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Labyrinth and neck reflex modification of the tonic vibration reflex in the decerebrate cat
Brain Research, 190 (1980) 425-433 © Elsevier/North-Holland Biomedical Press
L A B Y R I N T H A N D N E C K R E F L E X M O D I F I C A T I O N OF V I B R A T I O N R E F L E X I N T H E D E C E R E B R A T E CAT
425
THE TONIC
J. R. ROSENBERG, K. W. LINDSAY and J. J. LOGAN Institute of Physiology, University of Glasgow, Glasgow G12 8QQ ( U.K.)
(Accepted November 1st, 1979) Key words: tonic vibration reflex - - labyrinthine and neck reflexes - - decerebrate cat
SUMMARY The interaction between tonic labyrinth or neck reflexes and the tonic vibration reflex acting on the medial head of triceps in the decerebrate cat is described. Medial triceps was isotonically loaded and reflex actions were measured as changes in muscle length. Natural stimulation of the receptors giving rise to tonic labyrinth or neck reflexes can either enhance or diminish the size of a pre-existing tonic vibration reflex. It is also shown that descending activity from either the labyrinth or neck reflex systems can completely suppress the tonic vibration reflex, whereas the tonic vibration reflex was never observed to suppress an established labyrinth or neck reflex.
INTRODUCTION Rotation of the head or neck of the decerebrate cat about its long axis elicits the 'tonic labyrinth or neck reflexes'. These reflexes act together on the limb musculature to stabilize the trunk allowing the head to move freely on the body without affecting this stability 6. Some components of this postural adjustment of the limbs may involve an interaction between descending vestibular and neck reflex activity with inputs from Ia afferents. Previous studies of this interaction have reported the effects of electrical stimulation or ablation of the lateral vestibular nucleus on the size of the tonic vibration reflex4, 5. However, since these procedures do not take into account the intrinsic organization of the area stimulated or ablated, they cannot be expected to reveal the full range of interaction between activity arising from the vestibular nuclei and the tonic m o t o r neurones activated by vibration. A preparation has recently been developed in which the tonic labyrinth and neck reflexes acting on the forelimb of the decerebrate cat can be stimulated naturallyr, 12. The effects of stimulation of the labyrinth and neck receptors can then be examined
426 either independently or in combination in the same animal6,1L This preparation has now been used to extend earlier work on the interaction of activity in the vestibulospinal tract with the tonic vibration reflex4,5, and to include a description of the interaction between the neck reflexes acting on the limbs and the tonic vibration reflex. METHODS The effect of natural labyrinth and neck receptor stimulation on the tonic vibration reflex (TVR) was studied in ten cats. Intercollicular decerebrations were carried out while the cats were anaesthetized with an Ne0/02-halothane mixture. All the cats breathed spontaneously throughout the course of each experiment. The dorsal roots of C1 and the dorsal and ventral roots of C2 were cut on each side within the vertebral column under direct vision with the aid of a dissecting microscope. The head, neck and trunk were independently supported. The head was fixed in a head-holder arranged so that it could be rotated about a horizontal antero-posterior axis. The axis vertebra was clamped so that it could be rotated about an axis passing in an antero-posterior direction through the vertebral column. The trunk was suspended by a pair of knitting needles, one passing through the supraspinous ligament of the upper thoracic vertebrae, the other passing just ventral to the iliac crests of the pelvis. Rotation of the head with the axis vertebra clamped provided a natural labyrinth stimulus, since reflexes arising from the rotation of the joints above the axis vertebra had been eliminated by the bilateral section of C1 and Cz s. Conversely, when the head was fixed and the axis vertebra rotated, the intact receptors below the level of the axis vertebra were activated, thus providing neck reflexes in the absence of labyrinth reflexes. The right medial head of triceps (medial triceps) was dissected free, and a small portion of the olecrenon process containing its tendinous insertion removed. Bone pins were inserted into the humerus and fixed so that the forelimb was rigidly maintained in an almost vertical position. The muscle was connected to a compliant puller 11. The compliance of the puller was such that the muscle could change length throughout its full range with only negligible changes in the applied tension. The medial triceps was vibrated by means of a Pye-Ling V47 vibrator operating through the linkage of the compliant puller. A steady current was passed through the vibrator by an emitter-follower current amplifier. Vibration was produced by sinusoidally modulating this steady current. The vibration was transmitted to the muscle as a high frequency, sinusoidally fluctuating force. The amplitude of the resultant length fluctuations in medial triceps was monitored throughout the period of applied vibration. Amplitudes of vibration of 100/~m were found to provide length changes of approximately the same order as those observed normally during labyrinth and neck reflexes. For this reason the vibration amplitude was maintained at approximately 100 /~m when examining the interaction between labyrinth or neck reflexes and the TVR. Reflex changes in muscle length were measured with a photoelectric length transducer. The graded filter of the length transducer was suspended from the thread
427 connecting the muscle to the puller. The applied force was measured with an RCA 5734 mechano-electric transducer valve used as a diode in a bridge circuit. Head and neck positions were changed manually and monitored by linear potentiometers mounted in line with the axes of rotation. The direction of rotation was designated as 'side-down' when the vertex of the skull was rotated toward the limb being studied, and 'side-up' for rotations in the opposite sense. Length, force, and head or neck signals were amplified and displayed on a 3-channel pen recorder. The marker channel on the pen recorder was modified to allow the period of vibration to be recorded. The rectal temperature was maintained at approximately 37 °C by a thermistercontrolled radiant-heat lamp. The exposed tissues were coated with liquid paraffin to prevent drying. RESULTS The tonic vibration reflex (TVR) and its modification by descending activity was examined in the medial head of triceps under isotonic conditions. The resting muscle tension was set up in the range 20-80 g wt. In each of the 10 preparations studied the application of a low amplitude high frequency sinusoidally fluctuating force to the tendon of the medial triceps caused the muscle to reflexly shorten. Amplitudes of vibration of 100/~m at 100 Hz regularly induced reflex length changes in medial triceps of up to 2.5 mm depending on the initial muscle length at which the vibration was applied. When the vibration was maintained for periods of 20 sec the reflex response invariably persisted throughout. Shorter periods of vibration could be repeated every few seconds without diminution of the size of the response, and could be elicited regularly over periods of many hours. Under isometric recording conditions the time to reach a plateau value of tension has been shown to vary from 0.5-1 see v. In contrast, in our experiments, recording under isotonic conditions the average time to reach a plateau in the length change was 5 sec. Differences in the speed of the reaction of the tonic vibration reflex under isometric and isotonic conditions have also been observed in man3. The interaction between the TVR and the tonic labyrinth and neck reflexes were examined by first superimposing a tonic labyrinth or neck reflex on a pre-existing TVR, and secondly, by superimposing a TVR on a pre-existing tonic labyrinth or neck reflex. Examples of tonic labyrinth reflexes superimposed on pre-existing TVR are illustrated in Fig. 1A and B. Vibration was applied to the right medial head of triceps through the compliant linkage connecting the muscle to the puller. After a short delay medial triceps shortened by about 1 mm. Once the TVR became firmly established, a tonic labyrinth reflex was initiated by rotating the head 30 ° SD and fixing it in this position for about 3 sec. (Fig. 1A). The side-down head rotation resulted in the muscle shortening a further 0.5 mm. Once the head was returned to its normal position the muscle returned to the length determined by the pre-existing TVR. The head was then rotated 20 ° SU (Fig. 1B) against the background of a maintained TVR. The muscle then lengthened revealing the normal tonic labyrinth response to a side-up head
428 +2
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Fig. l. Tonic labyrinth (A, B) and neck (C, D) reflexes superimposed on a pre-existing tonic vibration reflex. Vibration amplitude 100 #m. rotation 6. On returning the head to its normal position medial triceps shortened to the length determined by the existing TVR. It is thus clear that tonic labyrinth reflexes can either enhance or diminish a pre-existing TVR. An analogous set of results was obtained when tonic neck reflexes were superimposed on a pre-existing T V R (Fig. IC and D). Tonic neck reflexes were elicited by fixing the skull and then rotating the axis vertebra either toward side-up or sidedown. When a TVR had been established and the axis vertebra rotated the resulting neck reflex was seen clearly superimposed on a pre-existing TVR. An example of this i s shown in Fig. 1C where the shortening of medial triceps produced by a side-up rotation of the neck is seen to add to the shortening produced in medial triceps by the tonic vibration reflex. The neck reflex response to a side-down rotation of the neck superimposed on a pre-existing tonic vibration reflex is illustrated in Fig. ID. In this case the normal response to side-down neck rotation was a lengthening of medial triceps which is seen to inhibit the shortening produced by the tonic vibration reflex. When the neck was rotated back to its normal position medial triceps returned to the length determined by the continued tonic vibration reflex. These results clearly demonstrate that the reflex responses to head or neck
429 rotation can be seen superimposed upon a pre-existing contraction of medial triceps produced by a tonic vibration reflex. The descending activity produced by natural stimulations of labyrinth or neck reflex systems can either enhance or diminish a preexisting shortening generated by a tonic vibration reflex. The order in which the descending activity and the tonic vibration reflex were initiated was reversed and the consequences of superimposing a tonic vibration reflex on a pre-existing tonic labyrinth or neck reflex were observed (Fig. 2A-D). An example of a tonic vibration reflex superimposed on a tonic labyrinth reflex produced by a side-down rotation of the head is given in Fig. 2A. A sustained shortening of medial triceps results from the side-down rotation of the head. A further small shortening of medial triceps occurred when the tonic vibration reflex was added to the labyrinth reflex. This additional small decrease in length is in contrast to the larger length change produced by a tonic vibration reflex superimposed on a labyrinth reflex in response to a side-up head rotation which lengthened medial triceps (Fig. 2B). A similar set of results was obtained when a tonic vibration reflex was superimposed on a pre-existing tonic neck reflex (Fig. 2C and D). The size of the tonic vibration reflex in response to the same amplitude of vibration was greater when the tonic vibration
Length(mm)
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Fig. 2. Tonic vibration reflexes superimposed on tonic labyrinth reflexes (A,B) and tonic neck reflexes (C,D). Vibration amplitude 100 pm.
430
+20 I B.~- .
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Length (rnm) -2 L_ '30
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Fig. 3. Suppression of the tonic vibration reflex by tonic neck reflexes. A: absence of a sustained response to vibration in the presence of a tonic neck reflex. B: reduced response to vibration in the presence of a tonic neck reflex.
reflex was superimposed on a neck reflex produced by a side-down neck rotation (Fig. 2D), than if the tonic vibration reflex was superimposed on a neck reflex resulting from a side-up rotation of the neck (Fig. 2C) when the muscle was at a shorter initial length. Taken together these results suggest that the amplitude of the tonic vibration reflex can
Spontaneous •
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Fig. 4. Relation between the amplitude of the tonic vibration reflex and the muscle length at which the reflex was initiated. Points on the graph were derived from a continuous 20-min record. Changes in muscle length were measured relative to the muscle length at the beginning of the record. Tonic vibration reflexes were initiated during sustained labyrinth reflexes ( 0 ) , neck reflexes (©), or in the absence of either (z~). Vibration amplitude 100 ~m.
431 be modified by the amount of descending activity generated by natural stimulation of the tonic labyrinth or neck reflexes. That the extent to which the tonic vibration reflex was reduced depended on the existing level of descending activity at the time of initiation of the TVR can be seen in Fig. 3 which illustrates pairs of responses to vibration alone followed by vibration superimposed on a pre-existing tonic neck reflex. These responses were taken from a continuous 20 min record. In Fig. 3 the tonic vibration reflexes preceding the superimposed reflexes were of the same magnitude. However, in the two cases illustrated the tonic neck reflexes were of different magnitude, and consequently the smaller tonic neck reflex (Fig. 3B) diminished the superimposed tonic vibration reflex slightly, whereas the larger tonic neck reflex (Fig. 3A) completely suppressed the response to vibration. Similarly, the tonic vibration reflex could be partially or fully suppressed by a tonic labyrinth reflex. When the supraspinal activity was adequate to suppress the maintained response to vibration (Fig. 3A) a 'twitch-like' change in length still occurred at the onset and cessation of vibration. This presumably represents a phasic component of the tonic vibration reflex which was not affected by activity from supraspinal centres. A muscle shortening produced by either a labyrinth or neck reflex was never observed to facilitate a superimposed tonic vibration reflex. This is in contrast to the observed facilitation of the vibration response by the crossed-extensor reflex or following cerebellectomy or spontaneous increases in muscle tone under isometric conditionsL The above results can be extended and brought together into a single figure which relates the amplitude of the response to vibration to the muscle length at which the vibration reflex was initiated (Fig. 4). Initial muscle length was set reflexly by labyrinth or neck reflex activity. Under isotonic conditions, lengthening and shortening reactions la which frequently follow labyrinth and neck reflexes also produced a variation in the initial muscle length at which a TVR was initiated. Fig. 4 was derived from a continuous 20-min record during which time tonic vibration reflexes were initiated either on their own or superimposed on tonic labyrinth or neck reflexes. The response to vibration clearly depended on the muscle length at the time of the applied vibration. The longer the length at which the muscle was vibrated, the larger the response to an applied vibration. When the muscle was reflexly shortened the amplitude of the vibration response became progressively reduced until a length was reached at which the tonic vibration reflex was completely inhibited, although the muscle could still be further shortened by tonic neck reflex activity. DISCUSSION It is clear that our results on the supraspinal modification of the tonic vibration reflex differ from those presented by Gillies, Burke and Lance4, 5. They point out that stimulation of the vestibular nuclei can facilitate the tonic vibration reflex, whereas end-organ activity produced by head rotation had no effect4,5. We find that head rotation giving rise to tonic labyrinth reflexes or neck rotation
432 producing tonic neck reflexes can enhance or diminish the size of the tonic vibration reflex depending on the direction of rotation. In general it appears that the size of the tonic vibration reflex is dependent upon the reflexly determined length of medial triceps at which it is initiated (Fig. 4). These differences between our results and those of Gillies et al. 4,5 are most likely a consequence of the use of different procedures to elicit supraspinal activity. Electrical stimulation or ablation of the lateral vestibular nucleus4, 5 may only reveal part of the interaction which can occur between activity in the vestibular system and the tonic vibration reflex. Our earlier work demonstrated that labyrinth and neck reflexes act in opposite directions on the forelimb when the head and neck are rotated in the same direction 6. Consequently, rotation of the head and neck together does not give rise to reflex changes of length in the forelimb muscles 6, and this could account for the observation by Gillies et al. 4 that head rotation, which in their experiments also involved neck rotation, did not affect the size of the tonic vibration reflex. In addition to the above differences between our results and those of Gillies et a14,5, an interesting asymmetry emerges in the interaction between the supraspinalmediated (tonic labyrinth and neck) reflexes and the tonic vibration reflex. In all the cases examined, descending reflex activity arising from natural stimulation of the labyrinth or neck receptors and producing a shortening of medial triceps, could be superimposed on a pre-existing shortening of medial triceps produced by the tonic vibration reflex (Fig. 1A and C). In a few instances there was some indication of a suppression of the labyrinth or neck reflex by the tonic vibration reflex. However, this effect was small, and neither of these reflexes could be completely suppressed by a tonic vibration reflex. On the other hand, the presence of either a pre-existing tonic labyrinth or neck reflex (Fig. 4) could either diminish the size of the tonic vibration reflex, or completely suppress the response to vibration. The complete absence of a response to vibration occurred at a length of medial triceps where labyrinth or neck reflex activity could produce further shortening of medial triceps. This interaction between the supraspinal activity and the [a afferent input elicited by vibration suggests that, under certain conditions, the descending supraspinal activity can selectively inhibit the Ia afferent input to the triceps motor neurone pool. This conclusion is consistent with the observation that electrical stimulation of the VIIIth nerve 2 or medial vestibular nucleus 1 gives rise to primary afferent depolarization of the Ia afferent input. This presynaptic inhibition of the Ia input would provide a mechanism for uncoupling this input to medial triceps from the descending labyrinth or neck reflex activity, but would not explain the absence of any significant suppression of the response to vibration when the vibration preceded head or neck rotation. Thus, under certain conditions, in the decerebrate cat, it appears that in the interaction between supraspinal and Ia afferent activity, the supraspinal activity can take priority in terms of reflex action. As there is evidence that muscle vibration does not alter the discharge of cells in the reticular formation 9 or the lateral vestibular nucleus 1° it would seem most likely that this interaction occurs at spinal level.
433 ACKNOWLEDGEMENTS This work was supported in part by a g r a n t from the Medical Research Council o f G r e a t Britain ( G r a n t NS02567). K. W. L. was a Wellcome Trust Research Fellow d u r i n g the period of this work.
REFERENCES 1 Barnes, C. D. and Pompeiano, O., The contribution of the medial and lateral vestibular nuclei to presynaptic and postsynaptic effects produced in the lumbar cord by vestibular volleys, Pfliigers Arch. ges. PhysioL, 317 (1970) 1-9. 2 Cook, W. A. Jr., Congiano, A. and Pompeiano, O., Vestibular control of transmission in primary afferents to the lumbar spinal cord, Arch. itaL bioL, 107 (1969) 296--320. 3 Eklund, G. and Hagbarth, K. E., Normal variability of tonic vibration reflexes in man, Exp. Neurol., 16 (1966) 80-92. 4 Gillies, J. D., Burke, D. J. and Lance, J. W., Tonic vibration reflex in the cat, J. Neurophysiol., 34 (1971) 252-262. 5 Gillies, J. D., Burke, D. J. and Lance, J. W., Supraspinal control of tonic vibration reflex, J. NeurophysioL, 34 (1971) 302-309. 6 Lindsay, K. W., Roberts, T. D. M. and Rosenberg, J. R., Asymmetric tonic labyrinth reflexes and their interaction with neck reflexes in the decerebrate cat, J. PhysioL (Lond.), 261 (1976) 583-601. 7 Matthews, P. B. C., The reflex excitation of the soleus muscle of the decerebrate cat caused by vibration applied to its tendon, J. PhysioL (Lond.), 184 (1966) 450-472. 8 McCouch, G. P., Deering, I. D. and Ling, T. H., Location of receptors for tonic neck reflexes, J. NeurophysioL, 14 (1951) 191-195. 9 Pompeiano, O. and Barnes, C. D., Response of brain stem reticular neurons to muscle vibration in the decerebrate cat, J. NeurophysioL, 34 (1971) 709-724. 10 Pompeiano, O. and Barnes, C. D., Effect of sinusoidal muscle stretch on neurons in medial and descending vestibular nuclei, J. NeurophysioL, 34 (1971) 725-734. 11 Roberts, T. D. M., Rhythmic excitation of a stretch reflex revealing (a) hysteresis and (b) a difference between the responses to pulling and stretching, Quart. J. exp. PhysioL, 48 (1963) 328-345. 12 Rosenberg, J. R. and Lindsay, K. W., Asymmetric tonic labyrinthine reflexes, Brain Research, 63 (1973) 347-350. 13 Sherrington, C. S., On plastic tonus and proprioceptive reflexes, Quart. J. exp. PhysioL, 2 (1909) 109-156.
L A B Y R I N T H A N D N E C K R E F L E X M O D I F I C A T I O N OF V I B R A T I O N R E F L E X I N T H E D E C E R E B R A T E CAT
425
THE TONIC
J. R. ROSENBERG, K. W. LINDSAY and J. J. LOGAN Institute of Physiology, University of Glasgow, Glasgow G12 8QQ ( U.K.)
(Accepted November 1st, 1979) Key words: tonic vibration reflex - - labyrinthine and neck reflexes - - decerebrate cat
SUMMARY The interaction between tonic labyrinth or neck reflexes and the tonic vibration reflex acting on the medial head of triceps in the decerebrate cat is described. Medial triceps was isotonically loaded and reflex actions were measured as changes in muscle length. Natural stimulation of the receptors giving rise to tonic labyrinth or neck reflexes can either enhance or diminish the size of a pre-existing tonic vibration reflex. It is also shown that descending activity from either the labyrinth or neck reflex systems can completely suppress the tonic vibration reflex, whereas the tonic vibration reflex was never observed to suppress an established labyrinth or neck reflex.
INTRODUCTION Rotation of the head or neck of the decerebrate cat about its long axis elicits the 'tonic labyrinth or neck reflexes'. These reflexes act together on the limb musculature to stabilize the trunk allowing the head to move freely on the body without affecting this stability 6. Some components of this postural adjustment of the limbs may involve an interaction between descending vestibular and neck reflex activity with inputs from Ia afferents. Previous studies of this interaction have reported the effects of electrical stimulation or ablation of the lateral vestibular nucleus on the size of the tonic vibration reflex4, 5. However, since these procedures do not take into account the intrinsic organization of the area stimulated or ablated, they cannot be expected to reveal the full range of interaction between activity arising from the vestibular nuclei and the tonic m o t o r neurones activated by vibration. A preparation has recently been developed in which the tonic labyrinth and neck reflexes acting on the forelimb of the decerebrate cat can be stimulated naturallyr, 12. The effects of stimulation of the labyrinth and neck receptors can then be examined
426 either independently or in combination in the same animal6,1L This preparation has now been used to extend earlier work on the interaction of activity in the vestibulospinal tract with the tonic vibration reflex4,5, and to include a description of the interaction between the neck reflexes acting on the limbs and the tonic vibration reflex. METHODS The effect of natural labyrinth and neck receptor stimulation on the tonic vibration reflex (TVR) was studied in ten cats. Intercollicular decerebrations were carried out while the cats were anaesthetized with an Ne0/02-halothane mixture. All the cats breathed spontaneously throughout the course of each experiment. The dorsal roots of C1 and the dorsal and ventral roots of C2 were cut on each side within the vertebral column under direct vision with the aid of a dissecting microscope. The head, neck and trunk were independently supported. The head was fixed in a head-holder arranged so that it could be rotated about a horizontal antero-posterior axis. The axis vertebra was clamped so that it could be rotated about an axis passing in an antero-posterior direction through the vertebral column. The trunk was suspended by a pair of knitting needles, one passing through the supraspinous ligament of the upper thoracic vertebrae, the other passing just ventral to the iliac crests of the pelvis. Rotation of the head with the axis vertebra clamped provided a natural labyrinth stimulus, since reflexes arising from the rotation of the joints above the axis vertebra had been eliminated by the bilateral section of C1 and Cz s. Conversely, when the head was fixed and the axis vertebra rotated, the intact receptors below the level of the axis vertebra were activated, thus providing neck reflexes in the absence of labyrinth reflexes. The right medial head of triceps (medial triceps) was dissected free, and a small portion of the olecrenon process containing its tendinous insertion removed. Bone pins were inserted into the humerus and fixed so that the forelimb was rigidly maintained in an almost vertical position. The muscle was connected to a compliant puller 11. The compliance of the puller was such that the muscle could change length throughout its full range with only negligible changes in the applied tension. The medial triceps was vibrated by means of a Pye-Ling V47 vibrator operating through the linkage of the compliant puller. A steady current was passed through the vibrator by an emitter-follower current amplifier. Vibration was produced by sinusoidally modulating this steady current. The vibration was transmitted to the muscle as a high frequency, sinusoidally fluctuating force. The amplitude of the resultant length fluctuations in medial triceps was monitored throughout the period of applied vibration. Amplitudes of vibration of 100/~m were found to provide length changes of approximately the same order as those observed normally during labyrinth and neck reflexes. For this reason the vibration amplitude was maintained at approximately 100 /~m when examining the interaction between labyrinth or neck reflexes and the TVR. Reflex changes in muscle length were measured with a photoelectric length transducer. The graded filter of the length transducer was suspended from the thread
427 connecting the muscle to the puller. The applied force was measured with an RCA 5734 mechano-electric transducer valve used as a diode in a bridge circuit. Head and neck positions were changed manually and monitored by linear potentiometers mounted in line with the axes of rotation. The direction of rotation was designated as 'side-down' when the vertex of the skull was rotated toward the limb being studied, and 'side-up' for rotations in the opposite sense. Length, force, and head or neck signals were amplified and displayed on a 3-channel pen recorder. The marker channel on the pen recorder was modified to allow the period of vibration to be recorded. The rectal temperature was maintained at approximately 37 °C by a thermistercontrolled radiant-heat lamp. The exposed tissues were coated with liquid paraffin to prevent drying. RESULTS The tonic vibration reflex (TVR) and its modification by descending activity was examined in the medial head of triceps under isotonic conditions. The resting muscle tension was set up in the range 20-80 g wt. In each of the 10 preparations studied the application of a low amplitude high frequency sinusoidally fluctuating force to the tendon of the medial triceps caused the muscle to reflexly shorten. Amplitudes of vibration of 100/~m at 100 Hz regularly induced reflex length changes in medial triceps of up to 2.5 mm depending on the initial muscle length at which the vibration was applied. When the vibration was maintained for periods of 20 sec the reflex response invariably persisted throughout. Shorter periods of vibration could be repeated every few seconds without diminution of the size of the response, and could be elicited regularly over periods of many hours. Under isometric recording conditions the time to reach a plateau value of tension has been shown to vary from 0.5-1 see v. In contrast, in our experiments, recording under isotonic conditions the average time to reach a plateau in the length change was 5 sec. Differences in the speed of the reaction of the tonic vibration reflex under isometric and isotonic conditions have also been observed in man3. The interaction between the TVR and the tonic labyrinth and neck reflexes were examined by first superimposing a tonic labyrinth or neck reflex on a pre-existing TVR, and secondly, by superimposing a TVR on a pre-existing tonic labyrinth or neck reflex. Examples of tonic labyrinth reflexes superimposed on pre-existing TVR are illustrated in Fig. 1A and B. Vibration was applied to the right medial head of triceps through the compliant linkage connecting the muscle to the puller. After a short delay medial triceps shortened by about 1 mm. Once the TVR became firmly established, a tonic labyrinth reflex was initiated by rotating the head 30 ° SD and fixing it in this position for about 3 sec. (Fig. 1A). The side-down head rotation resulted in the muscle shortening a further 0.5 mm. Once the head was returned to its normal position the muscle returned to the length determined by the pre-existing TVR. The head was then rotated 20 ° SU (Fig. 1B) against the background of a maintained TVR. The muscle then lengthened revealing the normal tonic labyrinth response to a side-up head
428 +2
A
La~leh
(,~)
_5 L..
Head
Petition
(deg)
+3~iSld e up
+3~01 SMe up ' -30 L. Side down
~
/ -30 LSIde down
Vibration I 0
t
1 10
I
I 20
m
I 30
!
I 40
I 0
,
! 10
t
i 20
I 30
Time (see)
Time (sec)
~n~h (ram)
-3
Neck
- 3 L_
+30
Side up
-3
Side down
~'
Position
(do0)
-30 ~- Side down Vlbmtlon I Time (see)
I
I
I Time
(see)
Fig. l. Tonic labyrinth (A, B) and neck (C, D) reflexes superimposed on a pre-existing tonic vibration reflex. Vibration amplitude 100 #m. rotation 6. On returning the head to its normal position medial triceps shortened to the length determined by the existing TVR. It is thus clear that tonic labyrinth reflexes can either enhance or diminish a pre-existing TVR. An analogous set of results was obtained when tonic neck reflexes were superimposed on a pre-existing T V R (Fig. IC and D). Tonic neck reflexes were elicited by fixing the skull and then rotating the axis vertebra either toward side-up or sidedown. When a TVR had been established and the axis vertebra rotated the resulting neck reflex was seen clearly superimposed on a pre-existing TVR. An example of this i s shown in Fig. 1C where the shortening of medial triceps produced by a side-up rotation of the neck is seen to add to the shortening produced in medial triceps by the tonic vibration reflex. The neck reflex response to a side-down rotation of the neck superimposed on a pre-existing tonic vibration reflex is illustrated in Fig. ID. In this case the normal response to side-down neck rotation was a lengthening of medial triceps which is seen to inhibit the shortening produced by the tonic vibration reflex. When the neck was rotated back to its normal position medial triceps returned to the length determined by the continued tonic vibration reflex. These results clearly demonstrate that the reflex responses to head or neck
429 rotation can be seen superimposed upon a pre-existing contraction of medial triceps produced by a tonic vibration reflex. The descending activity produced by natural stimulations of labyrinth or neck reflex systems can either enhance or diminish a preexisting shortening generated by a tonic vibration reflex. The order in which the descending activity and the tonic vibration reflex were initiated was reversed and the consequences of superimposing a tonic vibration reflex on a pre-existing tonic labyrinth or neck reflex were observed (Fig. 2A-D). An example of a tonic vibration reflex superimposed on a tonic labyrinth reflex produced by a side-down rotation of the head is given in Fig. 2A. A sustained shortening of medial triceps results from the side-down rotation of the head. A further small shortening of medial triceps occurred when the tonic vibration reflex was added to the labyrinth reflex. This additional small decrease in length is in contrast to the larger length change produced by a tonic vibration reflex superimposed on a labyrinth reflex in response to a side-up head rotation which lengthened medial triceps (Fig. 2B). A similar set of results was obtained when a tonic vibration reflex was superimposed on a pre-existing tonic neck reflex (Fig. 2C and D). The size of the tonic vibration reflex in response to the same amplitude of vibration was greater when the tonic vibration
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Fig. 2. Tonic vibration reflexes superimposed on tonic labyrinth reflexes (A,B) and tonic neck reflexes (C,D). Vibration amplitude 100 pm.
430
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Fig. 3. Suppression of the tonic vibration reflex by tonic neck reflexes. A: absence of a sustained response to vibration in the presence of a tonic neck reflex. B: reduced response to vibration in the presence of a tonic neck reflex.
reflex was superimposed on a neck reflex produced by a side-down neck rotation (Fig. 2D), than if the tonic vibration reflex was superimposed on a neck reflex resulting from a side-up rotation of the neck (Fig. 2C) when the muscle was at a shorter initial length. Taken together these results suggest that the amplitude of the tonic vibration reflex can
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Fig. 4. Relation between the amplitude of the tonic vibration reflex and the muscle length at which the reflex was initiated. Points on the graph were derived from a continuous 20-min record. Changes in muscle length were measured relative to the muscle length at the beginning of the record. Tonic vibration reflexes were initiated during sustained labyrinth reflexes ( 0 ) , neck reflexes (©), or in the absence of either (z~). Vibration amplitude 100 ~m.
431 be modified by the amount of descending activity generated by natural stimulation of the tonic labyrinth or neck reflexes. That the extent to which the tonic vibration reflex was reduced depended on the existing level of descending activity at the time of initiation of the TVR can be seen in Fig. 3 which illustrates pairs of responses to vibration alone followed by vibration superimposed on a pre-existing tonic neck reflex. These responses were taken from a continuous 20 min record. In Fig. 3 the tonic vibration reflexes preceding the superimposed reflexes were of the same magnitude. However, in the two cases illustrated the tonic neck reflexes were of different magnitude, and consequently the smaller tonic neck reflex (Fig. 3B) diminished the superimposed tonic vibration reflex slightly, whereas the larger tonic neck reflex (Fig. 3A) completely suppressed the response to vibration. Similarly, the tonic vibration reflex could be partially or fully suppressed by a tonic labyrinth reflex. When the supraspinal activity was adequate to suppress the maintained response to vibration (Fig. 3A) a 'twitch-like' change in length still occurred at the onset and cessation of vibration. This presumably represents a phasic component of the tonic vibration reflex which was not affected by activity from supraspinal centres. A muscle shortening produced by either a labyrinth or neck reflex was never observed to facilitate a superimposed tonic vibration reflex. This is in contrast to the observed facilitation of the vibration response by the crossed-extensor reflex or following cerebellectomy or spontaneous increases in muscle tone under isometric conditionsL The above results can be extended and brought together into a single figure which relates the amplitude of the response to vibration to the muscle length at which the vibration reflex was initiated (Fig. 4). Initial muscle length was set reflexly by labyrinth or neck reflex activity. Under isotonic conditions, lengthening and shortening reactions la which frequently follow labyrinth and neck reflexes also produced a variation in the initial muscle length at which a TVR was initiated. Fig. 4 was derived from a continuous 20-min record during which time tonic vibration reflexes were initiated either on their own or superimposed on tonic labyrinth or neck reflexes. The response to vibration clearly depended on the muscle length at the time of the applied vibration. The longer the length at which the muscle was vibrated, the larger the response to an applied vibration. When the muscle was reflexly shortened the amplitude of the vibration response became progressively reduced until a length was reached at which the tonic vibration reflex was completely inhibited, although the muscle could still be further shortened by tonic neck reflex activity. DISCUSSION It is clear that our results on the supraspinal modification of the tonic vibration reflex differ from those presented by Gillies, Burke and Lance4, 5. They point out that stimulation of the vestibular nuclei can facilitate the tonic vibration reflex, whereas end-organ activity produced by head rotation had no effect4,5. We find that head rotation giving rise to tonic labyrinth reflexes or neck rotation
432 producing tonic neck reflexes can enhance or diminish the size of the tonic vibration reflex depending on the direction of rotation. In general it appears that the size of the tonic vibration reflex is dependent upon the reflexly determined length of medial triceps at which it is initiated (Fig. 4). These differences between our results and those of Gillies et al. 4,5 are most likely a consequence of the use of different procedures to elicit supraspinal activity. Electrical stimulation or ablation of the lateral vestibular nucleus4, 5 may only reveal part of the interaction which can occur between activity in the vestibular system and the tonic vibration reflex. Our earlier work demonstrated that labyrinth and neck reflexes act in opposite directions on the forelimb when the head and neck are rotated in the same direction 6. Consequently, rotation of the head and neck together does not give rise to reflex changes of length in the forelimb muscles 6, and this could account for the observation by Gillies et al. 4 that head rotation, which in their experiments also involved neck rotation, did not affect the size of the tonic vibration reflex. In addition to the above differences between our results and those of Gillies et a14,5, an interesting asymmetry emerges in the interaction between the supraspinalmediated (tonic labyrinth and neck) reflexes and the tonic vibration reflex. In all the cases examined, descending reflex activity arising from natural stimulation of the labyrinth or neck receptors and producing a shortening of medial triceps, could be superimposed on a pre-existing shortening of medial triceps produced by the tonic vibration reflex (Fig. 1A and C). In a few instances there was some indication of a suppression of the labyrinth or neck reflex by the tonic vibration reflex. However, this effect was small, and neither of these reflexes could be completely suppressed by a tonic vibration reflex. On the other hand, the presence of either a pre-existing tonic labyrinth or neck reflex (Fig. 4) could either diminish the size of the tonic vibration reflex, or completely suppress the response to vibration. The complete absence of a response to vibration occurred at a length of medial triceps where labyrinth or neck reflex activity could produce further shortening of medial triceps. This interaction between the supraspinal activity and the [a afferent input elicited by vibration suggests that, under certain conditions, the descending supraspinal activity can selectively inhibit the Ia afferent input to the triceps motor neurone pool. This conclusion is consistent with the observation that electrical stimulation of the VIIIth nerve 2 or medial vestibular nucleus 1 gives rise to primary afferent depolarization of the Ia afferent input. This presynaptic inhibition of the Ia input would provide a mechanism for uncoupling this input to medial triceps from the descending labyrinth or neck reflex activity, but would not explain the absence of any significant suppression of the response to vibration when the vibration preceded head or neck rotation. Thus, under certain conditions, in the decerebrate cat, it appears that in the interaction between supraspinal and Ia afferent activity, the supraspinal activity can take priority in terms of reflex action. As there is evidence that muscle vibration does not alter the discharge of cells in the reticular formation 9 or the lateral vestibular nucleus 1° it would seem most likely that this interaction occurs at spinal level.
433 ACKNOWLEDGEMENTS This work was supported in part by a g r a n t from the Medical Research Council o f G r e a t Britain ( G r a n t NS02567). K. W. L. was a Wellcome Trust Research Fellow d u r i n g the period of this work.
REFERENCES 1 Barnes, C. D. and Pompeiano, O., The contribution of the medial and lateral vestibular nuclei to presynaptic and postsynaptic effects produced in the lumbar cord by vestibular volleys, Pfliigers Arch. ges. PhysioL, 317 (1970) 1-9. 2 Cook, W. A. Jr., Congiano, A. and Pompeiano, O., Vestibular control of transmission in primary afferents to the lumbar spinal cord, Arch. itaL bioL, 107 (1969) 296--320. 3 Eklund, G. and Hagbarth, K. E., Normal variability of tonic vibration reflexes in man, Exp. Neurol., 16 (1966) 80-92. 4 Gillies, J. D., Burke, D. J. and Lance, J. W., Tonic vibration reflex in the cat, J. Neurophysiol., 34 (1971) 252-262. 5 Gillies, J. D., Burke, D. J. and Lance, J. W., Supraspinal control of tonic vibration reflex, J. NeurophysioL, 34 (1971) 302-309. 6 Lindsay, K. W., Roberts, T. D. M. and Rosenberg, J. R., Asymmetric tonic labyrinth reflexes and their interaction with neck reflexes in the decerebrate cat, J. PhysioL (Lond.), 261 (1976) 583-601. 7 Matthews, P. B. C., The reflex excitation of the soleus muscle of the decerebrate cat caused by vibration applied to its tendon, J. PhysioL (Lond.), 184 (1966) 450-472. 8 McCouch, G. P., Deering, I. D. and Ling, T. H., Location of receptors for tonic neck reflexes, J. NeurophysioL, 14 (1951) 191-195. 9 Pompeiano, O. and Barnes, C. D., Response of brain stem reticular neurons to muscle vibration in the decerebrate cat, J. NeurophysioL, 34 (1971) 709-724. 10 Pompeiano, O. and Barnes, C. D., Effect of sinusoidal muscle stretch on neurons in medial and descending vestibular nuclei, J. NeurophysioL, 34 (1971) 725-734. 11 Roberts, T. D. M., Rhythmic excitation of a stretch reflex revealing (a) hysteresis and (b) a difference between the responses to pulling and stretching, Quart. J. exp. PhysioL, 48 (1963) 328-345. 12 Rosenberg, J. R. and Lindsay, K. W., Asymmetric tonic labyrinthine reflexes, Brain Research, 63 (1973) 347-350. 13 Sherrington, C. S., On plastic tonus and proprioceptive reflexes, Quart. J. exp. PhysioL, 2 (1909) 109-156.