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The laminar source of efferent projections from the avian Wulst
Brain Research, 275 (1983) 349-354
349
Elsevier
Short Communications
The laminar source of efferent projections from the avian Wulst ANTON REINER* and HARVEY J. KARTEN Department of Neurobiology and Behavior, SUNY at Stony Brook, N Y 11794 (U.S.A.)
(Accepted May 17th, 1983) Key words: pigeons - - Wulst - - horseradish peroxidase - - hyperstriatum accessorium- - tractus septomesencephalicus - - efferent
projections - - laminar organization
Following horseradish peroxidase injections into the pigeon tractus septomesencephalicus, the efferent outflow bundle of the avian Wulst, retrogradely labeled neurons within the Wulst were confined to the superficialmost layer, the hyperstriatum accessorium. These results suggest that the hyperstriatum accessorium is the sole source of Wulst efferent projections. In similarity to the laminar organization of mammalian striate cortex, this efferent layer is juxtaposed to the thalamorecipient layer of Wulst. The avian Wulst is a multilayered portion of the rostral pallial roof of the telencephalon. It is macroscopically visible as a bulge that extends from a lateral groove, termed the vallecula, to the midline. Considerable interspecific variation is present among birds in the size of the Wulst. In owls, the Wulst extends over the entire dorsal surface of the rostral telencephalon, while in pigeons and chickens it occupies only the rostromedial portion of the telencephalon. In all birds, however, the Wulst consists of 4 primary layers: (1) a deep layer of large cells, the hyperstriaturn dorsale (HD); (2) a more superficial layer of scattered cells, the hyperstriatum intercalatus superior (HIS); (3) a thin granule cell layer, the intercalated nucleus of the hyperstriatum accessorium (IHA); and (4) a broad superficial layer of mediumsized steilate cells, the hyperstriatum accessorium (HA)10. In owls these layers are arranged parallel to the dorsal surface of the telencephalon, while in pigeons and chickens these layers are oriented orthogonally to an imaginary line passing through the dorsomedial edge of the telencephalon. In all birds studied, the granule cell layer interposed between H A and HIS, namely I H A , receives a visual input from
retinorecipient dorsolateral thalamuslO,20,22. This thalamic nucleus receives retinal input only from the contralateral eye 17. The thalamic input to the Wulst apparently conveys an orderly retinotopic map. In owls, the nasal-temporal axis of the contralateral eye is mapped along the lateral-medial axis of the Wulst, while the superior-inferior visual axis is mapped along the caudal-rostral Wulst axis 15. In chickens and pigeons, the superior-inferior axis of the visual field is mapped on the Wulst as in owls, but the nasal-temporal axis is reportedly not mapped in a straightforward fashion6,14, 23. In all birds studied, however, lateral I H A receives input from both the contralateral and ipsilateral retinorecipient thalamusl0,20,2L Consistent with the anatomical data, the lateral Wulst of owl contains an over-representation of the binocular (nasal) visual field 15. Karten et al. 11 have noted that not all of the Wulst is visual in function. A rostral portion of the Wulst appears to be a somatosensory/somatomotor region, based on its connectionsS.11. The layer of termination of thalamic somatomotor input to the Wulst is unclear. Several authors have noted the similarity between the avian 'visual' Wulst and the striate cortex of
* To whom all correspondence should be addressed at: Dept. of Anatomy and Cell Biology, University of Michigan, Ann Arbor, MI 48109, U.S.A. 0006-8993/83/$03.00 © 1983 Elsevier Science Publishers B.V.
350 mammals 13. Both receive retinotopic visual inputs from retinorecipient thalamic cell groupst0.1L Further, both have similar efferent projection targets, including the retinorecipient thalamic cell group afferent to the telencephalon, the ventral geniculate nucleus, the tectum and several visual pretectal nuclei 10.19. In mammals, the extratelencephalic efferents of striate cortex arise from layers 5 and 612. In birds, the extratelencephalic projections of the Wulst have only been characterized for the Wulst-tectal projection. In owl and pigeon, H A has been reported to give rise to the projection to the tectum 4.5. Bagnoli et al. 2 have recently suggested that HIS also projects to the tectum. In order to more fully clarify the laminar organization of the Wulst, we have made horseradish peroxidase (HRP) injections (in pigeons) into the efferent outflow bundle of the Wulst, the tractus septomesencephalicus (TSM), to determine the laminar source of the extratelencephalic efferent projections from the Wulst. The TSM descends along the medial wall of the telencephalon and enters the diencephalon medial to the dorsal edge of the optic tract. Within the diencephalon, the TSM divides into a dorsal ramus, which terminates in visual areas of the diencephaion and mesencephalon, and a ventral ramus, which appears to be the outflow bundle of somatosensory Wulst 10. In pigeons the ventral ramus terminates in the medial pontine nucleus, the medial spiriform nucleus and the prerubral field. In owls, the ventral ramus has additional terminations in nucleus ruber and nucleus gracilis-cuneatus~. Injections of a 40% solution of HRP (in distilled water) were targeted in 6 pigeons so as to penetrate both the dorsal and ventral rami of the TSM at rostral diencephalic levels. A 1 pl Hamilton syringe was used for the injections to maximize the damage to and uptake by the fibers of the TSM. Processing of the tissue for H R P was carried out using benzidine dihydrochloride, as described previously 16. "In 4 birds, the HRP injections encroached on only a portion of the TSM or its ventral diencephalic target, the ventral geniculate nucleus. In all 4 birds, labeled neurons were observed only in the ipsilateral hyperstriatum accessorium. These neurons were only present within a limited portion of the full extent of HA, as defined in the stereotaxic atlas of Karten and Hodos 9. In two birds, the H R P injection site in-
~'~ RSv
A7.25 Fig. 1. Line drawing of transverse section illustrating the HRP injection site (blackened region) in pigeon T51. The injection site in this bird was centered in the lateral rostral diencephalon. The injection site included both the dorsal and ventral rami of the tractus septornesencephalicus. Abbreviations: A, archistriatum; AL, ansa lenticularis; APH, area parahippocampalis; FPL, fasciculusprosencephali lateralis; GLv, nucleus geniculatus lateralis, pars ventralis; HV, hyperstriatum ventrale; Hp, hippocampus; N, neostriatum; OM, tractus occipitomesencephalicus; PA, paleostriatum augmentatum; RSv, nucleus reticularis superior, pars ventralis; SL, nucleus septalis lateralis; TO, tractus opticus. cluded both the dorsal and ventral rami of the TSM (see Fig. 1). In one of these birds (T51), substantial orthograde H R P labeling was present in fibers and terminals in the target nuclei of the TSM, thus suggesting that H R P had been taken up by damaged TSM fibers of passage. Within the Wulst of this bird (see Fig. 2), numerous well-labeled neurons were seen throughout the entire rostro-caudal and mediolateral extent of HA, as defined in the atlas of Karten and Hodos 9. The field of labeled neurons cut off sharply at the boundary between H A and the granule cell layer, IHA. Careful high power examination of the deeper layers failed to disclose any labeled neurons in the granule cell layer, HIS or HD. At more caudal levels, labeled neurons were present in the dorsolateral extension of H A over HIS and IHA. Two or 3 labeled neurons per section were observed at intermediate depths of contralateral H A at a restricted rostral level of Wulst (corresponding to Fig. 2C). Thus, H A appears to be the exclusive source of the TSM, the extratelencephalic efferent outflow bundle of the Wulst. The labeled neurons of H A were medium-sized (15-20/~m) stellate neurons and were not morphologically distinguishable from unlabeled neurons of HA. Assuming that all efferent neurons of the Wulst were labeled in T51, these neurons
351 HA
D
HA.. ~
N
W .A ~ = ~
A100
~,s
E
A125
HA
c HA
Fig. 2. Line drawings of a rostro-caudal (A-F) series of transverse sections through the Wulst of the bird (T51) whose HRP injection site is illustrated in Fig. 1. Each circle represents the location of a single HRP-labeled neuron. The number next to each section corresponds to its approximate level in the atlas of Karten and Hodos9. The granule cell layer of the Wulst (IHA) is located ~ong the supertidal edge of HIS, immediately deep to HA. Abbreviations: B, nucleus basalis; CO, chiasma opticum; E, ectostriatum; HA, hyperstriatum accessorium; HD, hyperstriamm dorsale; HIS, hyperstriatum intercalatus superior; HV, hyperstriatum ventrale; INP, nucleus intrapeduncularis; LPO, lobus parolfactorius; N, neostriatum; PA, paleostriatum augmentatum; PP, paleostriatum primitivum; SL, nucleus septalis lateralis; TSM, tractus septomesencephalicus; TuO, tuberculum olfactorinm.
352 appear to make up 5-10% of the population of H A neurons. The present results are consistent with previous anterograde degeneration studies on the efferent projections of the Wulst. These studies, in several avian species, noted that only Wulst lesions that included the hyperstriatum accessorium resulted in degeneration of axons within the TSM 1,10. Further, several recent H R P studies have shown that H A is the exclusive source of the Wulst projection to the tectum4. 5. In addition, H R P injections into either the ventral geniculate (present study) or the mesencephalic lentiform region also label cells only of H A (unpublished observations). In the present study, partial or complete H R P injections into TSM resulted in labeled neurons within the same single layer of the Wulst, HA. Since the largest H R P injection sites in the present study included both the dorsal and ventral rami of the TSM, it seems likely that the extratelencephalic efferents of both 'visual' Wulst and the more anterior region, 'somatosensory/somatomotor' Wulst, arise from HA. The present results indicate that, while the granule cell layer of the 'visual' Wulst, I H A , receives visual input from the retinorecipient dorsolateral thalamic complexlO, 17, the immediately superficial layer gives rise to the output of the Wulst. The juxtaposition of input and output layer of Wulst raises the question of the direction of information flow within the 'visual' Wulst. Revzin TM has reported that the 'visual' Wulst shows a columnar visual receptive field organization in pigeon, with columns arranged perpendicular to the H A - I H A border. Pettigrew and Konishi 15 have shown a columnar organization in owl and have noted that units within I H A show simple visual receptive fields, while units in H A show more complex visual receptive fields. Further, Pettigrew and Konishi x5 and Rezvin TMindicate that the visual field maps of H A and I H A are in register with one another. These results imply that neurons of H A may receive input from I H A neurons that lie in the same 'column'. No direct evidence, however, is currently available of an I H A to H A projection. Since H A contains a visuotopic map and projects to visuotopically organized structures such as the tectum, it seems likely that the efferent projections of the Wulst are retinotopically organized. For the Wulst-tectal projection this has been shown clearly
in the owl 4,10 and suggestively in the pigeon 5. In the owl, the binocular portion of the Wulst has a crossed projection to the portion of the contralateral tectum that contains a representation of the inferior nasal visual field4,10. Very few labeled cells were, however, observed in the contralateral H A in the present study, and only at a restricted level of HA. Two factors may account for this: (1) the pigeon has a smaller binocular field in the Wulst than does the owl and has only a limited contralateral projection from the WulstlO, 15, and (2) the contralateral Wulst projection crosses via the supraoptic decussation, which lies largely caudal to the present H R P injections. Bagnoli et al. 2 have, however, recently reported that: (1) H A projects bilaterally and seemingly non-topographically to pigeon tectum, and (2) HIS also projects bilaterally and seemingly non-topographically to pigeon tectum. The former conclusion is inconsistent with the results of other studiesS, lo and the latter observation is inconsistent with this study and several others4,5, lo. The bases of the discrepancies with the Bagnoli et al. 2 study are unclear. Several recent physiological studies6. 23 concluded that the temporal-nasal visual axis is not represented in a simple fashion in pigeon and chicken Wulst. Specifically, although lateral I H A is reported by anatomical studies to receive bilateral input from the nasal hemifield of each eye 3,20,22, electrophysiological studies have reported that temporal hemifield representation is found in the lateral Wulst and nasal hemifield representation in medial Wulst6, 23. Both Wilson 23 and Denton 6 note the absence of evidence for separate visual field representations in H A and I H A and conclude that the temporal-nasal axis in chicken and pigeon is represented in a complex map that spans the dorsoventral extent of HA, I H A and HIS. These conclusions are difficult to reconcile with the anatomical data. The neurons of H A do not receive input from retinorecipient thalamus 22, which terminates on neurons of IHA. Thus, H A neurons must derive their visual responsivity from another input, presumably IHA. The anatomical data, as noted above, further indicate that lateral I H A should contain a representation of nasal hemifield in chicken, quail and pigeon. The anatomical data, and extrapolation from the electrophysiological work in owls, suggests that the nasal-temporal visual axis should be organized parallel to I H A in owls, pigeons and galli-
353 form birds. Previous physiological studies in pigeons and chickens, however, have used electrode penetrations oblique to I H A . Given the restricted medio-lateral extent of pigeon and chicken Wulst, electrode penetrations orthogonal or parallel to I H A might provide clearer indication as to: (1) the organization of the visual field in chicken and pigeon Wulst, and (2) the relation of the visual map in H A to that in IHA. The present study shows that in the avian Wulst, as in the mammalian striate cortex, the thalamorecipient layer is juxtaposed to the layer of origin of the extratelencephalic efferent projections. In mammals, the geniculostriate pathway terminates in layer 4, while neurons of layers 5 and 6 are the sources of extratelencephalic efferentsT,12. In birds, however, the extratelencephalic efferent layer is superficial to the thalamorecipient layer. In this context, it would be of interest to know the laminar source of the intratelencephalic projections of the Wulst. In mammals cortical layers 2 and 3 are the source of the intratelencephalic projections of the striate cortex7A2. If the hodologically defined layers of the Wulst have a completely inverted superficial-to-deep sequence as com-
Special thanks are in order to Theresa Gonzales for illustrating assistance and to Dr. Nicholas Brecha for valuable discussion during the course of the research. The research was supported by NS-05682 (A.R.) and NS-12078 (H.J.K.).
1 Adamo, N. J., Connections of efferent fibers from hyperstriatal areas in chicken, raven and African lovebird, J. comp. Neurol., 131 (1967) 337-356. 2 Bagnoli, P., Grassi, S. and Magni, F., A direct connection between visual Wulst and tectum opticum in the pigeon (Columbia livia) demonstrated by horseradish peroxidase, Arch. ital. Biol., 118 (1980)72-88. 3 Bagnoli, P. and Burkhalter, A., Organization of the afferent projections to the Wulst in the pigeon, J. comp. Neurol., 214 (1983) 103-113. 4 Bravo, H. and Pettigrew, J. D,, The distribution of neurons projecting from retina and visual cortex to the thalamus and tectum opticum of the barn owl, Tyto alba, and the burrowing owl, Speotyto cunicularia, J. comp. Neurol., 199 (1981) 418-441. 5 Brecha, N., Some Observations on the Organization of the Avian Tectum: Afferent Nuclei and their Tectal Projections, Ph.D. Thesis, SUNY at Stony Brook, NY, 1978. 6 Denton, C. J., Topography of the hyperstriatal visual projection area in the young domestic chicken, Exp. Neurol., 74 (1981) 482-498. 7 Gilbert, C. D. and Kelly, J. P., The projections of cells in different layers of the cat's visual cortex, J. comp. Neurol., 163 (1981) 81-106. 8 Karten, H. J., Efferent projections of the Wulst of the owl, Anat. Rec., 196 (1971) 353. 9 Karten, H. J. and Hodos, W., A Stereotaxic Atlas of the Brain of the Pigeon (Columbia livia) Johns Hopkins Press, Baltimore, MD, 1967.
10 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 (Columbia livia) and owl (Speotyto cunicularia), J. comp. Neurol., 150 (1973) 253-278. 11 Karten, H. J., Konishi, M. and Pettigrew, J., Somatosensory representation in the anterior Wulst of the owl (Speotyto cunicularia), Soc. Neurosci. Abstr., 4 (1978) 554. 12 Lund, J. S., Lund, R. D., Hendrickson, A. E., Bunt, A. H. and Fuchs, A. F., The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase, J. comp. Neurol., 164 (1975) 287-303. 13 Nauta, W. J. H. and Karten, H. J., A general profile of the vertebrate brain, with sidelights on the ancestry of cerebral cortex. In F. O. Schmitt (Ed.), The Neurosciences: Second Study Program, Rockefeller Univ. Press, New York, 1970, pp. 7-26. 14 Perisic, M., Mihailovic, J. and Cu6nod, M., Electrophysiology of contralateral and ipsilateral projections to the Wulst in pigeon (Columbia livia), Int. J. Neurosci., 2 (1971) 7-14. 15 Pettigrew, J. D. and Konishi, M., Neurons selective for orientation and binocular disparity in the visual Wulst of the barn owl (Tyro alba), Science, 193 (1976) 675-678. 16 Reiner, A. and Karten, H. J., Laminar distribution of the cells of origin of the descending tectofugal pathways in the pigeon (Columbia livia), J. comp. Neurol., 204 (1982) 165-187.
pared to the hodologically defined layers of striate cortex, then one would predict that layers deep to I H A (either HIS or H D ) give rise to the Wulst intratelencephalic projections. Of related interest, Tsai et al. 21 have recently shown that the layers of the Wulst show an outside-in neurogenetic sequence. In contrast, the layers of mammalian striate cortex are known to show an inside-out neurogenesis. If it is found that H D or HIS gives rise to intratelencephalic projections, this would indicate that the hodologically defined layers of Wulst show similar topological and neurogenetic relationships to one another as do the comparably defined layers of striate cortex. Such similarites would indicate either a strikingly parallel evolution of Wulst and striate cortex, or the c o m m o n inheritance of several features from the visual cortex of ancestral reptiles, features that are neither readily apparent nor well investigated in reptiles.
354 17 Reperant, J., Nouvelles donn6es sur tes projections visuelles chex le pigeon (Columbia livia), J. Hirnforsch., 14 (1973) 151-187. 18 Revzin, A. M., A specific visual projection area in the hyperstriatum of the pigeon, Brain Research, 15 (1969) 246--249. 19 Rodieck, R. W., Visual pathways, Ann. Rev. Neurosci.. 2 (1979) 193-225. 20 Streit, P., Stella, M. and Cu6nod, M., Transneuronal labeling in the pigeon visual system, Neuroscience, 5 (1980) 763-775.
21 Tsai, M. T., Garber, B. B. and Larramendi, L. M. H., Thymidine autoradiographic analysis of telencephalic histogenesis in the chick embryo: I. Neuronal birthdates of telencephalic compartments in situ, J. comp. Neurol., 198 ( 1981) 275-292. 22 Watanabe, M., Ito, H. and Masai, H., Cytoarchitecture and visual receptive neurons in the Wulst of the Japanese quail (Coturnix coturnix japonica), J. comp. Neurol., 213 (1983) 188--198. 23 Wilson, P., The organization of the visual hyperstriatum in the domestic chick. 1. Topology and topography of the visual projection, Brain Research, 188 (1980) 319--332.
Note added in proof In the time since this manuscript was sent to the printer, some pertinent results reported in an unpublished doctoral dissertation have come to our attention (Teresa C. Ritchie, lntratelencephalic visual connections and their relationship to the archistriatum in the pigeon, Columba livia, Ph.D. Dissertation, University of Virginia, VA, 1979). Ritchie has suggested, based on anterograde pathway tracing data, that the intratelencephalic projections of the Wuist appear to arise from deeper Wulst layers, particularly HD. This result supports our suggestion that the hodologically defined layers of Wulst show similar topological and neurogenetic relationships to one another as do the comparably defined layers of striate cortex in mammals.
349
Elsevier
Short Communications
The laminar source of efferent projections from the avian Wulst ANTON REINER* and HARVEY J. KARTEN Department of Neurobiology and Behavior, SUNY at Stony Brook, N Y 11794 (U.S.A.)
(Accepted May 17th, 1983) Key words: pigeons - - Wulst - - horseradish peroxidase - - hyperstriatum accessorium- - tractus septomesencephalicus - - efferent
projections - - laminar organization
Following horseradish peroxidase injections into the pigeon tractus septomesencephalicus, the efferent outflow bundle of the avian Wulst, retrogradely labeled neurons within the Wulst were confined to the superficialmost layer, the hyperstriatum accessorium. These results suggest that the hyperstriatum accessorium is the sole source of Wulst efferent projections. In similarity to the laminar organization of mammalian striate cortex, this efferent layer is juxtaposed to the thalamorecipient layer of Wulst. The avian Wulst is a multilayered portion of the rostral pallial roof of the telencephalon. It is macroscopically visible as a bulge that extends from a lateral groove, termed the vallecula, to the midline. Considerable interspecific variation is present among birds in the size of the Wulst. In owls, the Wulst extends over the entire dorsal surface of the rostral telencephalon, while in pigeons and chickens it occupies only the rostromedial portion of the telencephalon. In all birds, however, the Wulst consists of 4 primary layers: (1) a deep layer of large cells, the hyperstriaturn dorsale (HD); (2) a more superficial layer of scattered cells, the hyperstriatum intercalatus superior (HIS); (3) a thin granule cell layer, the intercalated nucleus of the hyperstriatum accessorium (IHA); and (4) a broad superficial layer of mediumsized steilate cells, the hyperstriatum accessorium (HA)10. In owls these layers are arranged parallel to the dorsal surface of the telencephalon, while in pigeons and chickens these layers are oriented orthogonally to an imaginary line passing through the dorsomedial edge of the telencephalon. In all birds studied, the granule cell layer interposed between H A and HIS, namely I H A , receives a visual input from
retinorecipient dorsolateral thalamuslO,20,22. This thalamic nucleus receives retinal input only from the contralateral eye 17. The thalamic input to the Wulst apparently conveys an orderly retinotopic map. In owls, the nasal-temporal axis of the contralateral eye is mapped along the lateral-medial axis of the Wulst, while the superior-inferior visual axis is mapped along the caudal-rostral Wulst axis 15. In chickens and pigeons, the superior-inferior axis of the visual field is mapped on the Wulst as in owls, but the nasal-temporal axis is reportedly not mapped in a straightforward fashion6,14, 23. In all birds studied, however, lateral I H A receives input from both the contralateral and ipsilateral retinorecipient thalamusl0,20,2L Consistent with the anatomical data, the lateral Wulst of owl contains an over-representation of the binocular (nasal) visual field 15. Karten et al. 11 have noted that not all of the Wulst is visual in function. A rostral portion of the Wulst appears to be a somatosensory/somatomotor region, based on its connectionsS.11. The layer of termination of thalamic somatomotor input to the Wulst is unclear. Several authors have noted the similarity between the avian 'visual' Wulst and the striate cortex of
* To whom all correspondence should be addressed at: Dept. of Anatomy and Cell Biology, University of Michigan, Ann Arbor, MI 48109, U.S.A. 0006-8993/83/$03.00 © 1983 Elsevier Science Publishers B.V.
350 mammals 13. Both receive retinotopic visual inputs from retinorecipient thalamic cell groupst0.1L Further, both have similar efferent projection targets, including the retinorecipient thalamic cell group afferent to the telencephalon, the ventral geniculate nucleus, the tectum and several visual pretectal nuclei 10.19. In mammals, the extratelencephalic efferents of striate cortex arise from layers 5 and 612. In birds, the extratelencephalic projections of the Wulst have only been characterized for the Wulst-tectal projection. In owl and pigeon, H A has been reported to give rise to the projection to the tectum 4.5. Bagnoli et al. 2 have recently suggested that HIS also projects to the tectum. In order to more fully clarify the laminar organization of the Wulst, we have made horseradish peroxidase (HRP) injections (in pigeons) into the efferent outflow bundle of the Wulst, the tractus septomesencephalicus (TSM), to determine the laminar source of the extratelencephalic efferent projections from the Wulst. The TSM descends along the medial wall of the telencephalon and enters the diencephalon medial to the dorsal edge of the optic tract. Within the diencephalon, the TSM divides into a dorsal ramus, which terminates in visual areas of the diencephaion and mesencephalon, and a ventral ramus, which appears to be the outflow bundle of somatosensory Wulst 10. In pigeons the ventral ramus terminates in the medial pontine nucleus, the medial spiriform nucleus and the prerubral field. In owls, the ventral ramus has additional terminations in nucleus ruber and nucleus gracilis-cuneatus~. Injections of a 40% solution of HRP (in distilled water) were targeted in 6 pigeons so as to penetrate both the dorsal and ventral rami of the TSM at rostral diencephalic levels. A 1 pl Hamilton syringe was used for the injections to maximize the damage to and uptake by the fibers of the TSM. Processing of the tissue for H R P was carried out using benzidine dihydrochloride, as described previously 16. "In 4 birds, the HRP injections encroached on only a portion of the TSM or its ventral diencephalic target, the ventral geniculate nucleus. In all 4 birds, labeled neurons were observed only in the ipsilateral hyperstriatum accessorium. These neurons were only present within a limited portion of the full extent of HA, as defined in the stereotaxic atlas of Karten and Hodos 9. In two birds, the H R P injection site in-
~'~ RSv
A7.25 Fig. 1. Line drawing of transverse section illustrating the HRP injection site (blackened region) in pigeon T51. The injection site in this bird was centered in the lateral rostral diencephalon. The injection site included both the dorsal and ventral rami of the tractus septornesencephalicus. Abbreviations: A, archistriatum; AL, ansa lenticularis; APH, area parahippocampalis; FPL, fasciculusprosencephali lateralis; GLv, nucleus geniculatus lateralis, pars ventralis; HV, hyperstriatum ventrale; Hp, hippocampus; N, neostriatum; OM, tractus occipitomesencephalicus; PA, paleostriatum augmentatum; RSv, nucleus reticularis superior, pars ventralis; SL, nucleus septalis lateralis; TO, tractus opticus. cluded both the dorsal and ventral rami of the TSM (see Fig. 1). In one of these birds (T51), substantial orthograde H R P labeling was present in fibers and terminals in the target nuclei of the TSM, thus suggesting that H R P had been taken up by damaged TSM fibers of passage. Within the Wulst of this bird (see Fig. 2), numerous well-labeled neurons were seen throughout the entire rostro-caudal and mediolateral extent of HA, as defined in the atlas of Karten and Hodos 9. The field of labeled neurons cut off sharply at the boundary between H A and the granule cell layer, IHA. Careful high power examination of the deeper layers failed to disclose any labeled neurons in the granule cell layer, HIS or HD. At more caudal levels, labeled neurons were present in the dorsolateral extension of H A over HIS and IHA. Two or 3 labeled neurons per section were observed at intermediate depths of contralateral H A at a restricted rostral level of Wulst (corresponding to Fig. 2C). Thus, H A appears to be the exclusive source of the TSM, the extratelencephalic efferent outflow bundle of the Wulst. The labeled neurons of H A were medium-sized (15-20/~m) stellate neurons and were not morphologically distinguishable from unlabeled neurons of HA. Assuming that all efferent neurons of the Wulst were labeled in T51, these neurons
351 HA
D
HA.. ~
N
W .A ~ = ~
A100
~,s
E
A125
HA
c HA
Fig. 2. Line drawings of a rostro-caudal (A-F) series of transverse sections through the Wulst of the bird (T51) whose HRP injection site is illustrated in Fig. 1. Each circle represents the location of a single HRP-labeled neuron. The number next to each section corresponds to its approximate level in the atlas of Karten and Hodos9. The granule cell layer of the Wulst (IHA) is located ~ong the supertidal edge of HIS, immediately deep to HA. Abbreviations: B, nucleus basalis; CO, chiasma opticum; E, ectostriatum; HA, hyperstriatum accessorium; HD, hyperstriamm dorsale; HIS, hyperstriatum intercalatus superior; HV, hyperstriatum ventrale; INP, nucleus intrapeduncularis; LPO, lobus parolfactorius; N, neostriatum; PA, paleostriatum augmentatum; PP, paleostriatum primitivum; SL, nucleus septalis lateralis; TSM, tractus septomesencephalicus; TuO, tuberculum olfactorinm.
352 appear to make up 5-10% of the population of H A neurons. The present results are consistent with previous anterograde degeneration studies on the efferent projections of the Wulst. These studies, in several avian species, noted that only Wulst lesions that included the hyperstriatum accessorium resulted in degeneration of axons within the TSM 1,10. Further, several recent H R P studies have shown that H A is the exclusive source of the Wulst projection to the tectum4. 5. In addition, H R P injections into either the ventral geniculate (present study) or the mesencephalic lentiform region also label cells only of H A (unpublished observations). In the present study, partial or complete H R P injections into TSM resulted in labeled neurons within the same single layer of the Wulst, HA. Since the largest H R P injection sites in the present study included both the dorsal and ventral rami of the TSM, it seems likely that the extratelencephalic efferents of both 'visual' Wulst and the more anterior region, 'somatosensory/somatomotor' Wulst, arise from HA. The present results indicate that, while the granule cell layer of the 'visual' Wulst, I H A , receives visual input from the retinorecipient dorsolateral thalamic complexlO, 17, the immediately superficial layer gives rise to the output of the Wulst. The juxtaposition of input and output layer of Wulst raises the question of the direction of information flow within the 'visual' Wulst. Revzin TM has reported that the 'visual' Wulst shows a columnar visual receptive field organization in pigeon, with columns arranged perpendicular to the H A - I H A border. Pettigrew and Konishi 15 have shown a columnar organization in owl and have noted that units within I H A show simple visual receptive fields, while units in H A show more complex visual receptive fields. Further, Pettigrew and Konishi x5 and Rezvin TMindicate that the visual field maps of H A and I H A are in register with one another. These results imply that neurons of H A may receive input from I H A neurons that lie in the same 'column'. No direct evidence, however, is currently available of an I H A to H A projection. Since H A contains a visuotopic map and projects to visuotopically organized structures such as the tectum, it seems likely that the efferent projections of the Wulst are retinotopically organized. For the Wulst-tectal projection this has been shown clearly
in the owl 4,10 and suggestively in the pigeon 5. In the owl, the binocular portion of the Wulst has a crossed projection to the portion of the contralateral tectum that contains a representation of the inferior nasal visual field4,10. Very few labeled cells were, however, observed in the contralateral H A in the present study, and only at a restricted level of HA. Two factors may account for this: (1) the pigeon has a smaller binocular field in the Wulst than does the owl and has only a limited contralateral projection from the WulstlO, 15, and (2) the contralateral Wulst projection crosses via the supraoptic decussation, which lies largely caudal to the present H R P injections. Bagnoli et al. 2 have, however, recently reported that: (1) H A projects bilaterally and seemingly non-topographically to pigeon tectum, and (2) HIS also projects bilaterally and seemingly non-topographically to pigeon tectum. The former conclusion is inconsistent with the results of other studiesS, lo and the latter observation is inconsistent with this study and several others4,5, lo. The bases of the discrepancies with the Bagnoli et al. 2 study are unclear. Several recent physiological studies6. 23 concluded that the temporal-nasal visual axis is not represented in a simple fashion in pigeon and chicken Wulst. Specifically, although lateral I H A is reported by anatomical studies to receive bilateral input from the nasal hemifield of each eye 3,20,22, electrophysiological studies have reported that temporal hemifield representation is found in the lateral Wulst and nasal hemifield representation in medial Wulst6, 23. Both Wilson 23 and Denton 6 note the absence of evidence for separate visual field representations in H A and I H A and conclude that the temporal-nasal axis in chicken and pigeon is represented in a complex map that spans the dorsoventral extent of HA, I H A and HIS. These conclusions are difficult to reconcile with the anatomical data. The neurons of H A do not receive input from retinorecipient thalamus 22, which terminates on neurons of IHA. Thus, H A neurons must derive their visual responsivity from another input, presumably IHA. The anatomical data, as noted above, further indicate that lateral I H A should contain a representation of nasal hemifield in chicken, quail and pigeon. The anatomical data, and extrapolation from the electrophysiological work in owls, suggests that the nasal-temporal visual axis should be organized parallel to I H A in owls, pigeons and galli-
353 form birds. Previous physiological studies in pigeons and chickens, however, have used electrode penetrations oblique to I H A . Given the restricted medio-lateral extent of pigeon and chicken Wulst, electrode penetrations orthogonal or parallel to I H A might provide clearer indication as to: (1) the organization of the visual field in chicken and pigeon Wulst, and (2) the relation of the visual map in H A to that in IHA. The present study shows that in the avian Wulst, as in the mammalian striate cortex, the thalamorecipient layer is juxtaposed to the layer of origin of the extratelencephalic efferent projections. In mammals, the geniculostriate pathway terminates in layer 4, while neurons of layers 5 and 6 are the sources of extratelencephalic efferentsT,12. In birds, however, the extratelencephalic efferent layer is superficial to the thalamorecipient layer. In this context, it would be of interest to know the laminar source of the intratelencephalic projections of the Wulst. In mammals cortical layers 2 and 3 are the source of the intratelencephalic projections of the striate cortex7A2. If the hodologically defined layers of the Wulst have a completely inverted superficial-to-deep sequence as com-
Special thanks are in order to Theresa Gonzales for illustrating assistance and to Dr. Nicholas Brecha for valuable discussion during the course of the research. The research was supported by NS-05682 (A.R.) and NS-12078 (H.J.K.).
1 Adamo, N. J., Connections of efferent fibers from hyperstriatal areas in chicken, raven and African lovebird, J. comp. Neurol., 131 (1967) 337-356. 2 Bagnoli, P., Grassi, S. and Magni, F., A direct connection between visual Wulst and tectum opticum in the pigeon (Columbia livia) demonstrated by horseradish peroxidase, Arch. ital. Biol., 118 (1980)72-88. 3 Bagnoli, P. and Burkhalter, A., Organization of the afferent projections to the Wulst in the pigeon, J. comp. Neurol., 214 (1983) 103-113. 4 Bravo, H. and Pettigrew, J. D,, The distribution of neurons projecting from retina and visual cortex to the thalamus and tectum opticum of the barn owl, Tyto alba, and the burrowing owl, Speotyto cunicularia, J. comp. Neurol., 199 (1981) 418-441. 5 Brecha, N., Some Observations on the Organization of the Avian Tectum: Afferent Nuclei and their Tectal Projections, Ph.D. Thesis, SUNY at Stony Brook, NY, 1978. 6 Denton, C. J., Topography of the hyperstriatal visual projection area in the young domestic chicken, Exp. Neurol., 74 (1981) 482-498. 7 Gilbert, C. D. and Kelly, J. P., The projections of cells in different layers of the cat's visual cortex, J. comp. Neurol., 163 (1981) 81-106. 8 Karten, H. J., Efferent projections of the Wulst of the owl, Anat. Rec., 196 (1971) 353. 9 Karten, H. J. and Hodos, W., A Stereotaxic Atlas of the Brain of the Pigeon (Columbia livia) Johns Hopkins Press, Baltimore, MD, 1967.
10 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 (Columbia livia) and owl (Speotyto cunicularia), J. comp. Neurol., 150 (1973) 253-278. 11 Karten, H. J., Konishi, M. and Pettigrew, J., Somatosensory representation in the anterior Wulst of the owl (Speotyto cunicularia), Soc. Neurosci. Abstr., 4 (1978) 554. 12 Lund, J. S., Lund, R. D., Hendrickson, A. E., Bunt, A. H. and Fuchs, A. F., The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase, J. comp. Neurol., 164 (1975) 287-303. 13 Nauta, W. J. H. and Karten, H. J., A general profile of the vertebrate brain, with sidelights on the ancestry of cerebral cortex. In F. O. Schmitt (Ed.), The Neurosciences: Second Study Program, Rockefeller Univ. Press, New York, 1970, pp. 7-26. 14 Perisic, M., Mihailovic, J. and Cu6nod, M., Electrophysiology of contralateral and ipsilateral projections to the Wulst in pigeon (Columbia livia), Int. J. Neurosci., 2 (1971) 7-14. 15 Pettigrew, J. D. and Konishi, M., Neurons selective for orientation and binocular disparity in the visual Wulst of the barn owl (Tyro alba), Science, 193 (1976) 675-678. 16 Reiner, A. and Karten, H. J., Laminar distribution of the cells of origin of the descending tectofugal pathways in the pigeon (Columbia livia), J. comp. Neurol., 204 (1982) 165-187.
pared to the hodologically defined layers of striate cortex, then one would predict that layers deep to I H A (either HIS or H D ) give rise to the Wulst intratelencephalic projections. Of related interest, Tsai et al. 21 have recently shown that the layers of the Wulst show an outside-in neurogenetic sequence. In contrast, the layers of mammalian striate cortex are known to show an inside-out neurogenesis. If it is found that H D or HIS gives rise to intratelencephalic projections, this would indicate that the hodologically defined layers of Wulst show similar topological and neurogenetic relationships to one another as do the comparably defined layers of striate cortex. Such similarites would indicate either a strikingly parallel evolution of Wulst and striate cortex, or the c o m m o n inheritance of several features from the visual cortex of ancestral reptiles, features that are neither readily apparent nor well investigated in reptiles.
354 17 Reperant, J., Nouvelles donn6es sur tes projections visuelles chex le pigeon (Columbia livia), J. Hirnforsch., 14 (1973) 151-187. 18 Revzin, A. M., A specific visual projection area in the hyperstriatum of the pigeon, Brain Research, 15 (1969) 246--249. 19 Rodieck, R. W., Visual pathways, Ann. Rev. Neurosci.. 2 (1979) 193-225. 20 Streit, P., Stella, M. and Cu6nod, M., Transneuronal labeling in the pigeon visual system, Neuroscience, 5 (1980) 763-775.
21 Tsai, M. T., Garber, B. B. and Larramendi, L. M. H., Thymidine autoradiographic analysis of telencephalic histogenesis in the chick embryo: I. Neuronal birthdates of telencephalic compartments in situ, J. comp. Neurol., 198 ( 1981) 275-292. 22 Watanabe, M., Ito, H. and Masai, H., Cytoarchitecture and visual receptive neurons in the Wulst of the Japanese quail (Coturnix coturnix japonica), J. comp. Neurol., 213 (1983) 188--198. 23 Wilson, P., The organization of the visual hyperstriatum in the domestic chick. 1. Topology and topography of the visual projection, Brain Research, 188 (1980) 319--332.
Note added in proof In the time since this manuscript was sent to the printer, some pertinent results reported in an unpublished doctoral dissertation have come to our attention (Teresa C. Ritchie, lntratelencephalic visual connections and their relationship to the archistriatum in the pigeon, Columba livia, Ph.D. Dissertation, University of Virginia, VA, 1979). Ritchie has suggested, based on anterograde pathway tracing data, that the intratelencephalic projections of the Wuist appear to arise from deeper Wulst layers, particularly HD. This result supports our suggestion that the hodologically defined layers of Wulst show similar topological and neurogenetic relationships to one another as do the comparably defined layers of striate cortex in mammals.