Fusimotor fiber responses in the decerebellate cat

Fusimotor fiber responses in the decerebellate cat

218 SHORT COMMUNICATIONS Fusimotor fiber responses in the decerebellate cat There is growing evidence of an important relationship between the cereb...

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218

SHORT COMMUNICATIONS

Fusimotor fiber responses in the decerebellate cat There is growing evidence of an important relationship between the cerebellum and the fusimotor regulation of the responses of muscle spindle afferents. Several studies have demonstrated that inactivation of the cerebellum by cooling or ablation depresses the responses to passive extension of spindle primary afferents within hindlimb extensor and flexor muscles 1-3,5,s. These studies also explored the spindle afferent responses to stimuli other than stretch of the muscle containing the spindle, such as passive movement of the neck, manipulation of the limbs, and twisting the pinna. In the initial studies, the spindle afferent responses to these 'external stimuli' were found to be depressed in decerebellate compared with control preparations ~,s. However, subsequent studies, in which large numbers of units were tested, failed to substantiate these findings2,3. In these experiments, the spindle afferent response occurring in advance or in the absence of extrafusal contraction was used as an index of corresponding fusimotor activity. However, the sensitivity of muscle spindles to mechanical stimuli makes it possible that a change in discharge reflects contraction of nearby extrafusal fibers rather than fusimotor excitation, even when muscle contraction cannot be detected with a myograph7. In the present study, fusimotor excitability was determined directly by recording the discharge of single gamma efferent fibers in peripheral nerve filaments. Seventeen cats were used for recording; complete cerebellar ablation was performed in 7 and the remainder was used for control observations. The extent of ablation was verified both grossly and histologically. Three to five days after the initial operation, the animals were prepared for fusimotor recording. Following anesthesia with pentobarbital, 30 mg/kg, the left gastrocnemius muscle was separated from the surrounding tissues and its severed tendon attached to a force transducer. The rack and pinion mounted transducer was clamped to the table where the animal was rigidly held. The nerves to the left hamstring muscles were sectioned. Following a laminectomy, the left ventral roots (VR) L6, L7, and $2 were sectioned and the intact VRS1 was placed on bipolar Ag-AgCI stimulating electrodes with the cathode oriented distally. Equilibrated with 95 ~o 02-5 ~ CO2 and warmed to 37°C, pools of paraffin oil covered the spinal cord and muscle. Small fascicles of the intact medial gastrocnemius nerve were sectioned at the nerve-muscle junction and separated for about 1 cm proximally. Dissected with fine scissors and forceps under a microscope, small filaments of the fascicle were laid across fine bipolar Ag-AgCI recording electrodes. The dissection was continued until single action potentials were recorded which occurred spontaneously or could be evoked by a pinna twist 6. The action potentials were shown to originate in fusimotor fibers by demonstrating that the conduction velocity (CV) was less than 50 m/sec. The CV was determined using the length of nerve measured from the cathode and the latency of the unit response to VRS1 stimulation at twice threshold intensity. The recorded CVs ranged from 14.9 to 46.0 m/sec in controls and 11.5 to 49.0 in decerebellates. A unit was not accepted unless occlusion of the electrically evoked response by spontaneously active units could be demonstrated. Occlusion and an all-or-nothing response to threshold electrical stimulation demonBrain Research, 14 (1969) 218-221

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219

TABLE I RESPONSES TO NATURAL EXTERNAL STIMULI OF MEDIAL GASTROCNEMIUS FUSIMOTOR UNITS IN LIGHTLY ANESTHETIZED CATS

The t test of each column compares values from control and decerebeUate preparations in the preceding colunm. Single asterisk indicates P < 0.05; double P < 0.01; triple P < 0.001. Abbreviations: mf, mean frequency; n, number of units. A. BASELINE(PRESTIMULUS)FREQUENCIES,IMPULSES/SEC Preparation

mf

Control 23.2 Decerebellate 10.2

n

t ind.

79 63

4.77***

B. RESPONSES TO PASSIVE NECK MOVEMENT

Preparation

Peak frequency

Frequency change

mean

t ind.

mean

79 63

25.2 18.8

2.66**

0.8 8.3

6.75***

79 63

29.4 24.4

1.79

5.0 13.6

3.95 ** *

m f preceding neck movement

n

24.4 11.3

24.4 11.3

t ind.

Neck extension

Control Decerebellate Neck flexion

Control Decerebellate

C . RESPONSES TO PASSIVE MOVEMENT OF LEFT HINDLIMB TOES

Preparation

Peak frequency

Frequency change

mean

mean

t ind.

4.71 ***

7.5 7.1

0.21

3.55***

8.2 8.5

0.14

m f preceding toe movement

n

24.4 12.7

69 60

32.2 19.6

24.4 12.7

69 60

32.6 21.2

t ind.

Toe extension

Control Decerebellate Toe flexion

Control Decerebellate

strated that each u n i t was completely isolated. P e n t o b a r b i t a l was administered intravenously in 1.0 mg doses as needed to keep the a n i m a l s lightly anesthetized at a consistent clinical level, so that a p i n n a twist caused withdrawal of the head a n d a t t e m p t e d progression movements. Recordings were made o n m o v i n g film n o sooner t h a n 30 m i n after each dose of b a r b i t u r a t e . Recorded before any stimulus was applied a n d measured d u r i n g a 1.0 sec interval, the m e a n baseline frequency was significantly ( P < 0.001) less in decerebellate Brain Research, 14 (1969) 218-221

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SHORT (7OMMUNI('ATIONS

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Fig. 1.5-day decerebellate cat. A, Recording from single fusimotor (small spike, conduction velocity 15.8 m/sec) and alpha (conduction velocity 88.7 m/sec) units in a filament of medial gastrocnemius nerve (upper trace). Middle trace shows gastrocnemius muscle tension. At the break in the lower trace the contralateral hindfoot is squeezed to evoke a crossed extensor reaction. Records B-D are parts of a continuous recording begun in A. An increase of gamma discharge (A) precedes alpha firing and muscle contraction (B). A burst of alpha discharge occurs again when the stimulus is discontinued (D). animals than controls (Table IA). In 53 of the 63 units in decerebellates the frequency range was 0-18/sec, but 10 units maintained high (20-73/sec) baseline rates. The following stimuli were applied: the neck was passively extended 60 ° from the horizontal position, immobilized until the discharge became constant, then flexed to the horizontal; the left hindlimb toes were dorsiflexed 45 °, maintained until the discharge stabilized, then flexed to the resting posture. It required a mean of 0.5 and 0.2 sec to perform each passive movement of the neck and toes, respectively. The cutaneous and proprioceptive components of these stimuli were not differentiated. The discharge rate induced by each stimulus was measured for an interval of 1.0 sec from the instant a frequency change appeared. As shown in Table IB, the units recorded from decerebellates responded to neck movement with a lower mean frequency but greater change from the prestimulus frequency than the units recorded from controls. The Brain Research, 14 (1969) 218-221

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221

meart frequencies induced by toe movement were less in decerebellates thanin controls, but the mean changes of frequency were not significantly different (Table IC). In 9 recordings from control and 6 f r o m decerebellate animals, the discharge of a single fusimotor and a single phasic alpha m o t o r unit was recorded simultaneously f r o m a single filament. In the present study, the term 'phasic unit' refers to units which are silent until some stimulus is applied. The activation sequence f r o m the following stimuli was studied: pinna twist, passive neck movements, passive movement of the left hindlimb toes, and squeezing the left artd right hindfoot. In 8 of the recordings in control and all 6 irt decerebellate animals, an increase of fusimotor discharge preceded the onset of alpha discharge and muscle contraction (Fig. 1). Van Der Meulen and McLeod 9 have observed a similar activation sequence irt decerebellate cats. It is concluded that cerebellar ablation decreases the baseline discharge rate of extensor fusimotor efferents, but does not diminish the frequency change induced by natural segmental artd suprasegmental stimuli. There is no change in the activation sequence of fusimotor and phasic alpha m o t o r fibers. The disorder of 'alpha-gamma linkage' from cerebellar lesions 4 may be expressed in terms of a depression of tonic fusimotor activity and an increase of tonic alpha motor activity, without alteration of the fusimotor-phasic alpha motor excitation pattern induced by natural external stimuli. Supported in part by U.S. Public Health Service Grants NB 05184 and PH 436454. I am indebted to Dr. Harvey C. Ebel for advice on the statistical analysis of the data.

Department of Neurology, College of Physicians and Surgeons, Columbia University, New York, N.Y. 10032 (U.S.A.)

SID GILMAN

1 GILMAN, S., The mechanism of cerebellar hypotonia: an experimental study in the monkey, Brain, in press. 2 GILMAN,S., AND McDoNALD, W. I., Cerebellar facilitation of muscle spindle activity, J. Neurophysiol., 30 (1967) 1494--1512. 3 GILMAN,S., AND MCDONALD,W. I., Relation of afferent fiber conduction velocity to reactivity of muscle spindle receptors after cerebellectomy, 2. Neurophysiol., 30 (1967) 1513-1522. 4 GRANIT,R., Receptors and Sensory Perception, Yale Univ. Press, New Haven, Conn., 1955, pp 269-273. 5 GRANIT,R., HOLMGm~N,B., ANDM~RTON,P. A., The two routes for excitation of muscle and their subservience to the cerebellum, J. PhysioL (Lond.), 130 (1955) 213-223. 6 GRANIT,R., JOB, C., AND KXADA, B. R., Activation of muscle spindles in pinna reflex, Acta physiol, scand., 27 (1952) 161-168. 7 MATTrmWS,P. B. C., Muscle spindles and their motor control, Physiol. Rev., 44 (1964) 219-288. 8 VANDeR MEULEN,J. P., ANOGILMAN,S., Recovery of muscle spindle activity in cats after cerebellar ablation, J. Neurophysiol., 28 (1965) 943-957. 9 VAN DEg MEtrLEN,J. P., AND McL~oo, J. G., unpublished observations. (Accepted March 8th, 1969) Brain Research, 14 (1969) 218-221