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Primary trigeminal afferents to the vestibular nuclei in the rat: existence of a collateral projection to the vestibulo-cerebellum
Neuroscience Letters 264 (1999) 133–136
Primary trigeminal afferents to the vestibular nuclei in the rat: existence of a collateral projection to the vestibulo-cerebellum Gabrielle Pinganaud a ,*, Florence Bourcier b, Catherine Buisseret-Delmas a, Pierre Buisseret b a
Laboratoire de Neuroanatomie Fonctionnelle des Syste`mes Sensorimoteurs, JE 2159, UP7, 2 Place Jussieu, case 7077, 75251 Paris Cedex 05, France b Laboratoire d’Anatomie Compare´e, Muse´um National d’Histoire Naturelle, 55 rue Buffon, 75005 Paris, France Received 20 January 1999; received in revised form 16 February 1999; accepted 18 February 1999
Abstract Projections from the mesencephalic trigeminal nucleus to the vestibular nuclei were analyzed using retrograde and anterograde tracing methods. The results show that neurons in the caudal part of the trigeminal mesencephalic nucleus project mainly to the medial, inferior and lateral vestibular nuclei and moderately to the peripheral part of the superior vestibular nucleus. Using the double-labeling technique we demonstrate that individual neurons of the mesencephalic nucleus send collaterals to the vestibular nuclei and the vestibulo-cerebellum. These results suggest that these anatomical connections are involved in mechanisms of eye-head coordination. 1999 Elsevier Science Ireland Ltd. All rights reserved.
Keywords: Vestibular nuclei; Mesencephalic trigeminal nucleus; Cerebellum; Neuronal tracers; Double labeling
Eye movements are intimately related to head and neck movements. The vestibulo-ocular reflex (VOR) produces compensatory eye movements in response to head displacements. During gaze shifts, eye and head co-operate. Vestibular nuclei (VN) are premotor nuclei of eye and head motor control. They receive inputs from extraocular muscles (EOM) and neck muscles. The medial vestibular nucleus (MVN) receives a direct projection from EOM sensory neurons located in the caudal part of the mesencephalic nucleus of the trigeminal nerve (5me) [7]. The lateral vestibular nucleus (LVN) neurons, as well as those of the inferior vestibular nucleus (IVN), receive sensory and proprioceptive projections from the cervical spinal cord [18]. Neurons in the lateral part of the MVN project to both abducens and neck motoneurons [17]. The vestibular neurons responsible for the horizontal VOR are in the MVN and in the ventral part of the LVN, those responsible for the vertical VOR are in the superior vestibular nucleus (SVN) [9]. The aim of the present experiments was to determine
* Corresponding author. Tel.: +33-1-4427-3126; fax: +33-1-44275653; e-mail: [email protected]
0304-3940/99/$ - see front matter PII: S03 04-3940(99)001 79-2
whether the IVN, the LVN and/or the SVN receive direct afferent signals from the cells located in the 5me. These 5me neurons also project directly to the cerebellum [5], which is involved in the control and coordination of eyehead movements. Therefore, the second aim of the experiments was to determine if the 5me outputs to the VN and to the cerebellum correspond to separate or collateral projections. Experiments consisted of local microinjections of retrogradely or anterogradely transported neuronal tracers into the VN, the cerebellum or the 5me. In ten adult rats anaesthetized with sodium pentobarbital (50 mg/kg, i.p.) injections of diverse retrograde transport tracers were made in the VN (Fig. 1): biotinylated dextran amine (BDA), complex of wheat germ agglutinin-apo-horseradish peroxidase coupled to colloidal gold (Gold-HRP) or fluorescent ‘fluorored’ (FR). Two animals (Fig. 1: cases V2, V7) also received an additional injection of horseradish peroxidase (HRP) or fluorescent ‘fluoro-green’ (FG) in the ipsilateral cerebellar cortex. In these experiments, retrogradely singly labeled or doubly labeled cells were searched for in the 5me. In one rat an anterograde transport tracer, biocytin, had been injected into the 5me [5]. Examination of this material was made and
1999 Elsevier Science Ireland Ltd. All rights reserved.
134
G. Pinganaud et al. / Neuroscience Letters 264 (1999) 133–136
anterogradely labeled terminals were searched for in the VN. A 10% solution of BDA (10 000 MW, Molecular Probes) in phosphate buffer (PB, 0.1 M, pH 7.4) was iontophoretically injected (7 mA; 7 s on; 7 s off during 20 min). Following 6–10 days of survival, the animals were perfused with 500 ml of fixative (1% glutaraldehyde – 1% formaldehyde in PB). Frozen sections (50 mm) were cut in the transverse plane. The sections were reacted in a 1% solution of avidinbiotin complex (ABC, Vector Laboratories) in PB and then in diaminobenzidine. All sections were counterstained with neutral red. A 5% solution of biocytin in 0.05 M Tris–buffer (pH 8.0) was injected by pressure in the 5me. After 48 h the rat was perfused (4% paraformaldehyde and 0.1% glutaraldehyde in PB). The sections were treated as for BDA injections. The HRP (10% in PB, 0.1 M, pH 7.4) and the gold-HRP were pressure injected (0.5–1 ml) through micropipettes with tip diameters of 40–50 mm. After 7 days survival time, frozen 50 mm thick sections were cut in the transverse plane. The sections were (i) treated for the HRP histochemical reaction or (ii) processed with a silver intensification method in a darkroom following the protocol described by Basbaum and Me´ne´trey [4] to reveal the protein gold complex. The sections were counterstained with neutral red. Injections of FR and FG (Tombow Pencil, Tokyo, Japan). The fluorescent tracers were administered by pressure in the VN or in the cerebellum (0.05–0.1 ml in several points). Following 13 days survival time, 50 mm thick frozen sections were cut in the transverse plane and treated according to Dong et al. [11]. In order to precisely determine the injection site, each third section was counterstained with neutral red. The sections were examined under illumination between 450 and 490 nm for the FG and between 515 and 560 nm for the FR. Injections in the vestibular complex were obtained without any diffusion to adjacent structures. Three injections (Fig. 1: cases V1, V2, V3) were localized within the MVN and three within the IVN (Fig. 1: cases V6, V7, V8). Two injections (Fig. 1: cases V4, V5) affected both the MVN and the IVN. Two injections were made in the LVN (Fig. 1: cases V9, V10): one (case V9) was limited to the ventral LVN, the other (case V10) to the dorsal LVN with a light diffusion of the tracer to the dorsally adjacent SVN. In each of these experiments, retrogradely labeled neurons were found in the 5me (Fig. 1). The present data demonstrate the existence of a projection from the 5me to the MVN, the IVN (Fig. 2A) and the LVN. As the SVN has not been selectively injected in any of our cases, projection from the 5me to the SVN cannot be excluded from these experiments. Following injection of biocytin within the 5me (Fig. 3A) few anterogradely fibers and terminals were labeled in the MVN (Fig. 3B), the IVN, and the ventral and dorsal LVN. In addition, few fibers exhibited small terminal boutons in the peripheral part of the SVN (Fig. 3C). Therefore, these
retrograde and anterograde tracing studies confirm the previously shown projection of 5me neurons onto the MVN [7] and demonstrate additional direct projections, which have not been previously described, from the 5me to the IVN, the LVN and the peripheral SVN. In two animals the technique of double labeling using fluorescent tracers, FR and FG (case V2) or gold-HRP and HRP (case V7), was used. In case V2 the FR injection was centered in the MVN and in case V7 the gold-HRP injection concerned only the IVN. The large cerebellar cortical injections of FG or HRP were performed in the vestibulo-cerebellum including the thin sagittal ‘zone X/CX’ [19] which receives specific projection from the 5me [5]. Involvement of the X/CX zone was verified by the retrograde labeling of inferior olivary neurons in the dorsomedial cell column, which is the specific origin of the climbing fibers reaching the X/CX zone. Singly retrogradely labeled gold-HRP (Fig. 2A), HRP, FG (Fig. 4A) or FR neurons as well as doubly gold-HRP/ HRP (Fig. 2B) or FR/FG (Fig. 4B,C) labeled neurons were observed in the 5me. In spite of the small numbers of doubly labeled neurons observed (Fig. 1), the results provide evidence that some neurons in the caudal part of the 5me project by axon collaterals to the MVN and the cerebellum, others to the IVN and the cerebellum. Whether neurons of the 5me may also project collaterally to the cerebellum and SVN or LVN requires further investigations.
Fig. 1. On the left, injection sites in the vestibular nuclei (V1–V10). On the right are indicated for each experiment (case V1–V10): column two, the tracer injected, column three, the location of injection sites in the vestibular nuclei and column four, the number of labeled neurons in the 5me following the vestibular (VN) and the cerebellar (cereb) injections. In the two cases V2 and V7, which received additional injections of FG or HRP in the cerebellum, the number of doubly labeled neurons is indicated followed by a star. IVN, inferior vestibular nuclei; LVN, lateral vestibular nuclei; MVN, medial vestibular nuclei; SVN, superior vestibular nuclei.
G. Pinganaud et al. / Neuroscience Letters 264 (1999) 133–136
Fig. 2. Injection of gold-HRP in the IVN and HRP in the cerebellum (case V7). (A) Three single retrogradely labeled gold-HRP neurons in the 5me. (B) Two doubly retrogradely gold-HRP/HRP neurons in the 5me. Scale bar, 10 mm.
In conclusion, this study demonstrates projections from the 5me mainly to the MVN, IVN and LVN and the existence of collateral projections from the 5me to the vestibular nuclei and the zone X/CX of the cerebellum. These pathways are likely to contribute to the control of gaze orientation as well as postural mechanisms [6]. The MVN and ventral LVN are a major source of the vestibulo-abducens pathways [13–15]. Neurons in the ventral LVN terminate upon medial rectus motoneurons [3,8]. Therefore the majority of these vestibular neurons are involved in the control of
135
Fig. 4. Injection of fluoro red (FR) in the MVN and fluoro green (FG) in the cerebellum (case V2). Labeled FG (A,B) and FR (C) neurons in the 5me. A doubly labeled neuron shows FG labeling (arrow head in B) and FR labeling (arrow head in C). Scale bar, 10 mm.
the horizontal eye movements, while only few contribute to vertical eye movements [16]. Furthermore, the LVN as well as the IVN have connections with the cervical spinal cord [8,18]. It appears that sensory inputs from the face, may influence oculomotor as well as head postural control through their projections upon the premotor regions of MVN, IVN or LVN. Afferent signals from EOM influence eye and neck muscle activities [2,10,12]. Whether the 5me afferents described here derive from EOM remains to be determined. However, the ganglionic neurons of the EOM sensory receptors are located in the caudal part of the 5me [1], and it has been demonstrated that some of these neurons project to the MVN [7]. We show here that, neurons projecting to the vestibular nuclei are exclusively localized in the caudal part of the 5me. Accordingly, the present data demonstrates a pathway through which proprioceptive information from the EOM may act upon the coordination of the associated eye and head movements for gaze stabilization. We are grateful to Dr. S. Wiener for helpful comments on an earlier version of the text. We thank M. Diagne for technical assistance and B. Jay for photographic assistance. This work was supported by INSERM, grant Nos. 4M102E and 4M103E.
Fig. 3. Injection in the 5me. (A) Injection site. Anterogradely labeled terminals in the MVN (B) and the SVN (C). Scale bar, 35 mm in (A), 20 mm in (B,C).
[1] Alvarado-Mallart, M.R., Batini, C., Buisseret-Delmas, C. and Corvisier, J., Trigeminal representation of the masticatory and extraocular proprioceptors as revealed by horseradish peroxidase retrograde transport, Exp. Brain Res., 23 (1975) 167– 179. [2] Ashton, J.A., Milleret, C. and Donaldson, I.M.L., Effects of affer-
136
[3]
[4]
[5]
[6]
[7]
[8]
[9] [10]
[11]
G. Pinganaud et al. / Neuroscience Letters 264 (1999) 133–136 ent signals from the extraocular muscles upon units in the cerebellum, vestibular nuclear complex and oculomotor nucleus of the trout, Neuroscience, 31 (1989) 529–541. Baker, J.A. and Highstein, S.M., Vestibular projections to medial rectus subdivision of oculomotor nucleus, J. Neurophysiol., 41 (1978) 1629–1646. Basbaum, A.I. and Menetrey, D., Wheat germ agglutininapoHRP gold: a new retrograde tracer for light and electronmicroscopic single and double-labeled studies, J. Comp. Neurol., 261 (1987) 306–318. Billig, I., Yatim, N. and Compoint, C., Cerebellar afferences from the mesencephalic trigeminal nucleus in the rat, NeuroReport, 6 (1995) 2293–2296. Buisseret-Delmas, C., Angaut, P., Compoint, C., Diagne, M. and Buisseret, P., Brainstem efferents from the interface between the nucleus medialis and the nucleus interpositus in the rat, J. Comp. Neurol., 402 (1998) 264–265. Buisseret-Delmas, C., Epelbaum, M. and Buisseret, P., The vestibular nuclei of the cat receive a primary afferent projection from receptors in extraocular muscles, Exp. Brain Res., 81 (1890) 654–658. Carleton, S.C. and Carpenter, M.B., Afferent and efferent connections of the medial inferior and lateral vestibular nuclei in the cat and the monkey, Brain Res., 278 (1983) 29–51. Carpenter, R.H.S., Movements of the Eyes, Pion, London, 1988. Donaldson, I.M.L. and Knox, P.C., Afferents signals from pigeon extraocular muscles modify the vestibular responses of units in the abducens nucleus, Proc. R. Soc. Lond., 244 (1991) 233–239. Dong, K., Qu, T., Ahmed, F.A.K.M., Zhang, L., Yamada, K.,
[12]
[13]
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[17]
[18]
[19]
Guison, N.G., Miller, M. and Yamadori, T., Fluoro-green and fluoro-red: two new fluorescent retrograde tracers with a number of unique properties, Brain Res., 736 (1996) 61–67. Hayman, M.R., Knox, P.C., Dutia, M.B. and Donaldson, I.M.L., Effects of extraocular muscle afferent signals on the electromyogram of pigeon neck muscles during the vestibulo-collic reflex, J. Physiol. (Lond.), 459 (1993) 458. Hoddevik, G.H., Dietrichs, E. and Walberg, F., Afferent connections to the abducent nucleus in the cat, Arch. Ital. Biol., 129 (1991) 63–72. Langer, T., Kaneko, C.R.S., Scudder, C.A. and Fuchs, A.F., Afferents to the abducens nucleus in the monkey and cat, J. Comp. Neurol., 245 (1986) 379–400. Maciewicz, R.J., Eagen, K., Kaneko, C.R.S. and Highstein, S.M., Medullar and medullary brain stem afferents to the abducens nucleus in the cat, Brain Res., 123 (1977) 229–240. Mc Crea, R.A., Strassman, A. and Highstein, S.M., Anatomical and physiological characteristics of vestibular neurons mediating the vertical vestibulo-ocular reflexes of the squirrel monkey, J. Comp. Neurol., 264 (1987) 571–594. Robinson, F.R., Phillips, J.O. and Fuchs, A.F., Coordination of gaze shifts in primates: brainstem inputs to neck and extraocular motoneuron pools, J. Comp. Neurol., 346 (1994) 43–62. Sato, H., Ohkawa, T., Uchino, Y. and Wilson, V.J., Excitatory connections between neurons of the central cervical nucleus and vestibular neurons in the cat, Exp. Brain Res., 115 (1997) 381–386. Yatim, N., Compoint, C., Buisseret, P., Angaut, P. and Buisseret-Delmas, C., On the caudal extension of the X zone in the cerebellar cortex of the rat, Neurosci. Res., 23 (1995) 223– 227.
Primary trigeminal afferents to the vestibular nuclei in the rat: existence of a collateral projection to the vestibulo-cerebellum Gabrielle Pinganaud a ,*, Florence Bourcier b, Catherine Buisseret-Delmas a, Pierre Buisseret b a
Laboratoire de Neuroanatomie Fonctionnelle des Syste`mes Sensorimoteurs, JE 2159, UP7, 2 Place Jussieu, case 7077, 75251 Paris Cedex 05, France b Laboratoire d’Anatomie Compare´e, Muse´um National d’Histoire Naturelle, 55 rue Buffon, 75005 Paris, France Received 20 January 1999; received in revised form 16 February 1999; accepted 18 February 1999
Abstract Projections from the mesencephalic trigeminal nucleus to the vestibular nuclei were analyzed using retrograde and anterograde tracing methods. The results show that neurons in the caudal part of the trigeminal mesencephalic nucleus project mainly to the medial, inferior and lateral vestibular nuclei and moderately to the peripheral part of the superior vestibular nucleus. Using the double-labeling technique we demonstrate that individual neurons of the mesencephalic nucleus send collaterals to the vestibular nuclei and the vestibulo-cerebellum. These results suggest that these anatomical connections are involved in mechanisms of eye-head coordination. 1999 Elsevier Science Ireland Ltd. All rights reserved.
Keywords: Vestibular nuclei; Mesencephalic trigeminal nucleus; Cerebellum; Neuronal tracers; Double labeling
Eye movements are intimately related to head and neck movements. The vestibulo-ocular reflex (VOR) produces compensatory eye movements in response to head displacements. During gaze shifts, eye and head co-operate. Vestibular nuclei (VN) are premotor nuclei of eye and head motor control. They receive inputs from extraocular muscles (EOM) and neck muscles. The medial vestibular nucleus (MVN) receives a direct projection from EOM sensory neurons located in the caudal part of the mesencephalic nucleus of the trigeminal nerve (5me) [7]. The lateral vestibular nucleus (LVN) neurons, as well as those of the inferior vestibular nucleus (IVN), receive sensory and proprioceptive projections from the cervical spinal cord [18]. Neurons in the lateral part of the MVN project to both abducens and neck motoneurons [17]. The vestibular neurons responsible for the horizontal VOR are in the MVN and in the ventral part of the LVN, those responsible for the vertical VOR are in the superior vestibular nucleus (SVN) [9]. The aim of the present experiments was to determine
* Corresponding author. Tel.: +33-1-4427-3126; fax: +33-1-44275653; e-mail: [email protected]
0304-3940/99/$ - see front matter PII: S03 04-3940(99)001 79-2
whether the IVN, the LVN and/or the SVN receive direct afferent signals from the cells located in the 5me. These 5me neurons also project directly to the cerebellum [5], which is involved in the control and coordination of eyehead movements. Therefore, the second aim of the experiments was to determine if the 5me outputs to the VN and to the cerebellum correspond to separate or collateral projections. Experiments consisted of local microinjections of retrogradely or anterogradely transported neuronal tracers into the VN, the cerebellum or the 5me. In ten adult rats anaesthetized with sodium pentobarbital (50 mg/kg, i.p.) injections of diverse retrograde transport tracers were made in the VN (Fig. 1): biotinylated dextran amine (BDA), complex of wheat germ agglutinin-apo-horseradish peroxidase coupled to colloidal gold (Gold-HRP) or fluorescent ‘fluorored’ (FR). Two animals (Fig. 1: cases V2, V7) also received an additional injection of horseradish peroxidase (HRP) or fluorescent ‘fluoro-green’ (FG) in the ipsilateral cerebellar cortex. In these experiments, retrogradely singly labeled or doubly labeled cells were searched for in the 5me. In one rat an anterograde transport tracer, biocytin, had been injected into the 5me [5]. Examination of this material was made and
1999 Elsevier Science Ireland Ltd. All rights reserved.
134
G. Pinganaud et al. / Neuroscience Letters 264 (1999) 133–136
anterogradely labeled terminals were searched for in the VN. A 10% solution of BDA (10 000 MW, Molecular Probes) in phosphate buffer (PB, 0.1 M, pH 7.4) was iontophoretically injected (7 mA; 7 s on; 7 s off during 20 min). Following 6–10 days of survival, the animals were perfused with 500 ml of fixative (1% glutaraldehyde – 1% formaldehyde in PB). Frozen sections (50 mm) were cut in the transverse plane. The sections were reacted in a 1% solution of avidinbiotin complex (ABC, Vector Laboratories) in PB and then in diaminobenzidine. All sections were counterstained with neutral red. A 5% solution of biocytin in 0.05 M Tris–buffer (pH 8.0) was injected by pressure in the 5me. After 48 h the rat was perfused (4% paraformaldehyde and 0.1% glutaraldehyde in PB). The sections were treated as for BDA injections. The HRP (10% in PB, 0.1 M, pH 7.4) and the gold-HRP were pressure injected (0.5–1 ml) through micropipettes with tip diameters of 40–50 mm. After 7 days survival time, frozen 50 mm thick sections were cut in the transverse plane. The sections were (i) treated for the HRP histochemical reaction or (ii) processed with a silver intensification method in a darkroom following the protocol described by Basbaum and Me´ne´trey [4] to reveal the protein gold complex. The sections were counterstained with neutral red. Injections of FR and FG (Tombow Pencil, Tokyo, Japan). The fluorescent tracers were administered by pressure in the VN or in the cerebellum (0.05–0.1 ml in several points). Following 13 days survival time, 50 mm thick frozen sections were cut in the transverse plane and treated according to Dong et al. [11]. In order to precisely determine the injection site, each third section was counterstained with neutral red. The sections were examined under illumination between 450 and 490 nm for the FG and between 515 and 560 nm for the FR. Injections in the vestibular complex were obtained without any diffusion to adjacent structures. Three injections (Fig. 1: cases V1, V2, V3) were localized within the MVN and three within the IVN (Fig. 1: cases V6, V7, V8). Two injections (Fig. 1: cases V4, V5) affected both the MVN and the IVN. Two injections were made in the LVN (Fig. 1: cases V9, V10): one (case V9) was limited to the ventral LVN, the other (case V10) to the dorsal LVN with a light diffusion of the tracer to the dorsally adjacent SVN. In each of these experiments, retrogradely labeled neurons were found in the 5me (Fig. 1). The present data demonstrate the existence of a projection from the 5me to the MVN, the IVN (Fig. 2A) and the LVN. As the SVN has not been selectively injected in any of our cases, projection from the 5me to the SVN cannot be excluded from these experiments. Following injection of biocytin within the 5me (Fig. 3A) few anterogradely fibers and terminals were labeled in the MVN (Fig. 3B), the IVN, and the ventral and dorsal LVN. In addition, few fibers exhibited small terminal boutons in the peripheral part of the SVN (Fig. 3C). Therefore, these
retrograde and anterograde tracing studies confirm the previously shown projection of 5me neurons onto the MVN [7] and demonstrate additional direct projections, which have not been previously described, from the 5me to the IVN, the LVN and the peripheral SVN. In two animals the technique of double labeling using fluorescent tracers, FR and FG (case V2) or gold-HRP and HRP (case V7), was used. In case V2 the FR injection was centered in the MVN and in case V7 the gold-HRP injection concerned only the IVN. The large cerebellar cortical injections of FG or HRP were performed in the vestibulo-cerebellum including the thin sagittal ‘zone X/CX’ [19] which receives specific projection from the 5me [5]. Involvement of the X/CX zone was verified by the retrograde labeling of inferior olivary neurons in the dorsomedial cell column, which is the specific origin of the climbing fibers reaching the X/CX zone. Singly retrogradely labeled gold-HRP (Fig. 2A), HRP, FG (Fig. 4A) or FR neurons as well as doubly gold-HRP/ HRP (Fig. 2B) or FR/FG (Fig. 4B,C) labeled neurons were observed in the 5me. In spite of the small numbers of doubly labeled neurons observed (Fig. 1), the results provide evidence that some neurons in the caudal part of the 5me project by axon collaterals to the MVN and the cerebellum, others to the IVN and the cerebellum. Whether neurons of the 5me may also project collaterally to the cerebellum and SVN or LVN requires further investigations.
Fig. 1. On the left, injection sites in the vestibular nuclei (V1–V10). On the right are indicated for each experiment (case V1–V10): column two, the tracer injected, column three, the location of injection sites in the vestibular nuclei and column four, the number of labeled neurons in the 5me following the vestibular (VN) and the cerebellar (cereb) injections. In the two cases V2 and V7, which received additional injections of FG or HRP in the cerebellum, the number of doubly labeled neurons is indicated followed by a star. IVN, inferior vestibular nuclei; LVN, lateral vestibular nuclei; MVN, medial vestibular nuclei; SVN, superior vestibular nuclei.
G. Pinganaud et al. / Neuroscience Letters 264 (1999) 133–136
Fig. 2. Injection of gold-HRP in the IVN and HRP in the cerebellum (case V7). (A) Three single retrogradely labeled gold-HRP neurons in the 5me. (B) Two doubly retrogradely gold-HRP/HRP neurons in the 5me. Scale bar, 10 mm.
In conclusion, this study demonstrates projections from the 5me mainly to the MVN, IVN and LVN and the existence of collateral projections from the 5me to the vestibular nuclei and the zone X/CX of the cerebellum. These pathways are likely to contribute to the control of gaze orientation as well as postural mechanisms [6]. The MVN and ventral LVN are a major source of the vestibulo-abducens pathways [13–15]. Neurons in the ventral LVN terminate upon medial rectus motoneurons [3,8]. Therefore the majority of these vestibular neurons are involved in the control of
135
Fig. 4. Injection of fluoro red (FR) in the MVN and fluoro green (FG) in the cerebellum (case V2). Labeled FG (A,B) and FR (C) neurons in the 5me. A doubly labeled neuron shows FG labeling (arrow head in B) and FR labeling (arrow head in C). Scale bar, 10 mm.
the horizontal eye movements, while only few contribute to vertical eye movements [16]. Furthermore, the LVN as well as the IVN have connections with the cervical spinal cord [8,18]. It appears that sensory inputs from the face, may influence oculomotor as well as head postural control through their projections upon the premotor regions of MVN, IVN or LVN. Afferent signals from EOM influence eye and neck muscle activities [2,10,12]. Whether the 5me afferents described here derive from EOM remains to be determined. However, the ganglionic neurons of the EOM sensory receptors are located in the caudal part of the 5me [1], and it has been demonstrated that some of these neurons project to the MVN [7]. We show here that, neurons projecting to the vestibular nuclei are exclusively localized in the caudal part of the 5me. Accordingly, the present data demonstrates a pathway through which proprioceptive information from the EOM may act upon the coordination of the associated eye and head movements for gaze stabilization. We are grateful to Dr. S. Wiener for helpful comments on an earlier version of the text. We thank M. Diagne for technical assistance and B. Jay for photographic assistance. This work was supported by INSERM, grant Nos. 4M102E and 4M103E.
Fig. 3. Injection in the 5me. (A) Injection site. Anterogradely labeled terminals in the MVN (B) and the SVN (C). Scale bar, 35 mm in (A), 20 mm in (B,C).
[1] Alvarado-Mallart, M.R., Batini, C., Buisseret-Delmas, C. and Corvisier, J., Trigeminal representation of the masticatory and extraocular proprioceptors as revealed by horseradish peroxidase retrograde transport, Exp. Brain Res., 23 (1975) 167– 179. [2] Ashton, J.A., Milleret, C. and Donaldson, I.M.L., Effects of affer-
136
[3]
[4]
[5]
[6]
[7]
[8]
[9] [10]
[11]
G. Pinganaud et al. / Neuroscience Letters 264 (1999) 133–136 ent signals from the extraocular muscles upon units in the cerebellum, vestibular nuclear complex and oculomotor nucleus of the trout, Neuroscience, 31 (1989) 529–541. Baker, J.A. and Highstein, S.M., Vestibular projections to medial rectus subdivision of oculomotor nucleus, J. Neurophysiol., 41 (1978) 1629–1646. Basbaum, A.I. and Menetrey, D., Wheat germ agglutininapoHRP gold: a new retrograde tracer for light and electronmicroscopic single and double-labeled studies, J. Comp. Neurol., 261 (1987) 306–318. Billig, I., Yatim, N. and Compoint, C., Cerebellar afferences from the mesencephalic trigeminal nucleus in the rat, NeuroReport, 6 (1995) 2293–2296. Buisseret-Delmas, C., Angaut, P., Compoint, C., Diagne, M. and Buisseret, P., Brainstem efferents from the interface between the nucleus medialis and the nucleus interpositus in the rat, J. Comp. Neurol., 402 (1998) 264–265. Buisseret-Delmas, C., Epelbaum, M. and Buisseret, P., The vestibular nuclei of the cat receive a primary afferent projection from receptors in extraocular muscles, Exp. Brain Res., 81 (1890) 654–658. Carleton, S.C. and Carpenter, M.B., Afferent and efferent connections of the medial inferior and lateral vestibular nuclei in the cat and the monkey, Brain Res., 278 (1983) 29–51. Carpenter, R.H.S., Movements of the Eyes, Pion, London, 1988. Donaldson, I.M.L. and Knox, P.C., Afferents signals from pigeon extraocular muscles modify the vestibular responses of units in the abducens nucleus, Proc. R. Soc. Lond., 244 (1991) 233–239. Dong, K., Qu, T., Ahmed, F.A.K.M., Zhang, L., Yamada, K.,
[12]
[13]
[14]
[15]
[16]
[17]
[18]
[19]
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