Brain Research, 100 (1975) 125-131 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands

The retino-thalamo-hyperstriatal pathway in the pigeon

125

(Columbo livio)

D O M MICELI, J E A N I N E P E Y R I C H O U X AND JACQUES REPI~RANT Laboratoire de Psychophysiologie Sensorielle, Universitd Paris VI, 4 place Jussieu, 75005 Paris, Laboratoire de Nearomorphologie, I.N.S.E.R.M. U-106, Hdpital de Port Royal, 75014 Paris and Laboratoire d'Anatomie Comparde, M.N.H.N., 75005 Paris (France) (Accepted August 26th, 1975)

Previous anatomical9,1a, 22 and physiological 1~ investigations have demonstrated the existence of a retino-thalamo-hyperstriatal pathway in different species of birds (Columba livia, Speotyto eanieularia, Gallus domesticus). However, divergent views have emerged concerning the exact location of the thalamic relay, the component nuclei giving rise to crossed and uncrossed projectionsS,13, 22, and the topographical distribution of these projections in the hyperstriatumS, 9. The present study was undertaken to clarify retino-thalamo-hyperstriatal interrelationships using (1) selective silver staining of degenerating fibres (Fink-Heimer) and autoradiographic methods for the identification of thalamic regions receiving retinal input and (2) a method based on the retrograde intraaxonal transport of horseradish peroxidase (HRP) 11 for the labelling of cell bodies in the thalamus following injection of the enzyme into regions of the hyperstriatum believed to subserve a visual function 9,1a,15,17,18,23. Unilateral eye enucleations were performed on adult pigeons. Following survival periods ranging from 3 to 12 days, the animals were perfused with l0 ~ formol-saline. The brains were sectioned at 20 #m and the sections processed according to the FinkHeimer method 3. Other animals were given unilateral intraocular injections of 100 /~Ci [3H]proline. Twenty-four hours to 10 days after injection the animals were perfused with l0 ~ formol-saline. The brains were embedded in paraffin wax, sectioned at 15 #m, and processed as described by Cowan et al. 1. Fifteen pigeons received unilateral hyperstriatal injections of either 0.3 #1 HRP (Sigma type V|) diluted in saline to 25 or 0.1 /A HRP diluted to 50~. HRP was injected at the rate of 0.3 #l/h. The injections were performed stereotaxically along the rostral-caudal axis of the Wulst between A 10.0 mm and A 12.5 mms and 2 mm from the midline. 0.3 #1 injections were made at a depth of 1 mm and 0.1 #! injections at 1 mm and 2-2.5 mm. Fortyeight hours after HRP injection the birds were perfused with 25 ~ Karnovsky solution 6. Brain sections of 40 #m were obtained, processed according to the Graham and Karnovsky method 4, and counterstained with cresyl violet. The nomenclature adopted for the relevant subdivisions of the thalamus follows, with certain modifications21, that of Karten and HodosS; nucleus lateralis anterior (LA); nucleus dorsolateralis anterior thalami, pars lateralis rostralis (DLAIr); nucleus

126 dorsolateralis anterior thalami, pars magnocellularis ( D L A m c ) and nucleus dorsolateralis anterior thalami, pars lateralis (DEE). The latter can be subdivided into three regions : pars ventralis (DLLv), pars dorsalis (DLLd), a n d a superficially located pars

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B

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2

Fig. |. Schematic representation of frontal sections through the pigeon thalamus. A : Fink-Heimer method. 1, axonal and 2, axon terminal degeneration following left eye enucleation. B: distribution and density of peroxidase-positive neurones in the dorsal thalamus following injection of 0.3 1,1 HRP into the right Wulst. Striped area in top illustration indicates enzyme diffusion. Labelling in the thalamus is shown as (3) light, (4) moderate and (5) heavy. Abbreviations: DLAIr, nucleus dorsolateralis anterior thalami, pars lateralis rostralis; DLAmc, nucleus dorsolateralis anterior thalami, pars magnocellularis; DLLd, nucleus dorsolateralis anterior thalami, pars lateralis dorsalis; DLLmc, nucleus dorsolateralis anterior thalami, pars lateralis magnocellularis; DLLv, nucleus dorsolateralis anterior thalami, pars lateralis ventralis; DLM, nucleus dorsolateralis anterior thalami, pars medialis; DMA, nucleus dorsomedialis anterior thalami; DS, decussatio supraoptica; FPL, fasciculus prosencephali lateralis; GLv, nucleus geniculatus lateralis ventralis; HA, hyperstriatum accessorium; HD, hyperstriatum dorsale; HIS, hyperstriatum intercalatus superior; HV, hyperstriatum ventrale; LA, nucleus lateralis anterior; OM, tractus occipitomesencephalicus; R, nucleus rotundus; RS, nucleus reticulatus superior; SMe, stria medullaris; T, nucleus triangularis; TRO, tractus opticus; VLT, nucleus ventrolateralis thalami.

127 magnocellularis (DLLmc). Owing to the relatively complex organization of DLL, the basis for differentiation of its subdivisions will be presented. A precise boundary between DLLv and DLLd is difficult to establish using cytoarchitectonic criteria alone. In Nissl-stained preparations DLLv which lies directly over the nucleus rotundus (R) generally exhibits a higher cell density than DLLd, the latter being a dense fibre region containing fewer more scattered cells. As we shall see, however (Fig. 1A and B), a more accurate distinction is possible by further taking into account functional differences as related to crossed and uncrossed projections of these areas to the Wulst 13. The nucleus here referred to as DLLmc is located peripherally and dorsal to more caudal regions of DLLd. It is a well differentiated nucleus composed of large deeply staining cells, and is easily distinguished from the more caudally placed nucleus superficialis parvocellularis (SPC). The latter contains paler staining and more closely packed cells of smaller diameter. The nomenclature used for subdivisions of the hyperstriatum is that of Karten and Hodos8: hyperstriatum accessorium (HA); intercalatus superior (HIS); dorsale (HD) and ventrale (HV). Fink-Heimer and autoradiographic methods furnished significantly similar results. Besides contralateral visual projections to the hypothalamus, ventral thalamus, pretectum, tegmentum and tectum, terminal arborization was observed in the dorsal thalamic complex. The most prominent density of optic fibre terminals was found in LA and the ventral portion of DLLd. Lower densities were observed in DLAlr, DLAmc and the ventral and lateral regions of DLLv. There was no visible evidence of retinal projections to the dorsal portion of DLLd, DLLmc, SPC, nucleus dorsolateralis anterior thalami, pars medialis (DLM), or nucleus dorsolateralis posterior thalami (DLP) (Fig. 1A). Immediately following more superficial injections of 0.3 #1 HRP into the Wulst, a quantity of the injected enzyme solution was observed to escape at the point of penetration and this excess was removed. Histological examination of the injection sites showed that HRP spread from the surface to all underlying structures of the Wulst (HA, HIS, HD), and in some cases extended into regions of HV. In general, medial and dorsomedial areas of HA were spared. Peroxidase-positive neurones were identified bilaterally in the thalamus (Fig. 1B). Ipsilateral to the injection, neurones containing enzyme product were in DLLv, ventral portions of DLLd and DLAmc, and in confined areas of DLAlr. The greatest density of positive-reacting neurones was found in the ventral aspect of DLLv adjacent to the nucleus rotundus. On the contralateral side, peroxidase product was localized in DLLd, DLLmc, and restricted to very small areas of DLAmc and DLAlr. Here, higher concentrations of HRP-conraining neurones were located in the ventral portions of DLLd and DLLmc. With smaller 0.1 #1 injections of HRP made at a depth of 1 mm, enzyme diffusion was more localized in dorsolateral parts of HA, and in all cases extended laterally to include regions of superficial HIS, entirely sparing HD. Labelling in the ipsilateral thalamus was comparable to that obtained with 0.3/~1 injections. On the contralateral side however, with the exception of a few peroxidase-positive neurones in the ventral pole of DLLd, an almost total absence of peroxidase product was observed. Following injections of 0.1 #1 HRP made at depths of 2.0-2.5 mm, the injection site

128

Fig. 2. A : injection site for 0.1 ffl H R P m a d e at a depth of 2 m m into the Wulst ( ,< 11 ). B - D : peroxidase-positive n e u r o n e s in D L L v o f the t h a l a m u s ipsilateral to the injection of H R P . B, x 200; D, :< 800. C, x 500, s h o w s heavy labelling in the ventral region of D L L v overlying the nucleus r o t u n d u s (R).

129 extended laterally and ventrally into HIS, HD, and in certain instances portions of HV (Fig. 2A). In HA copsiderable enTyme spread was visible along the injection path towards the surface of the Wulst. The transported HRP was localized bilaterally in the thalamus and labelling resembled that obtained with larger more superficial injections of 0.3 #1. The pattern of labelling in the thalamus ipsilateral to the injection remained in all cases remarkably constant (Fig. 2B-D), and the total area containing peroxidase product was always larger than on the contralateral side. Similarly, no significant differences in the distribution or density of peroxidase product was observed for all injection sites along the rostral-caudal plane of the Wulst. In only one animal where HRP was injected into the most posterior region of the Wulst tested (A 10.0 mm) and at a depth of 2.0-2.5 mm, a small number of peroxidase-positive neurones were seen in the ventral pole of SPC contralateral to the injection. No peroxidase product was ever observed in LA, DLM, DLP, or nucleus dorsomedialis anterior thalami (DMA). The partial overlap of ipsilateral and contralateral thalamic regions containing peroxidase product indicates the existence of three distinct areas with differential projections to the Wulst; in DLL, a major area with ipsilateral projections located in DLLv, one with contralateral projections essentially in DLLmc and the dorsal portion of DLLd, and one with bilateral projections in the ventral portion of DLLd. Rostrally in DLAmc and DLAlr, positive-reacting neurones are less numerous, and occupy progressively smaller regions, however, a similar spatial arrangement between the three areas appears to be maintained. A closer examination of labelling in the ventral portion of DLLd, which is at the origin of bilateral projections to the Wulst, reveals crossed projections to be more numerous than uncrossed. Meier et al. 13, using the retrograde cell degeneration method, demonstrated bilateral projections from thalamus to Wulst via collateral axon branching. In view of this evidence, it may be postulated that this area is not homogeneous and comprises at least two populations of neurones: one with exclusively crossed projections and one with bilateral projections via collateral branching. The possibility of a third population within this area with uncrossed projections cannot be excluded. The same methods described in the present study have been applied to investigate the retino-thalamo-hyperstriatal pathway in other birds of different species: chick ( Gallus domesticus), duck ( Anas platyrynchos), herring gull ( Larus argentatus) and jackdaw (Corvus monedula). In these species, the topographical arrangement of the areas in the thalamus with ipsilateral, contralateral, and bilateral projections to the Wulst was essentially the same as that observed in the pigeon (unpublished observations). DLAlr and DLAmc projections to the Wulst, and the existence of a thalamic area with an exclusively contralateral projection have not been reported by workers using the retrograde cell degeneration methodS, 13. A possible explanation is that following lesions of the Wulst, involved neurones in the thalamus may escape detection due to the 'sustaining collateral' phenomenon, a complicating factor apparently avoided with the HRP methodlL Another explanation may lie in the difficulty of detecting involved areas due to a relatively small number of cells showing the retrograde reaction 13. Our own study showed a low density of peroxidase-positive

130 neurones to be contained within most of these same areas. Electrophysiological evidence in support of a direct projection from DLAmc to the ipsilateral Wulst has been provided by Mihailovi~ et al. 15. At present, the sites of termination of LA efferents are subject to controversy. For certain authors, LA is part of the ventral thalamus 19,z°, for others it is included in the dorsal thalamus with direct projections to the telencephalon2,7,9,10,13,16, and more precisely to the visual WulstZ, 9. No indication that LA contributes to the direct thalamo-Wulst pathway was obtained with the H R P method, and is in agreement with findings derived from previous anatomicaP3, 2z and physiological studieslL Our study provided no conclusive evidence of a topographical rostral-caudal relationship between the Wulst and the thalamusS, 13. This may be attributed to the limited region of Wulst investigated and/or the relatively wide diffusion of the enzyme in the rostral-caudal plane. Comparing labelling patterns in the thalamus with superficial and deeper injections of HRP shows that distribution of bilateral projections to the Wulst is not homotopic. Regions of HA and/or lateral, more superficial, HIS receive fibers from DLLv and the ventral portion of DLLd of the ipsilateral thalamus, HD and/or deeper, more medial, HIS regions from DLLd and DLLmc of the contralateral thalamus. Due to the extent of HRP spread at the injection site, we were unable to isolate HIS from HA, or H D from HIS and HA, and could account for the consistent labelling of the ipsilateral thalamus. These findings are compatible with data obtained by Hunt and Webster z4. The thalamic nuclei which receive retinal fibres and project to the Wulst are DLLv, DLLd, DLAmc and DLAIr. The highest density of retinal terminal arborization was found in the ventral portion of DLLd which is mainly at the origin of bilateral projections. Such an organization would suggest the processing of binocular visual information by this forebrain structure. Peri~i6 et al. is, using electrophysiological methods, distinguished three areas in the Wulst: one dorsally located area receiving input from the contralateral eye, one ventrally from the ipsilateral eye and an intermediate area receiving binocular input. This is an interesting finding in the context of the data presented, and suggests that these areas of the Wulst respectively receive projections from three correspondingly distinct areas of the thalamus. In view of contrasting reports regarding the sites of termination of thalamic projectionsS, 9, it is difficult to assess to what degree the differential distribution of neurone populations in the visual Wulst is attributable to thalamic projections, or to intrinsic synaptic organization. We wish to thank Dr. Y. Galifret for his support and suggestions and Mrs. G. Sanchez, Mr. D. Le Cren and Mr. J. Loisil for excellent technical assistance.

I COWAN, W. M., GOTTLIEB, D. 1., HENDRICKSON, A. E., PRICE, J. L., AND WOOLSEY, T. A., The autoradiographic demonstration of axonal connections in the central nervous system, Brain Research, 37 (1972) 21-51. 2 EDINGER, L., WALLENBERG, A., UND HOLMES, G., Untersuchungen fiber die vergleichende Anato-

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11 12

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mie des Gehirnes. 5. Untersuchungen fiber das Vorderhirn der V6gel, Abh. Senek. Nat. Ges., 20 (1903) 343-426. FINK, R. P., AND HEIMER,L., Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system, Brain Research, 4 (1967) 369-374. GRAHAM, R. C., JR., AND KARNOVSKV, M. J., The early stages of absorption of injected horseradish peroxidase in the proximal tubule of mouse kidney: ultrastructural cytochemistry by a new technique, J. Histochem. Cytoehem., 14 (1966) 291-302. HUNT, S. P., AND WEBSTER, K. E., Tbalamo-hyperstriate interrelations in the pigeon, Brain Research, 44 (1972) 647-651. KARNOVSKY,M. J., Formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy, J. Cell Biol., 27 (1965) 137A. KARTEN,H. J., The organization of the avian telencephalon and some speculations on the phylogeny of the amniote telencephalon, Ann. N.Y. Acad. Sci., 167 (1969) 164-179. KARTEN, H. J., AND HODOS, W., A Stereotaxic Atlas of the Brain of the Pigeon (Columba livia), John Hopkins Press, Baltimore, Md., 1967. KARTEN, H. J., HODOS, W., NAUTA, W. J. H., AND REVZIN, A. M., Neural connections of the 'visual Wulst' of the avian telencephalon. Experimental studies in the pigeon (Columba livia) and owl (Speotyto canicularia), J. comp. Neurol., 150 (1973) 253-276. KURLENBECK,H., The ontogenetic development of the diencephalic centers in a bird's brain (chick) and comparison with the reptilian and mammalian diencephalon, J. comp. Neurol., 66 (1937) 23-75. LAVAIL, J. H., AND LAVAIL, M. M., Retrograde axonal transport in the central nervous system, Science, 176 (1972) 1416-1417. LAVAIL, J. H., WINSTON, K. R., AND TISH, A., A method based on retrograde intraaxonal transport of protein for identification of cell bodies of origin of axons terminating within the CNS, Brain Research, 58 (1973) 470-477. MEIER, R. E., MIHAILOVI(~,J., AND CUENOD, M., Thalamic organization of the retino-thalamohyperstriatal pathway in the pigeon (Columba livia), Exp. Brain Res., 19 (1974) 351-364. MICELI,D., AND GIOANNI,H., Unit responses to visual stimuli in the Wulst & t h e pigeon (Columba livia), in preparation. MlnkXLOVIt~,J., PERI~I(~, M., BERGONZI, R., AND MEIER, R. E., The dorsolateral thalamus as a relay in the retino-Wulst pathway in pigeon (Columba livia). An electrophysiological study, Exp Brain Res., 21 (1974) 229-240. MINELLI, G., Effeti delte degenerazioni sperimentali sulle corteccie e sui nuclei basali del telencefalo di Gallus e Coturnix, Boll. Zool., 31 (1964) 1273-1292. PARKER,D. M., AND DELIUS,J. D., Visual evoked potentials in the forebrain of the pigeon, Exp Brain Res., 14 (1972) 198-209. PERI~IC, M., MIHAILOVIC,J., AND CUI~NOD,M., Electrophysiology of contralateral and ipsilateral visual projections to the Wulst in pigeon (Columba livia), Int. J. Neurosci., 2 (1971) 7-14. POWELL,T. P. S., AND COWAN, W. M., The thalamic projection on the telencephalon in the pigeon (Columba livia), J. Anat. (Lond.), 95 (1961) 78-109. RENDAHL, H., Embryologische und morphologische Studien fiber das Zwischenhirn beim Huhn, Acta Zool., 5 (1924) 241-344. REPt~RANT,J., Nouvelles donn6es sur les projections visuelles chez le pigeon (Columba livia), J. Hirnforsch., 14 (1973) 151-187. REPI~RANT,J., RAFFIN, J.-P., ET MICELI, D., La voie r6tino-thalamo-hyperstriatale chez ie poussin (Gallus domesticus), C.R. Acad. Sci. (Paris), 279 (1974) 279-282. REVZIN, A. M., A specific visual projection area in the hyperstriatum of the pigeon (Columba livia), Brain Research, 15 (1969) 246-249. WEBSTER,K. E., Changing concepts of the organization of central visual pathways in birds. In R. BELLAIRSAND E. G. GRAY (Eds.), Essays on the Nervous System, Oxford University Press, 1974, pp. 258-298.

The retino-thalamo-hyperstriatal pathway in the pigeon (Columba livia).

Brain Research, 100 (1975) 125-131 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands The retino-thalamo-hyperstriatal...
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