Nigral Projections to the Inferior and the Superior Colliculus in the Rat: A Horseradish Peroxidase Study
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1 Okajimas Foils Anat. Jpn., 56(5) : , December 1979 Nigral Projections to the Inferior and the Superior Colliculus in the Rat: A Horseradish Peroxidase Study By KAZUO WATANABE and ETSURO KAWANA Department of Anatomy, Hamamatsu University School of Medicine, 3600 Handa-cho, Hamamatsu , Japan Received for Publication, March 19, 1979 Key Words: Substantia nigra, Inferior colliculus, Superior colliculus, Horseradish peroxidase, Summary. Nigral projections to the inferior colliculus were examined in the rat, using the HRP method. After HRP injections into the inferior colliculus, labeled cells were found mainly in the pars lateralis of the substantia nigra but a few were present in the contralateral pars lateralis. These cells were found abundantly in the posterior portion of the pars lateralis and to some extent in the anterior portion of this structure. When HRP was injected into the superior colliculus, HRPmarked neurons were found mainly in the pars reticulata together with a few in the anterior portion of the pars lateralis. The substantia nigra is divided into three parts : the pars compacta, pars reticulata and pars lateralis (Rioch, 1929; Gillilan, 1943 ; Konig and Klippel, 1963 ; Hanaway et al., 1970). Current knowledge about the regional projections of the substantia nigra indicates that the pars compacta projects to the striatum (see Faull and Mehler, 1978) and that the pars reticulata sends fibers to the thalamus (see Faull and Mehler, 1978), to the superior colliculus (Hopkins and Niessen, 1976 ; Rinvik et al., 1976; Jayaraman et al., 1977; Faull and Mehler, 1978 ; Graybiel, 1978 ; Grofova et al., 1978), and to the lower brain stem (Hopkins and Niessen, 1976 ; Rinvik et al., 1976). Using the pyridine silver method, Rioch ('29) reported nigral efferents to the inferior colliculus in the cat and dog. Afifi and Kaelber ('65) demonstrated nigral projections to the inferior colliculus in the cat, using the Nauta-Gygax technique. However, Afifi et al. ('70) later questioned these results, for the cortico-tectal and cortico-tegmental fibers passed through the substantia nigra. The purpose of the present paper is to confirm the existence of the nigro-inferior collicular pathway and to describe the exact location of the cells of origin, with which cells projecting to the superior colliculus are compared. Material and Methods The animals used in this investigation were Wistar strain male rats (7-14 weeks old) obtained commercially. Under pentobarbital anesthesia, 30-50% HRP (Sigma, Type VI) dissolved in saline was injected hydraulically into the inferior 289
2 290 K. Watanabe and E. Kawana colliculus or into the superior colliculus by means of a stereotaxically guided micropipette connected to a microsyringe (Nauta et al., 1974). After 1-3 days, the deeply anesthetized animals were perfused with' 0.85% sodium chloride solution through the ascending aorta and then with fixative consisting of 1.25% Fig. 1. Frontal sections showing the HRP-deposited part in the inferior colliculus (left) and HRP-marked neurons on the substantia nigra (right) in R145. The figures are numbered in the rostral to caudal direction. In the figure for the substantia nigra (right), the medial side of the substantia nigra is shown to the left. Oblique-shaded and dark areas indicate weakly and densely HRP-deposited parts, respectively. C, pars compacta of the substantia nigra ; CC, cerebral peduncle ; IC, inferior colliculus ; L, pars lateralis of the substantia nigra ; R, pars reticulata of the substantia nigra ; SC, superior colliculus.
3 Nigral Projections to the Inferior and the Superior Colliculns 291 glutaraldehyde, 0.5% paraformaldehyde, and 5% saccharose in 0.1 M phosphate buffer (ph 7.4). The brains were dissected out and stored in a solution of 1.25% glutaraldehyde and 30% saccharose in 0.1 M phosphate buffer (ph 7.4). Serial 40 pm sections were cut on a freezing microtome and incubated in the medium of Graham and Karnovsky ('66). These sections were then mounted on gelatincoated slide glasses and counterstained with cresyl violet. Part of the materials used in this investigation has been described previously (Watanabe and Kawana, 1979). Result and Discussion In 9 rats, an injection of pi of HRP was made into the inferior colliculus without diffusion to the periaqueductal gray or the superior colliculus. In R145, HRP was deposited mainly in the posterior half of the inferior colliculus, with diffusion in the anterior half of the inferior colliculus (Figs. 1 and 3A). Labeled cells were found mainly in the ipsilateral pars lateralis of the substantia nigra, but a few were present in the contralateral pars lateralis. These were somewhat denser in the posterior portion than in the anterior portion (Fig. 1). The cells labeled by HRP in the posterior portion were mainly fusiform and the long axis of each cell was oriented mainly in the dorsomedial direction (Fig. 4A and B). The labeled cells in the anterior portion exhibited various shapes (Fig. 4C and D). No HRP-marked neurons were found in the pars compacta or pars reticulata. Similar results were obtained in the 8 other cases. This indicated that nigral neurons projecting to the inferior colliculus are not situated in the pars compacta or pars reticulata, but in the pars lateralis. HRP was injected into the superior colliculus of 16 rats. In R101, HRP was deposited mainly in the whole laminae of the superior colliculus, but slight amounts of the enzyme diffused into the periaqueductal gray (Figs. 2 and 3B). HRP-marked neurons were located ipsilaterally in the pars reticulata and a few were present in the pars lateralis. At the anterior level of the pars reticulata, labeled cells were located in its medial portion, and in the posterior direction, HRP-marked cells were observed in the lateral portion of the pars reticulata. Finally, these cells were observed in its lateral margin (Fig. 2). In the contralateral pars reticulata, a few neurons were labeled. Some HRP-marked neurons were observed in the anterior portion of the pars lateralis on the injected side, but no labeling was observed in the posterior portion of this subdivision. Other cases, in which HRP was deposited in all laminae of the superior colliculus, showed similar results. No HRP-marked neurons were observed in the substantia nigra, when HRP was confined to the superficial layer of the superior colliculus. The above observations indicate that the pars lateralis of the substantia nigra projects to the inferior colliculus. The anterior portion of the pars lateralis projects to the inferior colliculus and probably to the superior colliculus, while the posterior portion sends fibers to the inferior colliculus. Hanaway et al. ('70) subdivided the pars lateralis into anterior and posterior portions based on Nissl picutures. Using the Nauta-Gygax technique, Afifi and Kaelber ('65) reported nigral projections to the inferior colliculus. However, Afifi et al. ('70) later questioned the existence of this route. Recently, Jayaraman et al. ('77) found that nigral fibers to the superior colliculus passed through the periaqueductal gray medial to the rostral portion of the inferior colliculus, but
4 292 K. Watanabe and E. Kawana Fig. 2. Frontal sections showing the HRP-deposited part in the superior colliculus (left) and HRP-marked neurons in the substantia nigra (right) in R101. Symbols and abbreviations as in Fig. 1. they did not describe nigral fibers to the inferior colliculus. There is some possibility that the labeling of cells of the pars lateralis after inferior collicular injections is a result of damage to nigrosuperior collicular fibers which pass medial to the rostral portion of the inferior colliculus. However, this seems unlikely for the following reasons. In our study, labeled cells were observed in the pars lateralis when the pipette used in HRP injection was placed even in the posterior portion of the inferior colliculus. If these fibers were damaged when HRP was injected into the inferior colliculus, it could be expected that some labeled cells would be observed in the pars reticulata. No such labeling was found in the pars reticulata after inferior collicular injection. Faun and Mehler ('78) reported that the pars reticulata of the substantia
5 Nigral Projections to the Inferior and the Superior Colliculus 293 nigra of the rat projected to the superior colliculus. In the present investigation, it was apparent that the pars reticulata projects to the superior colliculus and that the anterior portion of the pars lateralis sends fibers to the inferior colliculus and probably to the supperior colliculus, while the posterior portion projects to the inferior colliculus. Acknowledgement The authors are grateful to Mr. H. Hirade for his technical assistance. References 1) Afifi, A. K., Bhauth, N. and Jabbur, S. J. : The nigrotectal tract. An experimental study of its site of origin. Acta anat., 71: 67-77, ) Afifi, A. and Kaelber, W. W.: Efferent connections of the substantia nigra in the cat. Exp. Neurol., 11: , ) Faull, R. L. M. and Mehler, W. R.: The cells of origin of nigrotectal, nigrothalamic and nigrostriatal projections in the rat. Neuroscience, 3: , ) Gillilan, L. A.: The nuclear pattern of the non-tectal portions of the midbrain and isthmus in rodents. J. comp. Neurol., 79 : , ) Graham, R. C., Jr. and Karnovsky, M. J. : The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney : ultrastructual cytochemistry by a new technique. J. Histochem. Cytochem., 14 : , ) Graybiel, A. M.: Organization of the nigrotectal connection : an experimental tracer study in the cat. Brain Res., 143: , ) Grofova, I., Ottersen, 0. P. and Rinvik, E.: Mesencephalic and diencephalic afferents to the superior colliculus and periaqueductal gray substance demonstrated by retrograde axonal transport of horseradish peroxidase in the cat. Brain Res., 146: , ) Hanaway, J., McConnel, J. A. and Netsky, M. G.: Cytoarchitecture of the substantia nigra in the rat. Amer. J. Anat., 129: , ) Hopkins, D. A. and Niessen, L. W.: Substantia nigra projections to the reticular formation, superior colliculus and central gray in the rat, cat and monkey. Neurosci. Lett., 2: , ) Jayaraman, A., Batton, R. R., III, and Carpenter, M. B.: Nigrotectal projections in the monkey an autoradiographic study. Brain Res., 135: , ) Kanig, J. F. R. and Klippel, R. A.: The rat brain. A stereotaxic atlas of the forebrain and lower part of the brain stem. Williams and Wilkins, Baltimore, ) Nauta, H. J. W., Fritz, M. B. and Lasek, R. J. : Afferents to the rat caudoputamen studied with horseradish peroxidase. An evaluation of a retrograde neuroanatomical research method. Brain Res., 67: , ) Rinvik, E., Grofova, I. and Ottersen, 0. P.: Demonstration of nigrotectal and nigroreticular projections in the rat by axonal transport of proteins. Brain Res., 112: , ) Rioch, D. McK. : Studies on the diencephalon of carnivora. Part II. Certain nuclear configurations and fiber connections of the subthalamus and midbrain of the dog and cat. J. comp. Neurol., 49: , ) Watanabe, K. and Kawana, E.: Efferent projections of the parabigeminal nucleus in rats : A horseradish peroxidase (HRP) study. Brain Res., 168: 1-11, 1979.
6 294 K. Watanabe and E. Kawana Explanation Plate of Figures I i Fig. 3. Photographs showing the injection site. A, HRP into the inferior colliculus in R145, B, HRP injection into the superior colliculus in R101. Fig. 4. Photomicrographs of labeled cells in the pars lateralis of the substantia nigra. A and B, HRP-marked neurons in the posterior portion of the pars lateralis after HRP injection into the inferior colliculus ; C and D, HRP-marked neurons in the anterior portion of the pars lateralis after HRP injection into the inferior colliculus. Bars, 20 pm.
7 295 Plate I K. Watanabe and E. Kawana
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