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Vestibular compensation without brainstem commissures in the guinea pig
Neuroscience Letters, 65 (1986) 209-213 Elsevier Scientific Publishers Ireland Ltd.
209
NSL 03825 VESTIBULAR COMPENSATION WITHOUT BRAINSTEM COMMISSURES IN THE GUINEA PIG
PAUL F. SMITH*, CYNTHIA L. DARLINGTON, IAN S. CURTHOYS Department of Psychology, University of Sydney, Sydney, N.S.W. 2006 (Australia)
(Received October 30th, 1985; Accepted December 4th, 1985)
Key words." vestibular compensation - deafferentation - vestibular commissures - neural plasticity guinea pig
The rapid recovery from the postural and ocular motor asymmetries produced by unilateral vestibular damage (vestibular compensation) has been presented as an example of plasticity in the central nervous system. A recent model (J. Neurophysiol., 51 (1984) 242-259) has identified the fibers joining the two vestibular nuclei in the brainstem (the vestibular commissures) as the site of the plastic changes. We report that in guinea pigs, compensation of postural symptoms still occurs after sectioning these commissural fibers. We suggest that a number of mechanisms may be responsible for vestibular compensation , including some which are independent of the vestibular commissures. Acute unilateral labyrinthectomy causes severe disturbances o f eye m o v e m e n t and b o d y posture. These disturbances vary with species, but c o m m o n to most species is a deviation o f the head and b o d y t o w a r d the lesioned side in the vertical plane (longitudinal twist: LT) [6, 16] (Fig. 1). In all species, the s y m p t o m s are most severe immediately after the labyrinthectomy but diminish over time in the process k n o w n as vestibular compensation [ 16]. Recently, Galiana et al. [5] have proposed that gain changes in the commissural fibers between the vestibular nuclei (the vestibular commissures) are responsible for vestibular compensation. This proposal is supported by the observation in the frog that, once compensation is achieved, sectioning the vestibular commissures results in complete and irreversible return o f the longitudinal twist observed immediately after the unilateral labyrinthectomy [!]. We report that sectioning the vestibular commissures in the guinea pig does not prevent the c o m p e n s a t i o n o f longitudinal ,twist nor lateral head deviation ( L H D ) (Fig. 1), and therefore question the proposal that the vestibular commissures are responsible for vestibular compensation in m a m m a l s [5]. U n d e r ketamine (100 m g / k g , i.m.) and R o m p u n (4 mg/kg, i.m) anesthesia, 4 guinea pigs received a right labyrinthectomy (group LC). Following this, portions o f the occipital bone were removed and the dura opened to expose the cerebellum and spinal cord at C1. With a blunt .spatula, the intact cerebellum was gently lifted and a fine iris knife inserted into the midline o f the b r a i n s t e m , sectioning the vestibular *Author for correspondence. 0304-3940/86/$ 03.50 © 1986 Elsevier Scientific Publishers Ireland Ltd.
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10 20 30 40 50 HOURS POST-LABYRINTHECTOMY Fig. 1. The course of compensation of LT (angle between vertical axis and center of head) and LHD (angle between longitudinal body axis and center of snout) for each guinea pig in group LC. Dotted area indicates + 1 S.D. for previous data where guinea pigs received a right labyrinthectomy only (mean n for each data point during the 52-h period was 5.7) [18]. c o m m i s s u r e s from a b d u c e n s nucleus to the h y p o g l o s s a l nucleus, to a d e p t h o f a p p r o x i m a t e l y 2.5 m m (Fig. 2). T h e cerebellum was then carefully r e p o s i t i o n e d , the exposed areas covered with G e l f o a m a n d the o p e n i n g in the occipital b o n e sealed with dental cement. The w o u n d was then sutured. In 3 guinea pigs, only the c o m m i s s u r e c t o m y was p e r f o r m e d ( g r o u p C). All a n i m a l s were a l l o w e d to recover in n o r m a l light a n d were m e a s u r e d for L T a n d L H D with a p r o t r a c t o r (Fig. 1) as r e p o r t e d elsewhere [18]. F o l l o w i n g recovery from anesthesia, g r o u p C exhibited m o d e r a t e a t a x i a b u t n o n e o f the s y m p t o m s o f unilateral l a b y r i n t h e c t o m y . G r o u p LC, by c o n t r a s t , exhibited the severe L T a n d L H D t o w a r d the lesioned side characteristic o f acute unilateral labyrinthectomy, as well as ataxia.
211
Fig. 2. Schematicrepresentationin the midline sagittal plane showing the extent of the commissurectomy for each guinea pig in group LC. VI, abducens nucleus; MVN, medial vestibularnucleus; DVN, descending vestibularnucleus; XII, hypoglossalnucleus.
Our previous experiments have shown that following unilateral labyrinthectomy in the guinea pig, initially severe LT and L H D diminish, until by 52 h post-labyrinthectomy, less than 15° LT and L H D remain [18]. A similar pattern was observed in group LC (Fig. 1). The decrease in the postural asymmetries coincided with a gradual return of more normal locomotor behavior. Precautions were taken to ensure that the observed improvement in these postural symptoms was not simply due to ataxia. Data were obtained only when the following criteria were met: (i) the animal maintained itself in a standing position and could walk around its box; (ii) when lifted from the ground, the postural symptoms returned and then 'recompensated' when the animal was replaced [16]. The latter observation suggested that the state of postural compensation was reliant on sensory stimulation and was not the result of the inability to exhibit the previous symptoms. Because of these measurement criteria, not all animals were measured for the full 52 h; however, in each case compensation was clearly demonstrated. The results of histology showed that each commissurectomy extended from rostral to abducens nucleus, to the caudal pole of the hypoglossal nucleus, with a maximum depth not less than 2.5 mm (Fig. 2). There is currently no anatomical evidence on the course of the vestibular commissures in the guinea pig: however, the majority of the vestibular commissures in the cat course within 2 mm of the dorsal surface of the brainstem [4, 7]. We reasoned that a cut to a depth of 2.5 mm should section the vestibular commissures in the guinea pig, and electrophysiological studies after cuts to this depth suggest this reasoning is valid: normal interaction between the two vestibular nuclei is interrupted [3, 17]. However, the possibility exists that such a cut spares some more ventral commissural fibers [2, 12], whose function is currently unknown.
212
The present data demonstrate that in the guinea pig, compensation of the postural symptoms caused by unilateral labyrinthectomy occurs in the absence of the vestibular commissures. We conclude that these fibers are not responsible for the compensation of postural symptoms in mammals. This result leads us to question the suggestion of Galiana et al. [5] that a single process underlies the recovery of the variety of postural and ocular motor disturbances produced by unilateral labyrinthectomy. These behavioral disturbances recover at different rates [9]: therefore, a number of physiological processes may be participating [8]. The results of neural studies in compensated mammals support the hypothesis that some aspects of vestibular compensation are independent of the vestibular commissures. Vestibular compensation is associated with a return of spontaneous activity to type I neurons in the deafferented medial vestibular nucleus (dMVN) [14, 15]. However, as type I neurons are inhibited by vestibular commissural input [14, 15], these commissures cannot be responsible for the renewed spontaneous activity. One reason for the discrepancy between our results in the guinea pig and those in the frog may be that the vestibular commissures in the frog are predominantly excitatory [11], and, therefore, may contribute to the renewed spontaneous activity in the dMVN. Following unilateral labyrinthectomy, the deafferented lateral vestibular nucleus (dLVN) also undergoes a deficit and recovery of function similar to the dMVN [13, 19]; however, the LVN has only weak, if any, commissural connections with the contralateral vestibular nuclei (VN) [2, 12]. Therefore, whatever recovery occurs in the dLVN may be independent of the vestibular commissures~ The vestibular commissures are probably important'for the recovery of vestibular reflexes initiated by head movement, such as the vestibulo-ocular reflex, since they transmit information about head movement from the intact labyrinth to the dMVN [14]. However, the present data demonstrate that postural symptoms compensate in the absence of the vestibular commissures; therefore, other factors, such as adaptation in the intact VN [10], or denervation supersensitivity in the deafferented VN [14], may be responsible for this aspect of vestibular compensation in mammals. We are grateful to Professor O. Pompeiano for his critical review of an earlier version of the manuscript. 1 Bienhold, H. and Flohr, H., Role of commissural connexions between vestibular nuclei in compensation following unilateral labyrinthectomy, J. Physiol. (London), 284 (1978) 178. 2 Carleton, S.C. and Carpenter, M.B., Afferent and efferent connections of the medial, inferior and lateral vestibular nuclei in the cat and monkey, Brain Res., 278 (1983) 29-51. 3 Curthoys, I.S., unpublished observations. 4 Gacek, R.R., Location of commissural neurons in the vestibular nuclei of the cat, Exp. Neurol., 59 (1978) 479-491. 5 Galiana, H.L., Flohr, H. and Melvill Jones, G., A re-evaluation of intervestibular nuclear coupling: its role in vestibular compensation, J. Neurophysiol., 51 (1984) 242-259. 6 Jensen, D.W., Reflex control of acute postural asymmetry and compensatory symmetry after a unilateral vestibular lesion, Neuroscience, 4 (1979) 1059-1073. 7 Ladpli, R. and Brodal, A., Experimental studies of commissural and reticular formation projections from the vestibular nuclei of the cat, Brain Res., 8 (1968) 65-96.
213 8 Llinas, R. and Walton, K., Vestibular compensation: a distributed property of the central nervous system. In H. Asanuma and V.J. Wilson (Eds.), Integration in the Nervous System, Igaku Shoin, Tokyo, 1979, pp. 145-166. 9 Maioli, C., Precht, W. and Ried, S., Short and long term modifications of the vestibulo-ocular response dynamics following unilateral vestibular nerve lesions in the cat, Exp. Brain Res., 50 (1983) 259-274. 10 McClure, J.A. and Lycett, P., Recovery nystagmus, J. Otolaryngol., 7:2 (1978) 141-148. 11 Ozawa, S., Precht, W. and Shimazu, H., Crossed effects on central vestibular neurons in the horizontal canal system of the frog, Exp. Brain Res., 19 (1974) 394-405. 12 Pompeiano, O., Mergner, T. and Corjava, N., Commissural, perihypoglossal and reticular afferent projections to the vestibular nuclei in the cat, Arch. Ital. Biol., 116 (1978) 130-172. 13 Pompeiano, O,, Xerri, C., Gianni, S. and Manzoni, D., Central compensation of vestibular deficits. II. Influences of roll tilt on different size lateral vestibular neurons after ipsilateral labyrinth deafferentation, J. Neurophysiol., 52 (1984) 18-38. 14 Precht, W., Shimazu, H. and Markham, C.H., A mechanism of central compensation of vestibular function following hemilabyrinthectomy, J. Neurophysiol., 29 (1966) 996-1010. 15 Ried, S., Maioli, C. and Precht, W., Vestibular nuclear neuron activity in chronically hemilabyrinthectomized cats, Acta Otolaryngol., 98 (1984) 1-13. 16 Schaefer, K.P. and Meyer, D.L., Compensation of vestibular lesions. In H.H. Kornhuber (Ed.), Handbook of Sensory Physiology, Vol. 1/2, Part 2, Vestibular System, Springer, Berlin, 1974, pp. 463-490. 17 Shimazu, H. and Precht, W., Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway, J. Neurophysiol., 29 (1966) 467-492. 18 Smith, P.F., Darlington, C.L. and Curthoys, I.S., The effect of visual deprivation on vestibular compensation in the guinea pig, Brain Res., in press. 19 Xerri, C., Gianni, S., Manzoni, D. and Pompeiano, O., Central compensation of vestibular deficits. I. Response characteristics of lateral vestibular neurons to roll tilt after ipsilateral labyrinth deafferentation, J. Neurophysiol., 50 (1983) 428-448.
209
NSL 03825 VESTIBULAR COMPENSATION WITHOUT BRAINSTEM COMMISSURES IN THE GUINEA PIG
PAUL F. SMITH*, CYNTHIA L. DARLINGTON, IAN S. CURTHOYS Department of Psychology, University of Sydney, Sydney, N.S.W. 2006 (Australia)
(Received October 30th, 1985; Accepted December 4th, 1985)
Key words." vestibular compensation - deafferentation - vestibular commissures - neural plasticity guinea pig
The rapid recovery from the postural and ocular motor asymmetries produced by unilateral vestibular damage (vestibular compensation) has been presented as an example of plasticity in the central nervous system. A recent model (J. Neurophysiol., 51 (1984) 242-259) has identified the fibers joining the two vestibular nuclei in the brainstem (the vestibular commissures) as the site of the plastic changes. We report that in guinea pigs, compensation of postural symptoms still occurs after sectioning these commissural fibers. We suggest that a number of mechanisms may be responsible for vestibular compensation , including some which are independent of the vestibular commissures. Acute unilateral labyrinthectomy causes severe disturbances o f eye m o v e m e n t and b o d y posture. These disturbances vary with species, but c o m m o n to most species is a deviation o f the head and b o d y t o w a r d the lesioned side in the vertical plane (longitudinal twist: LT) [6, 16] (Fig. 1). In all species, the s y m p t o m s are most severe immediately after the labyrinthectomy but diminish over time in the process k n o w n as vestibular compensation [ 16]. Recently, Galiana et al. [5] have proposed that gain changes in the commissural fibers between the vestibular nuclei (the vestibular commissures) are responsible for vestibular compensation. This proposal is supported by the observation in the frog that, once compensation is achieved, sectioning the vestibular commissures results in complete and irreversible return o f the longitudinal twist observed immediately after the unilateral labyrinthectomy [!]. We report that sectioning the vestibular commissures in the guinea pig does not prevent the c o m p e n s a t i o n o f longitudinal ,twist nor lateral head deviation ( L H D ) (Fig. 1), and therefore question the proposal that the vestibular commissures are responsible for vestibular compensation in m a m m a l s [5]. U n d e r ketamine (100 m g / k g , i.m.) and R o m p u n (4 mg/kg, i.m) anesthesia, 4 guinea pigs received a right labyrinthectomy (group LC). Following this, portions o f the occipital bone were removed and the dura opened to expose the cerebellum and spinal cord at C1. With a blunt .spatula, the intact cerebellum was gently lifted and a fine iris knife inserted into the midline o f the b r a i n s t e m , sectioning the vestibular *Author for correspondence. 0304-3940/86/$ 03.50 © 1986 Elsevier Scientific Publishers Ireland Ltd.
210
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123 U.I
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10 20 30 40 50 HOURS POST-LABYRINTHECTOMY Fig. 1. The course of compensation of LT (angle between vertical axis and center of head) and LHD (angle between longitudinal body axis and center of snout) for each guinea pig in group LC. Dotted area indicates + 1 S.D. for previous data where guinea pigs received a right labyrinthectomy only (mean n for each data point during the 52-h period was 5.7) [18]. c o m m i s s u r e s from a b d u c e n s nucleus to the h y p o g l o s s a l nucleus, to a d e p t h o f a p p r o x i m a t e l y 2.5 m m (Fig. 2). T h e cerebellum was then carefully r e p o s i t i o n e d , the exposed areas covered with G e l f o a m a n d the o p e n i n g in the occipital b o n e sealed with dental cement. The w o u n d was then sutured. In 3 guinea pigs, only the c o m m i s s u r e c t o m y was p e r f o r m e d ( g r o u p C). All a n i m a l s were a l l o w e d to recover in n o r m a l light a n d were m e a s u r e d for L T a n d L H D with a p r o t r a c t o r (Fig. 1) as r e p o r t e d elsewhere [18]. F o l l o w i n g recovery from anesthesia, g r o u p C exhibited m o d e r a t e a t a x i a b u t n o n e o f the s y m p t o m s o f unilateral l a b y r i n t h e c t o m y . G r o u p LC, by c o n t r a s t , exhibited the severe L T a n d L H D t o w a r d the lesioned side characteristic o f acute unilateral labyrinthectomy, as well as ataxia.
211
Fig. 2. Schematicrepresentationin the midline sagittal plane showing the extent of the commissurectomy for each guinea pig in group LC. VI, abducens nucleus; MVN, medial vestibularnucleus; DVN, descending vestibularnucleus; XII, hypoglossalnucleus.
Our previous experiments have shown that following unilateral labyrinthectomy in the guinea pig, initially severe LT and L H D diminish, until by 52 h post-labyrinthectomy, less than 15° LT and L H D remain [18]. A similar pattern was observed in group LC (Fig. 1). The decrease in the postural asymmetries coincided with a gradual return of more normal locomotor behavior. Precautions were taken to ensure that the observed improvement in these postural symptoms was not simply due to ataxia. Data were obtained only when the following criteria were met: (i) the animal maintained itself in a standing position and could walk around its box; (ii) when lifted from the ground, the postural symptoms returned and then 'recompensated' when the animal was replaced [16]. The latter observation suggested that the state of postural compensation was reliant on sensory stimulation and was not the result of the inability to exhibit the previous symptoms. Because of these measurement criteria, not all animals were measured for the full 52 h; however, in each case compensation was clearly demonstrated. The results of histology showed that each commissurectomy extended from rostral to abducens nucleus, to the caudal pole of the hypoglossal nucleus, with a maximum depth not less than 2.5 mm (Fig. 2). There is currently no anatomical evidence on the course of the vestibular commissures in the guinea pig: however, the majority of the vestibular commissures in the cat course within 2 mm of the dorsal surface of the brainstem [4, 7]. We reasoned that a cut to a depth of 2.5 mm should section the vestibular commissures in the guinea pig, and electrophysiological studies after cuts to this depth suggest this reasoning is valid: normal interaction between the two vestibular nuclei is interrupted [3, 17]. However, the possibility exists that such a cut spares some more ventral commissural fibers [2, 12], whose function is currently unknown.
212
The present data demonstrate that in the guinea pig, compensation of the postural symptoms caused by unilateral labyrinthectomy occurs in the absence of the vestibular commissures. We conclude that these fibers are not responsible for the compensation of postural symptoms in mammals. This result leads us to question the suggestion of Galiana et al. [5] that a single process underlies the recovery of the variety of postural and ocular motor disturbances produced by unilateral labyrinthectomy. These behavioral disturbances recover at different rates [9]: therefore, a number of physiological processes may be participating [8]. The results of neural studies in compensated mammals support the hypothesis that some aspects of vestibular compensation are independent of the vestibular commissures. Vestibular compensation is associated with a return of spontaneous activity to type I neurons in the deafferented medial vestibular nucleus (dMVN) [14, 15]. However, as type I neurons are inhibited by vestibular commissural input [14, 15], these commissures cannot be responsible for the renewed spontaneous activity. One reason for the discrepancy between our results in the guinea pig and those in the frog may be that the vestibular commissures in the frog are predominantly excitatory [11], and, therefore, may contribute to the renewed spontaneous activity in the dMVN. Following unilateral labyrinthectomy, the deafferented lateral vestibular nucleus (dLVN) also undergoes a deficit and recovery of function similar to the dMVN [13, 19]; however, the LVN has only weak, if any, commissural connections with the contralateral vestibular nuclei (VN) [2, 12]. Therefore, whatever recovery occurs in the dLVN may be independent of the vestibular commissures~ The vestibular commissures are probably important'for the recovery of vestibular reflexes initiated by head movement, such as the vestibulo-ocular reflex, since they transmit information about head movement from the intact labyrinth to the dMVN [14]. However, the present data demonstrate that postural symptoms compensate in the absence of the vestibular commissures; therefore, other factors, such as adaptation in the intact VN [10], or denervation supersensitivity in the deafferented VN [14], may be responsible for this aspect of vestibular compensation in mammals. We are grateful to Professor O. Pompeiano for his critical review of an earlier version of the manuscript. 1 Bienhold, H. and Flohr, H., Role of commissural connexions between vestibular nuclei in compensation following unilateral labyrinthectomy, J. Physiol. (London), 284 (1978) 178. 2 Carleton, S.C. and Carpenter, M.B., Afferent and efferent connections of the medial, inferior and lateral vestibular nuclei in the cat and monkey, Brain Res., 278 (1983) 29-51. 3 Curthoys, I.S., unpublished observations. 4 Gacek, R.R., Location of commissural neurons in the vestibular nuclei of the cat, Exp. Neurol., 59 (1978) 479-491. 5 Galiana, H.L., Flohr, H. and Melvill Jones, G., A re-evaluation of intervestibular nuclear coupling: its role in vestibular compensation, J. Neurophysiol., 51 (1984) 242-259. 6 Jensen, D.W., Reflex control of acute postural asymmetry and compensatory symmetry after a unilateral vestibular lesion, Neuroscience, 4 (1979) 1059-1073. 7 Ladpli, R. and Brodal, A., Experimental studies of commissural and reticular formation projections from the vestibular nuclei of the cat, Brain Res., 8 (1968) 65-96.
213 8 Llinas, R. and Walton, K., Vestibular compensation: a distributed property of the central nervous system. In H. Asanuma and V.J. Wilson (Eds.), Integration in the Nervous System, Igaku Shoin, Tokyo, 1979, pp. 145-166. 9 Maioli, C., Precht, W. and Ried, S., Short and long term modifications of the vestibulo-ocular response dynamics following unilateral vestibular nerve lesions in the cat, Exp. Brain Res., 50 (1983) 259-274. 10 McClure, J.A. and Lycett, P., Recovery nystagmus, J. Otolaryngol., 7:2 (1978) 141-148. 11 Ozawa, S., Precht, W. and Shimazu, H., Crossed effects on central vestibular neurons in the horizontal canal system of the frog, Exp. Brain Res., 19 (1974) 394-405. 12 Pompeiano, O., Mergner, T. and Corjava, N., Commissural, perihypoglossal and reticular afferent projections to the vestibular nuclei in the cat, Arch. Ital. Biol., 116 (1978) 130-172. 13 Pompeiano, O,, Xerri, C., Gianni, S. and Manzoni, D., Central compensation of vestibular deficits. II. Influences of roll tilt on different size lateral vestibular neurons after ipsilateral labyrinth deafferentation, J. Neurophysiol., 52 (1984) 18-38. 14 Precht, W., Shimazu, H. and Markham, C.H., A mechanism of central compensation of vestibular function following hemilabyrinthectomy, J. Neurophysiol., 29 (1966) 996-1010. 15 Ried, S., Maioli, C. and Precht, W., Vestibular nuclear neuron activity in chronically hemilabyrinthectomized cats, Acta Otolaryngol., 98 (1984) 1-13. 16 Schaefer, K.P. and Meyer, D.L., Compensation of vestibular lesions. In H.H. Kornhuber (Ed.), Handbook of Sensory Physiology, Vol. 1/2, Part 2, Vestibular System, Springer, Berlin, 1974, pp. 463-490. 17 Shimazu, H. and Precht, W., Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway, J. Neurophysiol., 29 (1966) 467-492. 18 Smith, P.F., Darlington, C.L. and Curthoys, I.S., The effect of visual deprivation on vestibular compensation in the guinea pig, Brain Res., in press. 19 Xerri, C., Gianni, S., Manzoni, D. and Pompeiano, O., Central compensation of vestibular deficits. I. Response characteristics of lateral vestibular neurons to roll tilt after ipsilateral labyrinth deafferentation, J. Neurophysiol., 50 (1983) 428-448.