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Projection from the pretectal nuclei to the dorsal lateral geniculate nucleus in the cat: a wheat germ agglutinin-horseradish peroxidase study
Brain Research, 421 (1987) 30-40
30
Elsevier BRE 12862
Projection from the pretectal nuclei to the dorsal lateral geniculate nucleus in the cat: a wheat germ agglutinin-horseradish peroxidase study Toshiaki Kubota 1, Masatoshi Morimoto 1, Takeshi Kanaseki I and Hajime Inomata 2 1Third Department of Anatomy and 2Ophthalmology, Facultyof Medicine, Kyushu University, Fukuoka (Japan) (Accepted 10 February 1987)
Key words: Pretectum; Dorsal lateral geniculate nucleus; Retina; Retinotopic map; Cat; Wheat germ agglutinin-horseradish peroxidase (WGA-HRP)
To study the projection from the pretectum to the dorsal lateral geniculate nucleus (LGNd) in the cat, we used anterograde and retrograde transport of wheat germ agglutinin-horseradish peroxidase (WGA-HRP). Special attention was directed to the retinotopic maps of the pretectum and LGNd. Multiple restricted injections were made into different parts of the pretectum or LGNd. The pretectogeniculate pathway terminates mostly in the medial interlaminair nucleus (MIN) and layers A and A1, and to some extent in the lamina C within the ipsilateral LGNd. The lateral part of the nucleus of the optic tract (NTO) receives afferents from the superior retina, and the medial part of NTO and posterior pretectal nucleus (NPP) receives afferents from the inferior retina. There is no topographic organization in the retinal projection to the olivary pretectal nucleus (NOL). The lateral part of NTO projects ipsilaterally to the rostral portion of LGNd, which receives afferents from the superior retina. The medial part of NTO projects ipsilateraUy to the caudal portion of LGNd, which receives afferents from the inferior retina. The NOL projects to all laminar parts of LGNd, ipsilaterally. The NPP projects largely to the ipsilateral MIN, which receives afferents from the pericentral and peripheral retina. These results suggest that similar parts of the retinotopic maps present in the pretectum and LGNd are connected.
INTRODUCTION Ganglion cells of the retina project directly to the dorsal lateral geniculate nucleus (LGNd), pretectum and superior colliculus 2'6'12'17'19'20-22'30-32'34'37. The L G N d is a relay nucleus in the geniculate visual system, while pretectum and superior colliculus are relay nuclei in the extrageniculate visual system 9. L G N d receives fibers from the pretectum 3'1°'13'16' 18,23.25,36 and superior colliculus 4'7'8'11"12'15'27'
28,33. In the cat, the tectogeniculate pathway originates largely within the stratum griseum superficiale 8'~1 and terminates in the ventral C layers of the L G N d 4,7,12A5,27,28,33. The tectogeniculate pathway connects similar parts of the two retinotopic maps 35. While the pretectogeniculate pathway has been stud-
ied by other investigators 3'1°'13'16'18'23'25'36,the topographic organization of this pathway is not well understood, and there seems to be no documentation on the relation to the retinotopic maps of the pretectum and LGNd. Therefore, the present study was undertaken to determine whether the pretectogeniculate pathway is also retinotopically organized. MATERIALS AND METHODS An amount of 0.01-0.03/~1 of 2.5% wheat germ agglutinin conjugated to horseradish peroxidase ( W G A - H R P ) was injected stereotaxically into 20 adult cats. Injections were placed with a microsyringe or electrophoretically for 15-30 min, using 1-4 /~A of pulsed current (tip diameter of 20-30/~m).
Correspondence: T. Kubota, Third Department of Anatomy, Faculty of Medicine, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka, 812, Japan. 0006-8993/87/$03.50 © 1987 Elsevier Science Publishers B.V. (Biomedical Division)
31 Multiple restricted injections were placed into different parts of the pretectum or LGNd. Nine cats were given injections into the pretectum, and injection into the LGNd was given to 11 cats. Injection sites were restricted to the objective nucleus in all cats. Following a 45 to 50-h postinjection survival period, the cats were deeply anesthetized and perfused through the heart with normal saline, followed by a mixture of 2.5% formalin and 1.25% glutaraldehyde and then 5% sucrose in the phosphate buffer (0.1 M pH 7.4). The brains and eyeballs were removed and the former were placed in a 30% sucrose buffer solution (0.1 M phosphate buffer at pH 7.4). The whole retinae were reacted immediately after the perfusion. For the labeling of ganglion cells in whole mounts of the retina, the eyeballs were cut at the level of the ora serrata, and the vitreous body was removed from the eyecup, before immersion into the buffer. After soaking in the cold buffer, the eyecup with the choroid and the sclera was placed in incubation medium, according to Mesulam 5'24. The retinae and pigment layers were then separated from the remainder of the eyeball by cutting away the sclera and peeling off the choroid. The retina was mounted on a gelatinized slide with the pigment layer facing the slide, and then counterstained with Neutral red. The brains were sectioned in the frontal plane at 50/~m on a freezing microtome. The sections were also reacted 5'24 and counterstained with Neutral red. The preparations were examined microscopically under bright- and darkfield illumination. RESULTS
Pretectal cell groups which project to the LGNd (retrograde studies) To examine the localization of cells of origin in the pretectogeniculate pathway, W G A - H R P was injected into different parts of the LGNd. The site of injection did not include other nuclei such as the pulvinar or ventral lateral geniculate nucleus (LGNv). Figs. 1 (case D2), 2 (case D7), 3 (case D1), 4 (case D4) show illustrations of the injection site and serial coronal sections of the mesencephalon in which the pretectum appears. Case D2 (Figs. 1 and 5A): W G A - H R P was injected into the middle part of the rostrocaudal area of the LGNd on the left side, and the injection site did
not include the medial interlaminar nucleus (MIN) (Fig. 5A). Labeled cells were found in the olivary pretectal nucleus (NOL), nucleus of the optic tract (NTO) and posterior pretectal nucleus (NPP), bilaterally. Labeled cells were absent in the medial pretectal nucleus (NPM) and anterior pretectal nucleus (NPA), bilaterally. Labeled cells were numerous in the ipslateral NOL and NTO, and a few in the bilateral NPP, and in the contralateral NOL and NTO. In the ipsilateral NTO, labeled cells were rich in the middle part of the mediolateral area from the rostral to the caudal level. There was no topographic localization in the bilateral NOL, NPP and contralateral NTO. Case D7 (Figs. 2 and 5B): W G A - H R P was injected into the rostral part of the LGNd on the left side (Fig. 5B). Labeled cells were found in the ipsilateral NOL and bilateral NTO. Labeled cells were absent in the NPP, NPM and NPA, bilaterally, and in the NOL contralaterally. Labeled cells were numerous in the ipsilateral N O L and NTO, and a few in the contralateral NTO. In the ipsilateral NTO, labeled cells were rich in the lateral part from the rostral to the caudal level. There was no topographic localization in the ipsilateral NOL and contralateral NTO. Case D1 (Figs. 3 and 5C): W G A - H R P was injected into the caudal part of the LGNd on the left side. The injection site did not include the MIN (Fig. 5C). Labeled cells were found in the bilateral NOL and NTO, and in the ipsilateral NPP. Labeled cells were absent in the NPM and NPA, bilaterally, and in the NPP contralaterally. Labeled cells were numerous in the ipsilateral N O L and NTO, and a few in the contralateral NOL and NTO, and in the ipsilateral NPP. In the ipsilateral NTO, labeled cells were rich in the medial part from the rostral to the caudal level. There was no topographic localization in the bilateral NOL, contralateral NTO and ipsilateral NPP. Case D4 (Figs. 4 and 5D): W G A - H R P was injected into the MIN and the medial part of laminar lateral geniculate nucleus (Fig. 5D). Labeled cells were present in the bilateral NOL and NTO, and in the ipsilateral NPP. Labeled cells were absent in the NPM and NPA, bilaterally and in the NPP contralaterally. There were a large number of labeled cells in the ipsilateral NTO and NPP, and a small number in the bilateral NOL and contralateral NTO. In the ipsi-
32
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Figs. 1-4. Chartings illustrating the injection site and the serial coronal sections of the mesencephalon in which the pretectum appears. Dots indicate the labeled cells. The distance between each section is about 300 lxm. 3N, oculomotor nucleus; SN, substantia nigra; MGN, medial geniculate nucleus; R, red nucleus. Fig. 1 (case D2) shows a mapping of the bilateral pretectum. Fig. 2 (case D7), Fig. 3 (case D1) and Fig. 4 (case D4) show the mappings of the ipsilateral pretectum.
34
Fig. 5. Bright-field photographs illustrating the center of the injection site in cases D2 (A), D7(B), D1 (C) and D4 (D). Bar =- 1 mm. LGNd, dorsal lateral geniculate nucleus; LGNv, ventral lateral geniculate nucleus; Pul, pulvinar; MIN, medial interlaminar nucleus.
lateral NTO, labeled cells were rich in the middle part of the mediolateral area. In the ipsilateral NPP, labeled cells were present in the medial area. There was no topographic localization in the bilateral NOL and contralateral NTO.
Retinotopic maps of the LGNd and pretectum Retinogeniculate pathway. Fig. 6 shows the localization of labeled cells in the retina (cases D2, D7, D1 and D4). Labeled retinal ganglion cells were distributed along the midline, following injection of W G A - H R P into the middle part of the rostrocaudal area of the LGNd (case D2, Figs. 5A and 6A), in the upper quadrant, following injection of W G A - H R P into the rostral part of the LGNd (case D7, Figs. 5B and 6B), in the lower quadrant, following injection of W G A - H R P into the caudal part of the LGNd (case D1, Figs. 5C and 6C). When W G A - H R P was in-
jected into the MIN and the medial part of laminar lateral geniculate nucleus (case D4, Fig. 5D), numerous labeled cells were found to be distributed in the area centralis and pericentrai region, as well as a few in the peripheral region, of the ipsilateral temporal, contralateral nasal and contralateral temporal retina (Fig. 6D). Fig. 7 summarizes the findings when W G A - H R P was injected into different parts of the LGNd. Retinopretectal pathway. The retinal distribution of labeled cells depended on the site of injection, as shown in Fig. 8. Fig. 8A shows the findings when W G A - H R P was injected into the medial part of NTO and NPP (case PT4). In the contralateral eye, numerous labeled cells were distributed in the inferonasal quadrant, with a few in the temporal retina. In the ipsilateral eye, labeled cells were distributed in the inferotemporal quadrant. Fig. 8B shows the find-
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Fig. 6. Chartings showing the distribution of the labeled retinal ganglion cells in cases of W G A - H R P injected into different parts of the LGNd. A: case D2, B: case D7, C: case D1 and D: case D4. Dots indicate the labeled cells. Closed circle is a disc. V, vertical meridian; H, horizontal meridian. PT
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Fig. 7. Schematic illustrations showing the topographic organization in the retinogeniculate and pretectogeniculate pathways. Symbols indicate topographic distribution of retinal and pretectal labeled cells, following injection of W G A - H R P into the corresponding part of the LGNd.
36
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Fig. 8. The injection sites and the distribution of the retinal labeled cells after injections of WGA-HRP into the pretectum. The distance of the serial coronal sectionsis about 150/~m. A (case PT4): injection into the medial part of NTO and NPP. Retinal labeled cells are distributed in the inferior retina, bilaterally. B (case PT9): injection into the lateral part of NTO. Retinal labeled cells are distributed in the superior retina, bilaterally. C (case PT6): injection into the NOL. Retinal labeled cells are distributed throughout the homonymoushalf of the retina, bilaterally. Closed circle is a disc. V, vertical meridian; H, horizontal meridian.
ings when W G A - H R P was injected into the lateral part of NTO and the dorsal part of NPP (case PT9, Fig. 9A). In the contralateral eye, numerous labeled cells were distributed in the superonasal quadrant, as well as several in the temporal retina. In the ipsilateral eye, labeled cells were distributed in the superotemporal quadrant. Fig. 8C shows the findings when W G A - H R P was injected into the rostral region of the pretectum, NOL and the rostral part of NTO and NPP (case PT6). In the contralateral eye, numerous labeled cells were distributed throughout the nasal retina, as well as a few in the temporal retina. In the ipsilateral eye, labeled cells were distributed throughout the temporal retina.
Anterograde studies of the pretectal projection to the LGNd Figs. 9B and 10 illustrate a case in which the most dense labeling was seen in the LGNd when W G A HRP was injected into the pretectum. W G A - H R P was injected into the NTO and NPP (Fig. 9B). As shown Fig. 10, labeled terminals were densely dis-
tributed in the MIN and layers A and A 1, and to a fair extent in lamina C within the ipsilateral LGNd. Labeled terminals were few at laminae C1-C 3 within the ipsilateral LGNd. Sparse labeled terminals were also distributed within the contralateral LGNd. Labeled cells were absent in the LGNd, bilaterally. DISCUSSION
The main findings in our study are (1) a topographic organization in the pretectogeniculate pathway, (2) retinotopic maps in the LGNd and pretectum, (3) pattern of termination of the pretectogeniculate pathway. These findings are important to better understand the complete picture of the pretectogeniculate pathway and to determine whether this pathway is retinotopically organized. Following W G A - H R P injections into the LGNd, labeled cells in the pretectum were distributed in the bilateral NOL, NTO and NPP, areas in the cat which receive direct retinal afferents 1,2,14,19,22'32'37. Our study revealed that these 3 nuclei project to the
37
C Fig. 9. Bright-fieldphotographs illustrating the center of the injection site in cases of WGA-HRP injected into the pretectum. Bar = 1 mm. A: injection into the lateral part of the NTO. B: injection into the NTO and NPP. C: schematic diagram of A and B. PAG, periaqueductal grey; MGN, medial geniculate nucleus.
LGNd. The topographic organization in the pretectogeniculate pathway is as follows: the lateral part of the NTO projects to the rostral portion of the LGNd, middle part of the mediolateral area of the NTO to the middle portion of the rostrocaudal extent of the LGNd, medial part of the NTO to the caudal portion of the LGNd. Therefore, the mediolateral axis of the NTO runs along the caudorostral axis of the LGNd. The NOL projects to all laminar parts of the LGNd. It is assumed that the NPP projects largely to the MIN, though the injection site of case D4 included the medial part of laminar LGNd. In the retinogeniculate pathway, the superior retina projects to the rostral portion of the laminar LGNd, and the inferior retina to the caudal portion. In the retinopretectal pathway, the superior retina projects to the lateral part of the NTO, and the infe-
rior retina to the medial part of NTO and NPP. There is no topographic organization in the projection from the retina to the NOL. We conclude that similar parts of the retinotopic maps present in the NTO and laminar LGNd are connected. There seems to be no topographic organization in the projection from the retina to the NOL and from the N O L to the laminar LGNd. The projection from the L G N d to the visual cortex is also retinotopically organized 26. The visual information relayed in the pretectum ascends retinotopically to the visual cortex, via the LGNd. With respect to the cells of origin of the pretectogeniculate pathway, Graybiel and Berson 1° reported that the NTO projected to the ipsilateral LGNd in the cat, and that fibers from the medial part of the NTO terminated in the caudal part of the ipsilateral LGNd and that those from the lateral part termi-
38
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Fig. 10. a: schematic diagram showing the pattern of termination in the ipsilateral L G N d , following injection of W G A - H R P into the pretectum. Bar = 1 ram. b,c: dark-field photographs correspond to the insert rectangle in a. b: the labelings are n u m e r o u s in lamina C and few in laminae C 1 - C 3. Bar = 100pm. c: dense labelings are seen in the MIN, layers A and A 1. Bar = 500/~m.
39 nated in the rostral part of the ipsilateral LGNd. Mackay-Sim et al. 23 and Pasquier and Villar 25 detected the cells of origin of the pretectogeniculate pathway, following injection of H R P into the LGNd of the rat. The former authors observed that the labeled cells were distributed in the ipsilateral N O L and NTO, while the latter stated that the labeled cells were distributed in the pretectum, bilaterally. They did not discuss the nuclear subdivisions. Hughes and Mullikin 16 noted that the labeled cells in the cat were distributed in the bilateral NTO and NPP following H R P injection of the LGNd, and suggested that the NPP contributed to the pretectogeniculate pathway. Our results support their proposals and revealed that NOL, NTO and NPP projected to the LGNd. In addition, our study elucidated the topographic organization of the pretectogeniculate pathway. Retinotopic maps in the pretectum have been investigated using the H R P method. Koontz et al. 2° found that the labeled ganglion cells were confined to the temporal retina in the ipsilateral eye, and throughout the entire mediolateral area of the nasal retina, as well as a few cells in the temporal retina in the contralateral eye, following H R P injections into various portions of the cat pretectum. Labeled cells were distributed in the lower quadrant of the retina following H R P injection into the anteromedial prerectum, and in the upper quadrant of the retina following H R P injection into the posterolateral pretectum. They noted that the ventrodorsal retinal axis ran along the long axis of the pretectum. Our findings are consistent with these results. When we injected W G A - H R P into the rostral pretectum, N O L and the rostral part of NTO and NPP, labeled cells were distributed throughout the homonymous half of the retina and there was no topographic localization.
REFERENCES 1 Avendafio, C. and Juretschke, M.A., The pretectal region of the cat: a structural and topographical study with stereotaxic coordinates, J. Comp. Neurol., 193 (1980) 69-88. 2 Ballas, I., Hoffmann, K.P. and Wagner, H.-J., Retinal projection to the nucleus of the optic tract in the cat as revealed by retrograde transport of horseradish peroxidase, Neurosci. Lett., 26 (1981) 197-202. 3 Berman, N., Connections of the pretectum in the cat, J. Comp. Neurol., 174 (1977) 227-254. 4 Fitzpatrick, D., Carey, R.G. and Diamond, I.T., The pro-
Therefore, there is a topographic organization in the projection from the retina to the NTO and NPP, but no topographic organization from the retina to the NOL. These findings coincide with the topographic organization of the pretectogeniculate pathway. Retinotopic maps in the LGNd have been investigated, using the degeneration method 6'21'32'34. The superior retina projects to the rostral portion of the LGNd, the inferior retina to the caudal portion, the central retina to the medial part of the laminar LGNd, and the peripheral retina to the lateral area. Our findings using W G A - H R P coincide with evidence obtained in the degeneration studies. Rowe and Dreher 29 observed the retinal distribution of labeled ganglion cells after injections of H R P into the MIN. Following injection of H R P into the MIN, labeled ganglion cells were found in the pericentral and peripheral region of ipsilateral temporal, contralateral nasal, or contralateral temporal retina. Our results of W G A - H R P are consistent with those of the H R P study. We found that the pretectogeniculate pathway terminated mostly in the MIN and layers A and A1, and to some extent in the lamina C within the ipsilateral LGNd. According to the autoradiographic findings of Graybiel and Berson 1°, labeled fibers were distributed mainly in the MIN, layers A and A1, and sparsely in lamina C following injection of tritiated amino acid into the ipsilateral NTO in the cat. Our findings support this evidence. The possibility of a retrograde-anterograde transport in the bifurcating retinal Y-axons between the pretectum and LGNd 22 was not ruled out. However, the population of Y-cells which project to the pretectum is so small 2'2°'22, that participation of these cells is probably negligible.
jection of the superior coiliculus upon the lateral geniculate body in Tupaia glis and Galago sanegalensis, Brain Research, 194 (1980) 494-499. 5 Fujii, M. and Kusama, T., Fixation of horseradish peroxidase reaction products with ammonium molybdate, Neurosci. Res., 1 (1984) 153-156. 6 Garey, L.J. and Powell, T.P.S., The projection of the retina in the cat, J. Anat., 102 (1968) 189-222. 7 Graham, J., An autoradiographic study of the efferent connections of the superior colliculus in the cat, J. Comp. Neurol., 173 (1977) 629-654. 8 Graham, J, and Berman, N., Origins of the projections of
40 the superior colliculus to the dorsal lateral gemculate nucleus and the pulvinar in the rabbit, Neurosci. Lett., 26 (1981) 101-106. 9 Graybiel, A.M., Some extrageniculate visual pathways in the cat, Invest. Ophthalrnol., 11 (1972) 322-332. 10 Graybicl, A.M. and Berson, D.M., Autoradiographic evidence for a projection from the pretectal nucleus of the optic tract to the dorsal lateral geniculate complex in the cat, Brain Research, 195 (1980) 1-12. l l Harrell, J.V., Caldwell, R.B. and Mize, R.R., The superior colliculus neurons which project to the dorsal and ventral lateral geniculate nuclei in the cat, Exp. Brain Res., 46 (1982) 234-242. 12 Harting, J.K., Casagrande, V.A. and Weber, J.T., The projection of the primate superior colliculus upon the dorsal lateral geniculate nucleus: autoradiographic demonstration of interlaminar distribution of tectogeniculate axons, Brain Research, 150 (1978) 593-599. 13 Hatting, J.K., Hashikawa, T. and Lieshout, D., Laminar distribution of tectal, parabigeminal and pretectal inputs to the primate dorsal lateral geniculate nucleus: connectional studies in Galago crassicaudatus, Brain Research, 366 (1986) 358-363. 14 Hoffmann, K.-P, Ballas, I. and Wagner, H.-J., Double labelling of retinofugal projections in the cat: a study using anterograde transport of 3H-proline and horseradish peroxidase, Exp. Brain Res., 53 (1984) 420-430. 15 Holstege, G. and Collewijn, H., The efferent connections of the nucleus of the optic tract and the superior colliculus in the rabbit, J. Comp. Neurol., 209 (1982) 139-175. 16 Hughes, H,C. and Mullikin, W.H., Brainstem afferents to the lateral geniculate nucleus of the cat, Exp. Brain Res., 54 (1984) 253-258. 17 Hutchins, B. and Weber, J.T., The pretectal complex of the monkey: a reinvestigation of the morphology and retinal terminations, J. Comp. Neurol., 232 (1985) 425-442. 18 Itoh, K., Efferent projections of the pretectum in the cat, Exp. Brain Res., 30 (1977) 89-105. 19 Kanaseki, T. and Sprague, J.M., Anatomical organization of pretectal nuclei and tectal laminae in the cat, J. Comp. Neurol., 158 (1974) 319-338. 20 Koontz, M.A., Rodieck, R.W. and Farmer, S.G., The retinal projection to the cat pretectum, J. Comp. Neurol., 236 (1985) 42-59. 21 Laties, A.M. and Sprague, J.M., The projection of optic fibers to the visual centers in the cat, J. Cornp. Neurol., 127 (1966) 35-70. 22 Leventhal, A.G., Rodieck, R.W. and Dreher, B., Central projections of cat retinal ganglion cells, J, Comp. Neurol., 237 (1985) 216-226. 23 Mackay-Sim, A., Sefton, A.J. and Martin, P.R., Subcorti-
cal projections to lateral geniculate and thalamic reticular nuclei in the hooded rat, J. Comp. Neurol., 213 (1983) 24-35. 24 Mesulam, M.-M., Principles of horseradish peroxidase neurohistochemistry and their applications for tracing neural pathways-axonal transport, enzyme histochemistry and light microscopic analysis. In M.-M. Mesulam (Ed.), Tracing Neural Connections with Horseradish Peroxidase, Wiley, Chichester, 1982, pp. 1-151, 25 Pasquier, D.A. and Villar, M,J., Subcortical projections to the lateral geniculate body in the rat, Exp. Brain Res., 48 (1982) 409-419. 26 Polyak, S., A contribution to the cerebral representation of the retina, J. Comp. Neurol., 57 (1933) 541-617. 27 Reese, B.E., The projection from the superior colliculus to the dorsal lateral geniculate nucleus in the rat, Brain Research, 305 (1984) 162-168. 28 Robson, J.A. and Hall, W.C., Projections from the superior colliculus to the dorsal lateral genieulate nucleus of the grey squirrel (Sciurus carolinensis), Brain Research, 113 (1976) 379-385. 29 Rowe, M.H. and Dreher, B., Retinal W-cell projections to the medial interlaminar nucleus in the cat: implications for ganglion cell classification, J. Comp. Neurol., 204 (1982) 117-133. 30 Scalia, F., The termination of retinal axons in the pretectal region of mammals, J. Comp. Neurol. 145 (1972) 223-258. 31 Scalia, F. and Arango, V., Topographic organization of the projections of the retina to the pretectal region in the rat, J. Comp. Neurol., 186 (1979) 271-292. 32 Singleton, M.C. and Peele, T.L., Distribution of optic fibers in the cat, J. Comp. Neurol., 125 (1965) 303-328. 33 Stein, B.E., McHaffie, J.G., Harting, J.K., Huerta, M.F. and Hashikawa, T., Transient tectogenieulate projections in neonatal kittens: an autoradiographic study, J. Comp. Neurol., 239 (1985) 402-412. 34 Stone, J. and Hansen, S.M., The projection of the cat's retina on the lateral geniculate nucleus, J. Comp. Neurol., 126 (1966) 601-624. 35 Torrealba, F., Partlow, G.D. and Guillery, R.W., Organization of the projection from the superior colliculus to the dorsal lateral geniculate nucleus of the cat, Neuroscience, 6 (1981) 1341-1360. 36 Weber, J.T. and Harting, J.K., The efferent projections of the pretectal complex: an autoradiographic and horseradish peroxidase analysis, Brain Research, 194 (1980) 1-28. 37 Weber, J.T. and Hutchins, B., The demonstration of a retinal projection to the medial pretectal nucleus in the domestic cat and the squirrel monkey: an autoradiographic analysis, Brain Research, 232 (1982) 181-186.
30
Elsevier BRE 12862
Projection from the pretectal nuclei to the dorsal lateral geniculate nucleus in the cat: a wheat germ agglutinin-horseradish peroxidase study Toshiaki Kubota 1, Masatoshi Morimoto 1, Takeshi Kanaseki I and Hajime Inomata 2 1Third Department of Anatomy and 2Ophthalmology, Facultyof Medicine, Kyushu University, Fukuoka (Japan) (Accepted 10 February 1987)
Key words: Pretectum; Dorsal lateral geniculate nucleus; Retina; Retinotopic map; Cat; Wheat germ agglutinin-horseradish peroxidase (WGA-HRP)
To study the projection from the pretectum to the dorsal lateral geniculate nucleus (LGNd) in the cat, we used anterograde and retrograde transport of wheat germ agglutinin-horseradish peroxidase (WGA-HRP). Special attention was directed to the retinotopic maps of the pretectum and LGNd. Multiple restricted injections were made into different parts of the pretectum or LGNd. The pretectogeniculate pathway terminates mostly in the medial interlaminair nucleus (MIN) and layers A and A1, and to some extent in the lamina C within the ipsilateral LGNd. The lateral part of the nucleus of the optic tract (NTO) receives afferents from the superior retina, and the medial part of NTO and posterior pretectal nucleus (NPP) receives afferents from the inferior retina. There is no topographic organization in the retinal projection to the olivary pretectal nucleus (NOL). The lateral part of NTO projects ipsilaterally to the rostral portion of LGNd, which receives afferents from the superior retina. The medial part of NTO projects ipsilateraUy to the caudal portion of LGNd, which receives afferents from the inferior retina. The NOL projects to all laminar parts of LGNd, ipsilaterally. The NPP projects largely to the ipsilateral MIN, which receives afferents from the pericentral and peripheral retina. These results suggest that similar parts of the retinotopic maps present in the pretectum and LGNd are connected.
INTRODUCTION Ganglion cells of the retina project directly to the dorsal lateral geniculate nucleus (LGNd), pretectum and superior colliculus 2'6'12'17'19'20-22'30-32'34'37. The L G N d is a relay nucleus in the geniculate visual system, while pretectum and superior colliculus are relay nuclei in the extrageniculate visual system 9. L G N d receives fibers from the pretectum 3'1°'13'16' 18,23.25,36 and superior colliculus 4'7'8'11"12'15'27'
28,33. In the cat, the tectogeniculate pathway originates largely within the stratum griseum superficiale 8'~1 and terminates in the ventral C layers of the L G N d 4,7,12A5,27,28,33. The tectogeniculate pathway connects similar parts of the two retinotopic maps 35. While the pretectogeniculate pathway has been stud-
ied by other investigators 3'1°'13'16'18'23'25'36,the topographic organization of this pathway is not well understood, and there seems to be no documentation on the relation to the retinotopic maps of the pretectum and LGNd. Therefore, the present study was undertaken to determine whether the pretectogeniculate pathway is also retinotopically organized. MATERIALS AND METHODS An amount of 0.01-0.03/~1 of 2.5% wheat germ agglutinin conjugated to horseradish peroxidase ( W G A - H R P ) was injected stereotaxically into 20 adult cats. Injections were placed with a microsyringe or electrophoretically for 15-30 min, using 1-4 /~A of pulsed current (tip diameter of 20-30/~m).
Correspondence: T. Kubota, Third Department of Anatomy, Faculty of Medicine, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka, 812, Japan. 0006-8993/87/$03.50 © 1987 Elsevier Science Publishers B.V. (Biomedical Division)
31 Multiple restricted injections were placed into different parts of the pretectum or LGNd. Nine cats were given injections into the pretectum, and injection into the LGNd was given to 11 cats. Injection sites were restricted to the objective nucleus in all cats. Following a 45 to 50-h postinjection survival period, the cats were deeply anesthetized and perfused through the heart with normal saline, followed by a mixture of 2.5% formalin and 1.25% glutaraldehyde and then 5% sucrose in the phosphate buffer (0.1 M pH 7.4). The brains and eyeballs were removed and the former were placed in a 30% sucrose buffer solution (0.1 M phosphate buffer at pH 7.4). The whole retinae were reacted immediately after the perfusion. For the labeling of ganglion cells in whole mounts of the retina, the eyeballs were cut at the level of the ora serrata, and the vitreous body was removed from the eyecup, before immersion into the buffer. After soaking in the cold buffer, the eyecup with the choroid and the sclera was placed in incubation medium, according to Mesulam 5'24. The retinae and pigment layers were then separated from the remainder of the eyeball by cutting away the sclera and peeling off the choroid. The retina was mounted on a gelatinized slide with the pigment layer facing the slide, and then counterstained with Neutral red. The brains were sectioned in the frontal plane at 50/~m on a freezing microtome. The sections were also reacted 5'24 and counterstained with Neutral red. The preparations were examined microscopically under bright- and darkfield illumination. RESULTS
Pretectal cell groups which project to the LGNd (retrograde studies) To examine the localization of cells of origin in the pretectogeniculate pathway, W G A - H R P was injected into different parts of the LGNd. The site of injection did not include other nuclei such as the pulvinar or ventral lateral geniculate nucleus (LGNv). Figs. 1 (case D2), 2 (case D7), 3 (case D1), 4 (case D4) show illustrations of the injection site and serial coronal sections of the mesencephalon in which the pretectum appears. Case D2 (Figs. 1 and 5A): W G A - H R P was injected into the middle part of the rostrocaudal area of the LGNd on the left side, and the injection site did
not include the medial interlaminar nucleus (MIN) (Fig. 5A). Labeled cells were found in the olivary pretectal nucleus (NOL), nucleus of the optic tract (NTO) and posterior pretectal nucleus (NPP), bilaterally. Labeled cells were absent in the medial pretectal nucleus (NPM) and anterior pretectal nucleus (NPA), bilaterally. Labeled cells were numerous in the ipslateral NOL and NTO, and a few in the bilateral NPP, and in the contralateral NOL and NTO. In the ipsilateral NTO, labeled cells were rich in the middle part of the mediolateral area from the rostral to the caudal level. There was no topographic localization in the bilateral NOL, NPP and contralateral NTO. Case D7 (Figs. 2 and 5B): W G A - H R P was injected into the rostral part of the LGNd on the left side (Fig. 5B). Labeled cells were found in the ipsilateral NOL and bilateral NTO. Labeled cells were absent in the NPP, NPM and NPA, bilaterally, and in the NOL contralaterally. Labeled cells were numerous in the ipsilateral N O L and NTO, and a few in the contralateral NTO. In the ipsilateral NTO, labeled cells were rich in the lateral part from the rostral to the caudal level. There was no topographic localization in the ipsilateral NOL and contralateral NTO. Case D1 (Figs. 3 and 5C): W G A - H R P was injected into the caudal part of the LGNd on the left side. The injection site did not include the MIN (Fig. 5C). Labeled cells were found in the bilateral NOL and NTO, and in the ipsilateral NPP. Labeled cells were absent in the NPM and NPA, bilaterally, and in the NPP contralaterally. Labeled cells were numerous in the ipsilateral N O L and NTO, and a few in the contralateral NOL and NTO, and in the ipsilateral NPP. In the ipsilateral NTO, labeled cells were rich in the medial part from the rostral to the caudal level. There was no topographic localization in the bilateral NOL, contralateral NTO and ipsilateral NPP. Case D4 (Figs. 4 and 5D): W G A - H R P was injected into the MIN and the medial part of laminar lateral geniculate nucleus (Fig. 5D). Labeled cells were present in the bilateral NOL and NTO, and in the ipsilateral NPP. Labeled cells were absent in the NPM and NPA, bilaterally and in the NPP contralaterally. There were a large number of labeled cells in the ipsilateral NTO and NPP, and a small number in the bilateral NOL and contralateral NTO. In the ipsi-
32
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Figs. 1-4. Chartings illustrating the injection site and the serial coronal sections of the mesencephalon in which the pretectum appears. Dots indicate the labeled cells. The distance between each section is about 300 lxm. 3N, oculomotor nucleus; SN, substantia nigra; MGN, medial geniculate nucleus; R, red nucleus. Fig. 1 (case D2) shows a mapping of the bilateral pretectum. Fig. 2 (case D7), Fig. 3 (case D1) and Fig. 4 (case D4) show the mappings of the ipsilateral pretectum.
34
Fig. 5. Bright-field photographs illustrating the center of the injection site in cases D2 (A), D7(B), D1 (C) and D4 (D). Bar =- 1 mm. LGNd, dorsal lateral geniculate nucleus; LGNv, ventral lateral geniculate nucleus; Pul, pulvinar; MIN, medial interlaminar nucleus.
lateral NTO, labeled cells were rich in the middle part of the mediolateral area. In the ipsilateral NPP, labeled cells were present in the medial area. There was no topographic localization in the bilateral NOL and contralateral NTO.
Retinotopic maps of the LGNd and pretectum Retinogeniculate pathway. Fig. 6 shows the localization of labeled cells in the retina (cases D2, D7, D1 and D4). Labeled retinal ganglion cells were distributed along the midline, following injection of W G A - H R P into the middle part of the rostrocaudal area of the LGNd (case D2, Figs. 5A and 6A), in the upper quadrant, following injection of W G A - H R P into the rostral part of the LGNd (case D7, Figs. 5B and 6B), in the lower quadrant, following injection of W G A - H R P into the caudal part of the LGNd (case D1, Figs. 5C and 6C). When W G A - H R P was in-
jected into the MIN and the medial part of laminar lateral geniculate nucleus (case D4, Fig. 5D), numerous labeled cells were found to be distributed in the area centralis and pericentrai region, as well as a few in the peripheral region, of the ipsilateral temporal, contralateral nasal and contralateral temporal retina (Fig. 6D). Fig. 7 summarizes the findings when W G A - H R P was injected into different parts of the LGNd. Retinopretectal pathway. The retinal distribution of labeled cells depended on the site of injection, as shown in Fig. 8. Fig. 8A shows the findings when W G A - H R P was injected into the medial part of NTO and NPP (case PT4). In the contralateral eye, numerous labeled cells were distributed in the inferonasal quadrant, with a few in the temporal retina. In the ipsilateral eye, labeled cells were distributed in the inferotemporal quadrant. Fig. 8B shows the find-
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Fig. 7. Schematic illustrations showing the topographic organization in the retinogeniculate and pretectogeniculate pathways. Symbols indicate topographic distribution of retinal and pretectal labeled cells, following injection of W G A - H R P into the corresponding part of the LGNd.
36
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Fig. 8. The injection sites and the distribution of the retinal labeled cells after injections of WGA-HRP into the pretectum. The distance of the serial coronal sectionsis about 150/~m. A (case PT4): injection into the medial part of NTO and NPP. Retinal labeled cells are distributed in the inferior retina, bilaterally. B (case PT9): injection into the lateral part of NTO. Retinal labeled cells are distributed in the superior retina, bilaterally. C (case PT6): injection into the NOL. Retinal labeled cells are distributed throughout the homonymoushalf of the retina, bilaterally. Closed circle is a disc. V, vertical meridian; H, horizontal meridian.
ings when W G A - H R P was injected into the lateral part of NTO and the dorsal part of NPP (case PT9, Fig. 9A). In the contralateral eye, numerous labeled cells were distributed in the superonasal quadrant, as well as several in the temporal retina. In the ipsilateral eye, labeled cells were distributed in the superotemporal quadrant. Fig. 8C shows the findings when W G A - H R P was injected into the rostral region of the pretectum, NOL and the rostral part of NTO and NPP (case PT6). In the contralateral eye, numerous labeled cells were distributed throughout the nasal retina, as well as a few in the temporal retina. In the ipsilateral eye, labeled cells were distributed throughout the temporal retina.
Anterograde studies of the pretectal projection to the LGNd Figs. 9B and 10 illustrate a case in which the most dense labeling was seen in the LGNd when W G A HRP was injected into the pretectum. W G A - H R P was injected into the NTO and NPP (Fig. 9B). As shown Fig. 10, labeled terminals were densely dis-
tributed in the MIN and layers A and A 1, and to a fair extent in lamina C within the ipsilateral LGNd. Labeled terminals were few at laminae C1-C 3 within the ipsilateral LGNd. Sparse labeled terminals were also distributed within the contralateral LGNd. Labeled cells were absent in the LGNd, bilaterally. DISCUSSION
The main findings in our study are (1) a topographic organization in the pretectogeniculate pathway, (2) retinotopic maps in the LGNd and pretectum, (3) pattern of termination of the pretectogeniculate pathway. These findings are important to better understand the complete picture of the pretectogeniculate pathway and to determine whether this pathway is retinotopically organized. Following W G A - H R P injections into the LGNd, labeled cells in the pretectum were distributed in the bilateral NOL, NTO and NPP, areas in the cat which receive direct retinal afferents 1,2,14,19,22'32'37. Our study revealed that these 3 nuclei project to the
37
C Fig. 9. Bright-fieldphotographs illustrating the center of the injection site in cases of WGA-HRP injected into the pretectum. Bar = 1 mm. A: injection into the lateral part of the NTO. B: injection into the NTO and NPP. C: schematic diagram of A and B. PAG, periaqueductal grey; MGN, medial geniculate nucleus.
LGNd. The topographic organization in the pretectogeniculate pathway is as follows: the lateral part of the NTO projects to the rostral portion of the LGNd, middle part of the mediolateral area of the NTO to the middle portion of the rostrocaudal extent of the LGNd, medial part of the NTO to the caudal portion of the LGNd. Therefore, the mediolateral axis of the NTO runs along the caudorostral axis of the LGNd. The NOL projects to all laminar parts of the LGNd. It is assumed that the NPP projects largely to the MIN, though the injection site of case D4 included the medial part of laminar LGNd. In the retinogeniculate pathway, the superior retina projects to the rostral portion of the laminar LGNd, and the inferior retina to the caudal portion. In the retinopretectal pathway, the superior retina projects to the lateral part of the NTO, and the infe-
rior retina to the medial part of NTO and NPP. There is no topographic organization in the projection from the retina to the NOL. We conclude that similar parts of the retinotopic maps present in the NTO and laminar LGNd are connected. There seems to be no topographic organization in the projection from the retina to the NOL and from the N O L to the laminar LGNd. The projection from the L G N d to the visual cortex is also retinotopically organized 26. The visual information relayed in the pretectum ascends retinotopically to the visual cortex, via the LGNd. With respect to the cells of origin of the pretectogeniculate pathway, Graybiel and Berson 1° reported that the NTO projected to the ipsilateral LGNd in the cat, and that fibers from the medial part of the NTO terminated in the caudal part of the ipsilateral LGNd and that those from the lateral part termi-
38
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Fig. 10. a: schematic diagram showing the pattern of termination in the ipsilateral L G N d , following injection of W G A - H R P into the pretectum. Bar = 1 ram. b,c: dark-field photographs correspond to the insert rectangle in a. b: the labelings are n u m e r o u s in lamina C and few in laminae C 1 - C 3. Bar = 100pm. c: dense labelings are seen in the MIN, layers A and A 1. Bar = 500/~m.
39 nated in the rostral part of the ipsilateral LGNd. Mackay-Sim et al. 23 and Pasquier and Villar 25 detected the cells of origin of the pretectogeniculate pathway, following injection of H R P into the LGNd of the rat. The former authors observed that the labeled cells were distributed in the ipsilateral N O L and NTO, while the latter stated that the labeled cells were distributed in the pretectum, bilaterally. They did not discuss the nuclear subdivisions. Hughes and Mullikin 16 noted that the labeled cells in the cat were distributed in the bilateral NTO and NPP following H R P injection of the LGNd, and suggested that the NPP contributed to the pretectogeniculate pathway. Our results support their proposals and revealed that NOL, NTO and NPP projected to the LGNd. In addition, our study elucidated the topographic organization of the pretectogeniculate pathway. Retinotopic maps in the pretectum have been investigated using the H R P method. Koontz et al. 2° found that the labeled ganglion cells were confined to the temporal retina in the ipsilateral eye, and throughout the entire mediolateral area of the nasal retina, as well as a few cells in the temporal retina in the contralateral eye, following H R P injections into various portions of the cat pretectum. Labeled cells were distributed in the lower quadrant of the retina following H R P injection into the anteromedial prerectum, and in the upper quadrant of the retina following H R P injection into the posterolateral pretectum. They noted that the ventrodorsal retinal axis ran along the long axis of the pretectum. Our findings are consistent with these results. When we injected W G A - H R P into the rostral pretectum, N O L and the rostral part of NTO and NPP, labeled cells were distributed throughout the homonymous half of the retina and there was no topographic localization.
REFERENCES 1 Avendafio, C. and Juretschke, M.A., The pretectal region of the cat: a structural and topographical study with stereotaxic coordinates, J. Comp. Neurol., 193 (1980) 69-88. 2 Ballas, I., Hoffmann, K.P. and Wagner, H.-J., Retinal projection to the nucleus of the optic tract in the cat as revealed by retrograde transport of horseradish peroxidase, Neurosci. Lett., 26 (1981) 197-202. 3 Berman, N., Connections of the pretectum in the cat, J. Comp. Neurol., 174 (1977) 227-254. 4 Fitzpatrick, D., Carey, R.G. and Diamond, I.T., The pro-
Therefore, there is a topographic organization in the projection from the retina to the NTO and NPP, but no topographic organization from the retina to the NOL. These findings coincide with the topographic organization of the pretectogeniculate pathway. Retinotopic maps in the LGNd have been investigated, using the degeneration method 6'21'32'34. The superior retina projects to the rostral portion of the LGNd, the inferior retina to the caudal portion, the central retina to the medial part of the laminar LGNd, and the peripheral retina to the lateral area. Our findings using W G A - H R P coincide with evidence obtained in the degeneration studies. Rowe and Dreher 29 observed the retinal distribution of labeled ganglion cells after injections of H R P into the MIN. Following injection of H R P into the MIN, labeled ganglion cells were found in the pericentral and peripheral region of ipsilateral temporal, contralateral nasal, or contralateral temporal retina. Our results of W G A - H R P are consistent with those of the H R P study. We found that the pretectogeniculate pathway terminated mostly in the MIN and layers A and A1, and to some extent in the lamina C within the ipsilateral LGNd. According to the autoradiographic findings of Graybiel and Berson 1°, labeled fibers were distributed mainly in the MIN, layers A and A1, and sparsely in lamina C following injection of tritiated amino acid into the ipsilateral NTO in the cat. Our findings support this evidence. The possibility of a retrograde-anterograde transport in the bifurcating retinal Y-axons between the pretectum and LGNd 22 was not ruled out. However, the population of Y-cells which project to the pretectum is so small 2'2°'22, that participation of these cells is probably negligible.
jection of the superior coiliculus upon the lateral geniculate body in Tupaia glis and Galago sanegalensis, Brain Research, 194 (1980) 494-499. 5 Fujii, M. and Kusama, T., Fixation of horseradish peroxidase reaction products with ammonium molybdate, Neurosci. Res., 1 (1984) 153-156. 6 Garey, L.J. and Powell, T.P.S., The projection of the retina in the cat, J. Anat., 102 (1968) 189-222. 7 Graham, J., An autoradiographic study of the efferent connections of the superior colliculus in the cat, J. Comp. Neurol., 173 (1977) 629-654. 8 Graham, J, and Berman, N., Origins of the projections of
40 the superior colliculus to the dorsal lateral gemculate nucleus and the pulvinar in the rabbit, Neurosci. Lett., 26 (1981) 101-106. 9 Graybiel, A.M., Some extrageniculate visual pathways in the cat, Invest. Ophthalrnol., 11 (1972) 322-332. 10 Graybicl, A.M. and Berson, D.M., Autoradiographic evidence for a projection from the pretectal nucleus of the optic tract to the dorsal lateral geniculate complex in the cat, Brain Research, 195 (1980) 1-12. l l Harrell, J.V., Caldwell, R.B. and Mize, R.R., The superior colliculus neurons which project to the dorsal and ventral lateral geniculate nuclei in the cat, Exp. Brain Res., 46 (1982) 234-242. 12 Harting, J.K., Casagrande, V.A. and Weber, J.T., The projection of the primate superior colliculus upon the dorsal lateral geniculate nucleus: autoradiographic demonstration of interlaminar distribution of tectogeniculate axons, Brain Research, 150 (1978) 593-599. 13 Hatting, J.K., Hashikawa, T. and Lieshout, D., Laminar distribution of tectal, parabigeminal and pretectal inputs to the primate dorsal lateral geniculate nucleus: connectional studies in Galago crassicaudatus, Brain Research, 366 (1986) 358-363. 14 Hoffmann, K.-P, Ballas, I. and Wagner, H.-J., Double labelling of retinofugal projections in the cat: a study using anterograde transport of 3H-proline and horseradish peroxidase, Exp. Brain Res., 53 (1984) 420-430. 15 Holstege, G. and Collewijn, H., The efferent connections of the nucleus of the optic tract and the superior colliculus in the rabbit, J. Comp. Neurol., 209 (1982) 139-175. 16 Hughes, H,C. and Mullikin, W.H., Brainstem afferents to the lateral geniculate nucleus of the cat, Exp. Brain Res., 54 (1984) 253-258. 17 Hutchins, B. and Weber, J.T., The pretectal complex of the monkey: a reinvestigation of the morphology and retinal terminations, J. Comp. Neurol., 232 (1985) 425-442. 18 Itoh, K., Efferent projections of the pretectum in the cat, Exp. Brain Res., 30 (1977) 89-105. 19 Kanaseki, T. and Sprague, J.M., Anatomical organization of pretectal nuclei and tectal laminae in the cat, J. Comp. Neurol., 158 (1974) 319-338. 20 Koontz, M.A., Rodieck, R.W. and Farmer, S.G., The retinal projection to the cat pretectum, J. Comp. Neurol., 236 (1985) 42-59. 21 Laties, A.M. and Sprague, J.M., The projection of optic fibers to the visual centers in the cat, J. Cornp. Neurol., 127 (1966) 35-70. 22 Leventhal, A.G., Rodieck, R.W. and Dreher, B., Central projections of cat retinal ganglion cells, J, Comp. Neurol., 237 (1985) 216-226. 23 Mackay-Sim, A., Sefton, A.J. and Martin, P.R., Subcorti-
cal projections to lateral geniculate and thalamic reticular nuclei in the hooded rat, J. Comp. Neurol., 213 (1983) 24-35. 24 Mesulam, M.-M., Principles of horseradish peroxidase neurohistochemistry and their applications for tracing neural pathways-axonal transport, enzyme histochemistry and light microscopic analysis. In M.-M. Mesulam (Ed.), Tracing Neural Connections with Horseradish Peroxidase, Wiley, Chichester, 1982, pp. 1-151, 25 Pasquier, D.A. and Villar, M,J., Subcortical projections to the lateral geniculate body in the rat, Exp. Brain Res., 48 (1982) 409-419. 26 Polyak, S., A contribution to the cerebral representation of the retina, J. Comp. Neurol., 57 (1933) 541-617. 27 Reese, B.E., The projection from the superior colliculus to the dorsal lateral geniculate nucleus in the rat, Brain Research, 305 (1984) 162-168. 28 Robson, J.A. and Hall, W.C., Projections from the superior colliculus to the dorsal lateral genieulate nucleus of the grey squirrel (Sciurus carolinensis), Brain Research, 113 (1976) 379-385. 29 Rowe, M.H. and Dreher, B., Retinal W-cell projections to the medial interlaminar nucleus in the cat: implications for ganglion cell classification, J. Comp. Neurol., 204 (1982) 117-133. 30 Scalia, F., The termination of retinal axons in the pretectal region of mammals, J. Comp. Neurol. 145 (1972) 223-258. 31 Scalia, F. and Arango, V., Topographic organization of the projections of the retina to the pretectal region in the rat, J. Comp. Neurol., 186 (1979) 271-292. 32 Singleton, M.C. and Peele, T.L., Distribution of optic fibers in the cat, J. Comp. Neurol., 125 (1965) 303-328. 33 Stein, B.E., McHaffie, J.G., Harting, J.K., Huerta, M.F. and Hashikawa, T., Transient tectogenieulate projections in neonatal kittens: an autoradiographic study, J. Comp. Neurol., 239 (1985) 402-412. 34 Stone, J. and Hansen, S.M., The projection of the cat's retina on the lateral geniculate nucleus, J. Comp. Neurol., 126 (1966) 601-624. 35 Torrealba, F., Partlow, G.D. and Guillery, R.W., Organization of the projection from the superior colliculus to the dorsal lateral geniculate nucleus of the cat, Neuroscience, 6 (1981) 1341-1360. 36 Weber, J.T. and Harting, J.K., The efferent projections of the pretectal complex: an autoradiographic and horseradish peroxidase analysis, Brain Research, 194 (1980) 1-28. 37 Weber, J.T. and Hutchins, B., The demonstration of a retinal projection to the medial pretectal nucleus in the domestic cat and the squirrel monkey: an autoradiographic analysis, Brain Research, 232 (1982) 181-186.