Namxrience Voi. 4. pp. 651 to 657 Pergamon Press Ltd. 1979. Printed in Great
Britain
MULTIPOLAR NEURONS IN THE CAT VESTIBULAR GANGLION M. CHAT and A. SANS Laboratoire de Neurophysiologie
Seusorielle, Universitt de Montpellier II-34060 Montpellier Cedes France
Ahstraet-Multipolar neurons of the vestibular ganglion were studied in the cat. Seriaf semi-thin sections showed that they were most frequently tripolar and unmyelinated. Injections of horseradish peroxidase at the level of the vestibular receptor or in the vestibular nuclei showed that these neurons were indeed of the vestibular type. Several hypotheses are suggested concerning the role of these multipolar neurons.
NEURONSof the vestibular
ganglion are typically bi- phate buffer, and then dehydrated in graded alcohols. After embedding in Araldite, semi-thin sections were seriahy cut polar and their perikaryon is surrounded by a myelin and stained with toluidine blue. sheath. Their ultrastructural features were described nticks sections. Using 6 cats, anesthetized with sodium for the first time in the goldfish by R~~ENBLUTH& pentobarbital, we sectioned the posterior ampullar nerve PALAY(1961) and in the rat by ROSENBLU~B (1962). very close to the crista ampullaris. 0.5-l pi of 20% horseHowever, some of these ganglion cells are multipolar. radish peroxidase (HRP) (type VI Sigma) was used. Time This fact had been suggested by the first anatomists allowed for survival was spaced out from 2 to 24 h. With (AYERS,1893; RETZIUS, 1895; BCNERO,1914), but it a knife positioned stereotaxically, sections of the vestibular has since been almost totally forgotten. Using a scanfibers at the level of the superior nucleus and the ventral ning electron microscope, Ross 8c BURKEL (1973) part of the lateral vestibular nucleus were made on 9 cats. Three microliters of HRP was slowly injected through a recently proved the existence of multipolar neurons syringe. Survival time was spaced in the rat spiral g~glion which they described as 10 ~1 rna~~r-Hamilton being unmyelinated and parasympathetic. In a out from 4 to 17 h. After perfusion with 1% glutaraldehyde physiological study, however, CASTON& GROBBNSKI and 1% paraformaldehyde in a 0.f M phosphate buffer (pH 7.4) the vestibular ganglia were stored at 4°C overnight (1975) showed the existence of a control by receptorin a 0.1 M phosphate buffer with 30% sucrose. 20/cm thick receptor fibers in the frog which could be explained frozen sections were cut in a cryostat, put onto the slide. by the presence of multipolar vestibular neurons. The and then incubated in 3,3’-diaminobenzidine in tris buffer aim of this paper is to record the different multipolar (pH 7.6) and hydrogen peroxide. They were afterwards neurons and, more particularly, to determine whether rinsed in phosphate buffer and distilled water, stained with they are vegetative or sensory. toluidine blue, and mounted. In order to demonstmte the existence of multipolar neurons, a series of semi-thin sections (l-2 m) of the vestibular ganglion were cut serially. We also used RESULTS the property of damaged axons of absorbing horseradish peroxidase (HRP) more intensely (HALPERIN Multipolar neurons on semi-thin serial sections A small percentage of neurons (see below) were & LA VAIL, 1975). Under these conditions, we obtained highly contrasted neurons (ROBERTSON,multipolar which rendered identifying them particu1977) as well as nerve fibers similar to Golgi 9ne.s larly difficult. The investigative method of using semi(REPERANT,1977; HUNT, STREIT,K~JNZLE& CUENOD, thin serial sections revealed 2 facts: the first that the 1977). majority of the multipolar neurons studied using this technique appeared to be. tripolar, and the second that these neurons very often have a pro~ngation EXPERIMENTAL PROCEDURES process located in a peripheral position and two Vestibular ganglia of 20 adult cats were studied using others located in a central position (Figs IA, B, E semi-thin serial sections with an ultramicrotome and thick and F). However, we also found neurons having a sections on a freezing microtome. double peripheral process (Fig 1G). We furthermore Semi-thin sections.AAer perfusing 5 animals with 1% gluestablished that generally 2 processes emerge from the taraldehyde and 4% paraformaldehyde in a 0.1 M phosphate buffer (pH 7.4), the vestibular ganglion was removed, same point (Fig 1). In some cases, this departure post-fixed for 2 h in 1% osmium tetroxide in a 0.1 M phospoint was in a lateral position (Fig 11), but we were unable firmly to substantiate the multipolar nature Abbreviation: HRP, horseradish peroxidase. of these neurons. The soma of the muitipolar neurons 651
652
M. CHAT and A. SANS
are often unmyelinated; most frequently the myelin sheath appears at the first node of Ranvier (Fig. 1). Multipolar neurons on thick sections in horseradish peroxidase preparations
An evaluation of the number of the multipolar neurons was made on 3 ganglia. Of the 928 neurons observed, 39 show more than 2 processes, an average of 4.2% Distal ending section. The HRP deposit on the transected ampullar nerve slice causes a massive intraaxonal cellulipetal enzyme transport after survival periods varying from 2 to 24 h, depending upon the animal. For example, in cats having survived 4 h, a very intense reaction of HRP to the diaminobenzidine at the cell body level and their processes occurs. For longer survival periods or for those shorter than 4 h, the reaction was much weaker or absent on the vestibular ganglion level. After 8 h, the fibers located at the intracerebral level of the vestibular root showed an intra-axonal transport of HRP. For a suitable period (4 h), the thick sections also indicated bipolar, tripolar and quadripolar neurons with processes showing extremely clear emerging points (Fig. 2). Proximal ending section. After sectioning the axonal endings in order to make the enzyme uptake easier, we injected 3~1 of HRP into the vestibular nuclei. Following several attempts using different survival periods (see experimental procedures), we found that the retrograde flow of HRP reached the vestibular ganglion cells after 7 h. Incubation with diaminobenzidine revealed heavily stained bipolar cells as well as the multipolar cells described above (Fig. 3). This last result enabled us to confirm that the multipolar neurons of the Scarpa ganglion were indeed vestibular neurons. DISCUSSION Using silver impregnation techniques, BOVERO (1914) showed the existence of multipolar neurons of various shapes in the Scarpa ganglion of numerous mammals, including man. Ross & BURKEL(1973) also described multipolar neurons in the rat spiral ganglion. Our results confirm the existence of these neurons in the vestibular ganglion, of which the majority are tripolar.
lar neurons was similar to that of neurons of the otic ganglion of the rabbit (DIXON,1966). We must take into consideration 2 facts: the first that the efferent fibers, unmyelinated in their great majority, cross the spiral and vestibular ganglia and are cholinergic; the second, that we were unable to show synapses on the multipolar neurons. Finally, if the multipolar neurons have a unmyelinated soma, they most frequently show expansions which become myelinated at the first Ranvier node. That would lead to the assumption that they are modified sensory cells with a mixture of morphological patterns characteristic for both bipolar and pseudounipolar nerve cells. Our results show that the multipolar neurons are not post-ganglionic. Indeed, after injecting small amounts of HRP into the vestibular nuclei, we noticed that the enzyme spread during its retrograde vestibular migration was intra-axonal and that the multipolar neurons appeared not only marked, but also marked in the same intensive way as the bipolar neurons. Accepting the hypothesis of the post-ganglionic nature of multipolar neurons, we would also have to admit that HRP could migrate through the axoplasm fibers undergoing a direct Wallerian degeneration and cross the synaptic barrier, though this has never been proved. We can confirm that the multipolar neurons are of the vestibular type. We must emphasize that SPO~VDLIN(1972) showed in the spiral ganglion, after a section of the cochlear nerve, that only the unmyelinated neurons did not degenerate. Ross & BURKEL (1973) came to the conclusion that they were multipolar neurons which did not give off central processes. We maintain that the absence of irreversible degeneration in this case can be explained by the fact that the amount of excluded axoplasm is insufficient in relation to the remaining axoplasmic volume (SANS, RAYMOND& MARTY,1969). What is the role of the multipolar neurons?
We know that bipolar neurons of the vestibular ganglion transmit information to the primary nuclei. This information comes from a cell or a group of sensory cells belonging to the same receptor. Concerning the multipolar cells, the distal processes which occupy the dendrite position can be explained in 1 of9 ways: either the fibers come from the vestibular receptor or they come from 2 distinct receptors. What is the nature of the multipolar neurons? Theoretically, the 2 proximal processes can either go Fluorescent studies (SPOENDLIN dc LICHTENSTEIGER, together into the vestibular nuclei or go separately, 1966, 1967; TERAYAMA,HOLZ & BECK, 1966; Ross, 1 to the vestibular nuclei and the other to a receptor. 1969) have shown that the unmyelinated neurons of In the latter case, there would be the possibility of a direct control of one receptor by another (CASTON the spiral ganglion which correspond to multipolar neurons & GRIBENSKI,1975). It is not impossible that a second were not sympathetic post-ganglionic efferent system exists in the labyrinth. neurons. However, Ross & BURKEL(1973) believed that they could be parasympathetic neurons. In fact, they observed a positive acetylcholinesterase reaction in the spiral ganglion (Ross, 1969; 1973) and, accordAcknowledgement-This research was supported by grants ing to these authors, the ultrastructure of the multipofrom the INSERM (CL. 78.1.001.6).
FIG. 1. Multipolar neurons in the vestibular ganglion: semi-thin section (I pm) stained with toluidine blue. Their preganglionic process is located in the top part of the pictures. AB. EF, Serial sections of tripolar cells showing one peripheral process and two central processes. x 1100. x 475; C. Unmyetinated cell whose axonal processes are laid out in a central position. x 1320: D-H, Another unmyelinated cell whose one {double arrow) of the two axonal processes (arrow) seems to take a peripheral direction. x 1320, x 500; G, Cell with two peripheral processes. x 450; I, Cell with two laterally located processes. x 1320. FIG. 2. Vestibular ganglion neurons 4 h after deposition of horseradish peroxidase on the posterior ampullar nerve. Their preganglionic process is located in the top part of the pictures. A. Quadripolar cell. x 1650: B,C. Tripolar cells x 700, x 1250. FIG. 3. Vestibular ganglion neurons 7 h after injection of horseradish peroxidase into the vestibuiar nuclei. Their pre~nglionic process is located in the top part of the pictures: A, Quadripolar cell x 1250; B,C,D, Tripolar cells. x 1200, x 1320, x 1320.
653
FIG. 1 654
FIG. 2.
655
FIG. 3.
656
Multipolar neurons in vestibular ganglion
651
REFERENCES AYERSH. (1893) ijber das peripherische Verhalten der Geh6rnerven
und den Wert der Haarzellen des Gehiirorganes.
Anar. Anz. 8, 435-440. BOVEROA. (1914) Sulla fine struttura e sulle connessioni del ganglio vestibolare de1 nervo acoustico. Memorie
R. Accad.
Sci. Torino (Grie II) 64, 10, l-37. CASTONJ. & GRIBENSKIA. (1975) Influence of receptor-receptor fibres on the spontaneous agerent activity from semicircular canals in the frog. P&ers Arch. ges. Physiol. 358, 81-88. DIXON J. (1966) The fine structure of parasympathetic nerve cells in the otic ganglion of the rabbit. Anar. Rec. 1%.
239. HALPERINJ. J. & LA VAILJ. H. (1975) A study of the dynamics of retrograde transport and accumulation of horseradish peroxidase in injured neurons. Brain Res. 100, 253-270.
HUNT S. P., STREITP., KUNZLE H. & CUENODM. (1977) Characterization of the pigeon isthmo-tectal pathway by selective uptake and retrograde movement of radio-active compounds and by Golgi-like horseradish peroxidase labeling. Bruin Res. 129, 197-212. REPERANTJ. (1977) The orthograde transport of horseradish peroxidase in the visual system. Brain Res. 85, 307-312. RETZIUSG. (1895) Biologische Untersuchungen. Vol. 6, Leipzig, Vogel. ROBERTSON R. T. (1977) Bidirectional movement of horseradish peroxidase and the demonstration of reciprocal thalamocortical connections. Brain Res. 130, 538-544. ROSENBLUTH J. (1962) The fine structure of acoustic ganglia in the rat. J. Cell Biol. 12, 329-359. ROSENBLUTH J. & PALAY S. (1961) The fine structure of nerve cell bodies and their myelin sheaths in the eighth nerve ganglion of the goldfish. J. biophys. biochem. Cytol. 9, 853-877. Ross M. D. (1969) The general visceral efferent component of the eighth cranial nerve. J. camp. Neural. 135, 45>477. Ross M. D. (1973) Autonomic components of the VIIIth nerve. Adu. Oto-rhino-luryng. 20, 316336. Ross M. & BURKELW. (1973) Multipolar neurons in the spiral ganglion of the Rat. Acta Oto-lar. 76, 381-394. SANSA., RAYMOND J. & MARTYR. (1969) %gCntrescence exp&imentale des neurones du ganglion de Scarpa constcutive B la section de leurs axones. C. r. hebd. SGanc. Acad. Sci., Paris 268, 543-545. SPOENDLINH. (1972) Innervation densities of the cochlea. Acta Oto-lar. 73, 235-248. SPOENDLINH. & LICHTENSTEIGER W. (1966) The adrenergic innervation of the labyrinth. Acta Oto-lur. 61, 421-434. SPOENDLINH. & LICHTENSTEIGER W. (1967) The sympathetic nerve supply to the inner ear. Arch. Klin. Exp. Ohr. Nas Kehlkopfheilk.
189, 346-359.
TERAYAMA Y., HOLZ E. & BECK C. (1966) Adrenergic innervation of the cochlea. Ann. Otol. Rhinol. Lar. 75, 69-86. (Accepted
8 December
1978)
Britain
MULTIPOLAR NEURONS IN THE CAT VESTIBULAR GANGLION M. CHAT and A. SANS Laboratoire de Neurophysiologie
Seusorielle, Universitt de Montpellier II-34060 Montpellier Cedes France
Ahstraet-Multipolar neurons of the vestibular ganglion were studied in the cat. Seriaf semi-thin sections showed that they were most frequently tripolar and unmyelinated. Injections of horseradish peroxidase at the level of the vestibular receptor or in the vestibular nuclei showed that these neurons were indeed of the vestibular type. Several hypotheses are suggested concerning the role of these multipolar neurons.
NEURONSof the vestibular
ganglion are typically bi- phate buffer, and then dehydrated in graded alcohols. After embedding in Araldite, semi-thin sections were seriahy cut polar and their perikaryon is surrounded by a myelin and stained with toluidine blue. sheath. Their ultrastructural features were described nticks sections. Using 6 cats, anesthetized with sodium for the first time in the goldfish by R~~ENBLUTH& pentobarbital, we sectioned the posterior ampullar nerve PALAY(1961) and in the rat by ROSENBLU~B (1962). very close to the crista ampullaris. 0.5-l pi of 20% horseHowever, some of these ganglion cells are multipolar. radish peroxidase (HRP) (type VI Sigma) was used. Time This fact had been suggested by the first anatomists allowed for survival was spaced out from 2 to 24 h. With (AYERS,1893; RETZIUS, 1895; BCNERO,1914), but it a knife positioned stereotaxically, sections of the vestibular has since been almost totally forgotten. Using a scanfibers at the level of the superior nucleus and the ventral ning electron microscope, Ross 8c BURKEL (1973) part of the lateral vestibular nucleus were made on 9 cats. Three microliters of HRP was slowly injected through a recently proved the existence of multipolar neurons syringe. Survival time was spaced in the rat spiral g~glion which they described as 10 ~1 rna~~r-Hamilton being unmyelinated and parasympathetic. In a out from 4 to 17 h. After perfusion with 1% glutaraldehyde physiological study, however, CASTON& GROBBNSKI and 1% paraformaldehyde in a 0.f M phosphate buffer (pH 7.4) the vestibular ganglia were stored at 4°C overnight (1975) showed the existence of a control by receptorin a 0.1 M phosphate buffer with 30% sucrose. 20/cm thick receptor fibers in the frog which could be explained frozen sections were cut in a cryostat, put onto the slide. by the presence of multipolar vestibular neurons. The and then incubated in 3,3’-diaminobenzidine in tris buffer aim of this paper is to record the different multipolar (pH 7.6) and hydrogen peroxide. They were afterwards neurons and, more particularly, to determine whether rinsed in phosphate buffer and distilled water, stained with they are vegetative or sensory. toluidine blue, and mounted. In order to demonstmte the existence of multipolar neurons, a series of semi-thin sections (l-2 m) of the vestibular ganglion were cut serially. We also used RESULTS the property of damaged axons of absorbing horseradish peroxidase (HRP) more intensely (HALPERIN Multipolar neurons on semi-thin serial sections A small percentage of neurons (see below) were & LA VAIL, 1975). Under these conditions, we obtained highly contrasted neurons (ROBERTSON,multipolar which rendered identifying them particu1977) as well as nerve fibers similar to Golgi 9ne.s larly difficult. The investigative method of using semi(REPERANT,1977; HUNT, STREIT,K~JNZLE& CUENOD, thin serial sections revealed 2 facts: the first that the 1977). majority of the multipolar neurons studied using this technique appeared to be. tripolar, and the second that these neurons very often have a pro~ngation EXPERIMENTAL PROCEDURES process located in a peripheral position and two Vestibular ganglia of 20 adult cats were studied using others located in a central position (Figs IA, B, E semi-thin serial sections with an ultramicrotome and thick and F). However, we also found neurons having a sections on a freezing microtome. double peripheral process (Fig 1G). We furthermore Semi-thin sections.AAer perfusing 5 animals with 1% gluestablished that generally 2 processes emerge from the taraldehyde and 4% paraformaldehyde in a 0.1 M phosphate buffer (pH 7.4), the vestibular ganglion was removed, same point (Fig 1). In some cases, this departure post-fixed for 2 h in 1% osmium tetroxide in a 0.1 M phospoint was in a lateral position (Fig 11), but we were unable firmly to substantiate the multipolar nature Abbreviation: HRP, horseradish peroxidase. of these neurons. The soma of the muitipolar neurons 651
652
M. CHAT and A. SANS
are often unmyelinated; most frequently the myelin sheath appears at the first node of Ranvier (Fig. 1). Multipolar neurons on thick sections in horseradish peroxidase preparations
An evaluation of the number of the multipolar neurons was made on 3 ganglia. Of the 928 neurons observed, 39 show more than 2 processes, an average of 4.2% Distal ending section. The HRP deposit on the transected ampullar nerve slice causes a massive intraaxonal cellulipetal enzyme transport after survival periods varying from 2 to 24 h, depending upon the animal. For example, in cats having survived 4 h, a very intense reaction of HRP to the diaminobenzidine at the cell body level and their processes occurs. For longer survival periods or for those shorter than 4 h, the reaction was much weaker or absent on the vestibular ganglion level. After 8 h, the fibers located at the intracerebral level of the vestibular root showed an intra-axonal transport of HRP. For a suitable period (4 h), the thick sections also indicated bipolar, tripolar and quadripolar neurons with processes showing extremely clear emerging points (Fig. 2). Proximal ending section. After sectioning the axonal endings in order to make the enzyme uptake easier, we injected 3~1 of HRP into the vestibular nuclei. Following several attempts using different survival periods (see experimental procedures), we found that the retrograde flow of HRP reached the vestibular ganglion cells after 7 h. Incubation with diaminobenzidine revealed heavily stained bipolar cells as well as the multipolar cells described above (Fig. 3). This last result enabled us to confirm that the multipolar neurons of the Scarpa ganglion were indeed vestibular neurons. DISCUSSION Using silver impregnation techniques, BOVERO (1914) showed the existence of multipolar neurons of various shapes in the Scarpa ganglion of numerous mammals, including man. Ross & BURKEL(1973) also described multipolar neurons in the rat spiral ganglion. Our results confirm the existence of these neurons in the vestibular ganglion, of which the majority are tripolar.
lar neurons was similar to that of neurons of the otic ganglion of the rabbit (DIXON,1966). We must take into consideration 2 facts: the first that the efferent fibers, unmyelinated in their great majority, cross the spiral and vestibular ganglia and are cholinergic; the second, that we were unable to show synapses on the multipolar neurons. Finally, if the multipolar neurons have a unmyelinated soma, they most frequently show expansions which become myelinated at the first Ranvier node. That would lead to the assumption that they are modified sensory cells with a mixture of morphological patterns characteristic for both bipolar and pseudounipolar nerve cells. Our results show that the multipolar neurons are not post-ganglionic. Indeed, after injecting small amounts of HRP into the vestibular nuclei, we noticed that the enzyme spread during its retrograde vestibular migration was intra-axonal and that the multipolar neurons appeared not only marked, but also marked in the same intensive way as the bipolar neurons. Accepting the hypothesis of the post-ganglionic nature of multipolar neurons, we would also have to admit that HRP could migrate through the axoplasm fibers undergoing a direct Wallerian degeneration and cross the synaptic barrier, though this has never been proved. We can confirm that the multipolar neurons are of the vestibular type. We must emphasize that SPO~VDLIN(1972) showed in the spiral ganglion, after a section of the cochlear nerve, that only the unmyelinated neurons did not degenerate. Ross & BURKEL (1973) came to the conclusion that they were multipolar neurons which did not give off central processes. We maintain that the absence of irreversible degeneration in this case can be explained by the fact that the amount of excluded axoplasm is insufficient in relation to the remaining axoplasmic volume (SANS, RAYMOND& MARTY,1969). What is the role of the multipolar neurons?
We know that bipolar neurons of the vestibular ganglion transmit information to the primary nuclei. This information comes from a cell or a group of sensory cells belonging to the same receptor. Concerning the multipolar cells, the distal processes which occupy the dendrite position can be explained in 1 of9 ways: either the fibers come from the vestibular receptor or they come from 2 distinct receptors. What is the nature of the multipolar neurons? Theoretically, the 2 proximal processes can either go Fluorescent studies (SPOENDLIN dc LICHTENSTEIGER, together into the vestibular nuclei or go separately, 1966, 1967; TERAYAMA,HOLZ & BECK, 1966; Ross, 1 to the vestibular nuclei and the other to a receptor. 1969) have shown that the unmyelinated neurons of In the latter case, there would be the possibility of a direct control of one receptor by another (CASTON the spiral ganglion which correspond to multipolar neurons & GRIBENSKI,1975). It is not impossible that a second were not sympathetic post-ganglionic efferent system exists in the labyrinth. neurons. However, Ross & BURKEL(1973) believed that they could be parasympathetic neurons. In fact, they observed a positive acetylcholinesterase reaction in the spiral ganglion (Ross, 1969; 1973) and, accordAcknowledgement-This research was supported by grants ing to these authors, the ultrastructure of the multipofrom the INSERM (CL. 78.1.001.6).
FIG. 1. Multipolar neurons in the vestibular ganglion: semi-thin section (I pm) stained with toluidine blue. Their preganglionic process is located in the top part of the pictures. AB. EF, Serial sections of tripolar cells showing one peripheral process and two central processes. x 1100. x 475; C. Unmyetinated cell whose axonal processes are laid out in a central position. x 1320: D-H, Another unmyelinated cell whose one {double arrow) of the two axonal processes (arrow) seems to take a peripheral direction. x 1320, x 500; G, Cell with two peripheral processes. x 450; I, Cell with two laterally located processes. x 1320. FIG. 2. Vestibular ganglion neurons 4 h after deposition of horseradish peroxidase on the posterior ampullar nerve. Their preganglionic process is located in the top part of the pictures. A. Quadripolar cell. x 1650: B,C. Tripolar cells x 700, x 1250. FIG. 3. Vestibular ganglion neurons 7 h after injection of horseradish peroxidase into the vestibuiar nuclei. Their pre~nglionic process is located in the top part of the pictures: A, Quadripolar cell x 1250; B,C,D, Tripolar cells. x 1200, x 1320, x 1320.
653
FIG. 1 654
FIG. 2.
655
FIG. 3.
656
Multipolar neurons in vestibular ganglion
651
REFERENCES AYERSH. (1893) ijber das peripherische Verhalten der Geh6rnerven
und den Wert der Haarzellen des Gehiirorganes.
Anar. Anz. 8, 435-440. BOVEROA. (1914) Sulla fine struttura e sulle connessioni del ganglio vestibolare de1 nervo acoustico. Memorie
R. Accad.
Sci. Torino (Grie II) 64, 10, l-37. CASTONJ. & GRIBENSKIA. (1975) Influence of receptor-receptor fibres on the spontaneous agerent activity from semicircular canals in the frog. P&ers Arch. ges. Physiol. 358, 81-88. DIXON J. (1966) The fine structure of parasympathetic nerve cells in the otic ganglion of the rabbit. Anar. Rec. 1%.
239. HALPERINJ. J. & LA VAILJ. H. (1975) A study of the dynamics of retrograde transport and accumulation of horseradish peroxidase in injured neurons. Brain Res. 100, 253-270.
HUNT S. P., STREITP., KUNZLE H. & CUENODM. (1977) Characterization of the pigeon isthmo-tectal pathway by selective uptake and retrograde movement of radio-active compounds and by Golgi-like horseradish peroxidase labeling. Bruin Res. 129, 197-212. REPERANTJ. (1977) The orthograde transport of horseradish peroxidase in the visual system. Brain Res. 85, 307-312. RETZIUSG. (1895) Biologische Untersuchungen. Vol. 6, Leipzig, Vogel. ROBERTSON R. T. (1977) Bidirectional movement of horseradish peroxidase and the demonstration of reciprocal thalamocortical connections. Brain Res. 130, 538-544. ROSENBLUTH J. (1962) The fine structure of acoustic ganglia in the rat. J. Cell Biol. 12, 329-359. ROSENBLUTH J. & PALAY S. (1961) The fine structure of nerve cell bodies and their myelin sheaths in the eighth nerve ganglion of the goldfish. J. biophys. biochem. Cytol. 9, 853-877. Ross M. D. (1969) The general visceral efferent component of the eighth cranial nerve. J. camp. Neural. 135, 45>477. Ross M. D. (1973) Autonomic components of the VIIIth nerve. Adu. Oto-rhino-luryng. 20, 316336. Ross M. & BURKELW. (1973) Multipolar neurons in the spiral ganglion of the Rat. Acta Oto-lar. 76, 381-394. SANSA., RAYMOND J. & MARTYR. (1969) %gCntrescence exp&imentale des neurones du ganglion de Scarpa constcutive B la section de leurs axones. C. r. hebd. SGanc. Acad. Sci., Paris 268, 543-545. SPOENDLINH. (1972) Innervation densities of the cochlea. Acta Oto-lar. 73, 235-248. SPOENDLINH. & LICHTENSTEIGER W. (1966) The adrenergic innervation of the labyrinth. Acta Oto-lur. 61, 421-434. SPOENDLINH. & LICHTENSTEIGER W. (1967) The sympathetic nerve supply to the inner ear. Arch. Klin. Exp. Ohr. Nas Kehlkopfheilk.
189, 346-359.
TERAYAMA Y., HOLZ E. & BECK C. (1966) Adrenergic innervation of the cochlea. Ann. Otol. Rhinol. Lar. 75, 69-86. (Accepted
8 December
1978)
