooling to the LGS: the outer (lateral) surface of the I,GS was kept warm (above 36°C) by means of a heat lamp and insulation was some-
608
C A N . J. PHYSHBL. P I l A.RMACC>&. VOL. 57. 1979
Can. J. Physiol. Pharmacol. Downloaded from www.nrcresearchpress.com by McMaster University on 12/22/14 For personal use only.
B
H 5 crn FIG. 1. This figure illustrates the placement of thermistors used for monitoring muscle temperatures in various experiments. ( A ) Semidiagrammatic cross section of the leg (looking caudally) illlastrates the major muscles and positions of the cooling plates (CP) during coc~lingof the MI
