EXPERIMENTAL
Adaptation
NEUROLOGY
52,
49-57 (1976)
to Long-Term Stretch in the of Muscle Spindles1
Passive
Discharge
ALFREDMAIER 2 AND EARL ELDRED Dcpartmwt
of Anatomy alzd the Brain Research California at Los Angeles, Los Angclrs, Reccivcd
February
Institute, California
University 90024
of
17,1976
The effect of long-term stretch on the discharge of muscle spindles was studied by placing a cast on one hindlimb of cats so as to keep the calf region under moderate extension and after 2 to 6 weeks comparing responses of gastrocnemius al&rents on casted and unrestrained sides to step wise extensi,on of the muscle. The mean slope of the frequency-length relationshi#p for populations of afferent fibers from immobilized limbs showed mixed effects. Th’e slope was less in three animals, greater in three, and not significantly different in four. Th.ree cats in which the calf region had been under stretch for only 3 to 5 days also demonstrated reduced sensitivity. In contrast, all cats in an earli#er series in which the leg had been casted for 2 to 7 weeks with the calf muscles at resting length, showed greater stretch sensitivity. It is concluded that the spindl’e receptor adapts to long-term str’etch of the muscle with a decrease in stretch sensitivity.
INTRODUCTION After a muscle has been held near its resting length for several weeks by means of a cast, its spindles are found to show increased position sensitivity compared to afferent units in the contralateral unrestrained limb (6). This increase in ‘the discharge frequency-length relationship could arise from true adaptation of the spindle mechanism due to the lax state of the muscle, or it might be a more indirect consequenceof the rather extensive atrophy that develops in extrafusal tissue surrounding the spindle. If adaptation is the cause of the increase, then spindles in a muscle maintained under stretch should conversely show a diminution in position sensitivity. Atrophy would be present in both experimental conditions, 1 Supported by USPHS Grant NS 01143. 2 Dr. Maier is now at the Department of Anatomy, mingham, Alabama 35294. 49 Copyright All rights
0 1976 by Academic Press, Inc. of reproduction in any form reserved.
University
of Alabama,
Bir-
50
MAIER
AND
ELDRED
although somewhat less extensive in the muscle immobilized under stretch (9). The following observations were made to see if prolonged stretch of a muscle does result in reduced position sensitivity of its spindles. Afferent responses from the cat’s medial gastrocnemius held in extension for several weeks by a cast were compared terminally with spindle responses from the opposite unrestrained leg. The findings from these animals are contrasted with results from our earlier series (6) in which the muscle was held at near the resting length. METHODS Ten adults cats were used for the long-term experiments. While under barbiturate anesthesia, one hindlimb was placed in a plaster cast extending from the thigh to metatarsus, so as to hold the knee nearly fully extended and the ankle dorsiflexed about 30”. In bringing the leg to this position moderate resistance was encountered from the calf muscles. After a period of 2 to 6 weeks, the animal was again placed under deep barbiturate anesthesia, the lumbosacral spinal cord exposed, and a thorough denervation made bilaterally of lumbar, gluteal, and leg regions except for the medial gastrocenemius muscles. The cat was then placed in a hammock and the hindquarters immobilzed by clamps on the spinous processes and the pelvis. Each leg was fixed with the femur in a vertical position and the tibia at a right angle to it, care being taken to have the hindlimbs in precisely symmetrical positions. Extension of the gastrocnemius could be obtained by flexing the ankle, or by connecting the severed tendon to a traversible strain gauge by an inelastic silk thread. An oil pool was formed about the spinal cord, and ventral roots L6 to Sl cut bilaterally. In some animals the integrated sensory discharge from the gastrocnemius muscle was bipolarly recorded from the well-isolated, severed Sl dorsal roots, the amplification of the two recording channels being equalized initially while recording simultaneously from the normal dorsal root. In other animals the activity of units teased from these roots was monitored and photographed on an oscilloscope. Units were identified as originating in spindles by the response exhibited during an induced twitch, but to facilitate collection of sizeable populations of units, the conduction rate was not generally measured. Most units were presumably Ia afferents, as these larger fibers better survive the teasing procedure. On the average, 22 units were monitored per muscle, the smallest sample having nine units. Statistical significance of differences between means for the slopes of length-frequency regression curves and other values was determined by the unpaired t test, with P
Adaptation
NEUROLOGY
52,
49-57 (1976)
to Long-Term Stretch in the of Muscle Spindles1
Passive
Discharge
ALFREDMAIER 2 AND EARL ELDRED Dcpartmwt
of Anatomy alzd the Brain Research California at Los Angeles, Los Angclrs, Reccivcd
February
Institute, California
University 90024
of
17,1976
The effect of long-term stretch on the discharge of muscle spindles was studied by placing a cast on one hindlimb of cats so as to keep the calf region under moderate extension and after 2 to 6 weeks comparing responses of gastrocnemius al&rents on casted and unrestrained sides to step wise extensi,on of the muscle. The mean slope of the frequency-length relationshi#p for populations of afferent fibers from immobilized limbs showed mixed effects. Th’e slope was less in three animals, greater in three, and not significantly different in four. Th.ree cats in which the calf region had been under stretch for only 3 to 5 days also demonstrated reduced sensitivity. In contrast, all cats in an earli#er series in which the leg had been casted for 2 to 7 weeks with the calf muscles at resting length, showed greater stretch sensitivity. It is concluded that the spindl’e receptor adapts to long-term str’etch of the muscle with a decrease in stretch sensitivity.
INTRODUCTION After a muscle has been held near its resting length for several weeks by means of a cast, its spindles are found to show increased position sensitivity compared to afferent units in the contralateral unrestrained limb (6). This increase in ‘the discharge frequency-length relationship could arise from true adaptation of the spindle mechanism due to the lax state of the muscle, or it might be a more indirect consequenceof the rather extensive atrophy that develops in extrafusal tissue surrounding the spindle. If adaptation is the cause of the increase, then spindles in a muscle maintained under stretch should conversely show a diminution in position sensitivity. Atrophy would be present in both experimental conditions, 1 Supported by USPHS Grant NS 01143. 2 Dr. Maier is now at the Department of Anatomy, mingham, Alabama 35294. 49 Copyright All rights
0 1976 by Academic Press, Inc. of reproduction in any form reserved.
University
of Alabama,
Bir-
50
MAIER
AND
ELDRED
although somewhat less extensive in the muscle immobilized under stretch (9). The following observations were made to see if prolonged stretch of a muscle does result in reduced position sensitivity of its spindles. Afferent responses from the cat’s medial gastrocnemius held in extension for several weeks by a cast were compared terminally with spindle responses from the opposite unrestrained leg. The findings from these animals are contrasted with results from our earlier series (6) in which the muscle was held at near the resting length. METHODS Ten adults cats were used for the long-term experiments. While under barbiturate anesthesia, one hindlimb was placed in a plaster cast extending from the thigh to metatarsus, so as to hold the knee nearly fully extended and the ankle dorsiflexed about 30”. In bringing the leg to this position moderate resistance was encountered from the calf muscles. After a period of 2 to 6 weeks, the animal was again placed under deep barbiturate anesthesia, the lumbosacral spinal cord exposed, and a thorough denervation made bilaterally of lumbar, gluteal, and leg regions except for the medial gastrocenemius muscles. The cat was then placed in a hammock and the hindquarters immobilzed by clamps on the spinous processes and the pelvis. Each leg was fixed with the femur in a vertical position and the tibia at a right angle to it, care being taken to have the hindlimbs in precisely symmetrical positions. Extension of the gastrocnemius could be obtained by flexing the ankle, or by connecting the severed tendon to a traversible strain gauge by an inelastic silk thread. An oil pool was formed about the spinal cord, and ventral roots L6 to Sl cut bilaterally. In some animals the integrated sensory discharge from the gastrocnemius muscle was bipolarly recorded from the well-isolated, severed Sl dorsal roots, the amplification of the two recording channels being equalized initially while recording simultaneously from the normal dorsal root. In other animals the activity of units teased from these roots was monitored and photographed on an oscilloscope. Units were identified as originating in spindles by the response exhibited during an induced twitch, but to facilitate collection of sizeable populations of units, the conduction rate was not generally measured. Most units were presumably Ia afferents, as these larger fibers better survive the teasing procedure. On the average, 22 units were monitored per muscle, the smallest sample having nine units. Statistical significance of differences between means for the slopes of length-frequency regression curves and other values was determined by the unpaired t test, with P
