A second ascending visual pathway from the optic tectum to the telencephalon in the pigeon (Columba livia)
Dr. Paul D. R. Gamlin
Department of Neurobiology and Behavior, SUNY at Stony Brook, Stony Brook, NY, 11794
Search for more papers by this authorDavid H. Cohen
Department of Neurobiology and Behavior, SUNY at Stony Brook, Stony Brook, NY, 11794
Search for more papers by this authorDr. Paul D. R. Gamlin
Department of Neurobiology and Behavior, SUNY at Stony Brook, Stony Brook, NY, 11794
Search for more papers by this authorDavid H. Cohen
Department of Neurobiology and Behavior, SUNY at Stony Brook, Stony Brook, NY, 11794
Search for more papers by this authorAbstract
Previous studies in the pigeon (Karten and Revzin: Brain Res. 2:368–377, '66; Karten and Hodos: J. Comp. Neurol. 140:35–52,'70) have described an ascending tectofugal visual pathway from the optic tectum to the ectostriatum by way of the nucleus rotundus of the thalamus. This present study used anterograde autoradiographic and retrograde horseradish peroxidase pathway-tracing techniques to investigate another ascending tectofugal pathway in the pigeon. Injections of 3H-proline/leucine confirmed a previous report that the optic tectum projects to the nucleus dorsolateralis posterior of the thalamus (DLP). This projection is predominantly ipsilateral and is confined to a large-celled caudal region of the nucleus (DLPc); the rostral region of the nucleus (DLPr) is not tectorecipient. Injections of horseradish peroxidase in DLPc labeled cells predominantly ipsilaterally in layers 8–15 of the optic tectum. Injections of 3H-proline/leucine placed in the DLPc labeled a discrete region of the ipsilateral telencephalon. Similar injections of DLPr labeled a contiguous, but more rostral, region of the neostriatum intermedium. Nissl- and silver-stained material indicated that the region in which DLP terminates is cytoarchitecturally distinct from ventromedial ectostriatal core and belt. Injections of horseradish peroxidase at various locations in the neostriatal DLP terminal field demonstrated a rostrocaudal ordering of the DLP projection upon the neostriatum intermedium. Singleunit recording demonstrated that cells in DLPc respond to whole-field illumination at the same latency as cells in the nucleus rotundus, indicating that the tecto-DLPc-neostriatal pathway transmits visual information to the telencephalon. We suggest that comparable pathways may exist in both reptiles and mammals.
Literature Cited
- Bagnoli, P., and A. Burkhalter (1983) Organization of the afferent projections to the Wulst in the pigeon. J. Comp. Neurol. 214: 103–113.
- Benevento, L. A. and J. H. Fallon (1975) The ascending projections of the superior colliculus in the rhesus monkey (Macaca mulatta). J. Comp. Neurol. 160: 339–362.
- Benevento, L. A., M. Rezak, and R. Santos-Anderson (1977) An autoradiographic study of the projections of the pretectum in the rhesus monkey (Macace mulatta): Evidence for sensorimotor links to the thalamus and oculumotor nuclei. Brain Res. 127: 197–218.
- Benevento, L. A., and G. P. Standage (1983) The organization of projections of the retinorecipient and non retino recipient nuclei of the pretectal complex and layers of the superior colliculus to the lateral pulvinar and medial pulvinar in the macaque monkey. J. Comp. Neurol. 217: 307–336.
- Benowitz, L. I. and H. J. Karten (1976) Organization of the tectofugal visual pathway in the pigeon: A retrograde transport study. J. Comp. Neurol. 167: 503–520.
- Braford, M. R., Jr. (1972) Ascending efferent tectal projections in the South American spectacled caiman. Anat. Rec. 172: 275–276.
- Bruce, L. L. and A. B. Butler (1984) Telencephalic connections in lizards. II. Projections to anterior dorsal ventricular ridge. J. Comp. Neurol. 229: 602–615.
- Cajal, P. R. (1891) Sur la fine structure de lobe optique des oiseaux et sur I'origine reelle des nerfs optiques. Int. Mschr. Anat. Physiol. 8: 337–366.
- Campbell, H. S. and J. L. Smith (1962) The pharmacology of the pigeon pupil. Arch. Ophthalmol. 67: 141–144.
- Cowan, W. M., L. Adamson and T. P. S. Powell (1961) An experimental study of the avian visual system. J. Anat. 95: 545–563.
- Crossland, W. J. and C. P. Hughes (1978) Observations on the afferent and efferent connections of the avian isthmo-optic nucleus. Brain Res. 145: 239–256.
- Delius, J. D., and K. Bennetto (1972) Cutaneous sensory projections to the avian forebrain. Brain Res. 4: 369–374.
- Duff, T. A. and D. H. Cohen (1975) Optic chiasm fibers of the pigeon: Discharge characteristics in response to whole field illumination. Brain Res. 92: 146–148.
- Foster, R. E. and W. C. Hall (1975) The connections and laminar organization of the optic tectum in a reptile (Iguana iguana). J. Comp. Neurol. 163: 397–426.
- Galifret, Y. (1966) Le Système Visuel du Pigeon. Anatomie et Physiologie. Correlations psychophysiologiques. Paris: These de Doctorat.
- Gamlin, P. D. R. and D. H. Cohen (1982) A possible second ascending avian tectofugal pathway. Soc. Neurosci. Abstr. 8: 206.
-
Gold, M. R. and
D. H. Cohen
(1981)
Heart rate conditioning in the pigeon immobilized with α-bungarotoxin.
Brain Res.
216:
163–172.
10.1016/0006-8993(81)91284-1 Google Scholar
- Graham, J. (1977) An autoradiographic study of the efferent connections of the superior colliculus in the cat. J. Comp. Neurol. 173: 629–654.
- Graybiel, A. M. (1972a) Some extrastriate visual pathways in the cat. Invest. Ophthalmol. 11: 322–333.
- Graybiel, A. M. (1972b) Some fiber pathways related to the posterior thalamic region in the cat. Brain Behav. Evol. 6: 363–393.
- Hanker, J. S., P. E. Yates, C. B. Metz, and A. Rustioni (1977) A new specific, sensitive and noncarcinogenic reagent for the demonstration of horseradish peroxidase. Histochem. J. 9: 789–792.
- Harting, J. K., W. C. Hall, I. T. Diamond and G. F. Martin (1973) Anterograde degeneration study of the superior colliculus in Tupaia glis: Evidence for a subdivision between superficial and deep layers. J. Comp. Neurol. 148: 361–386.
- Harting, J. K., M. F. Huerta, A. J. Frankfurter, N. L. Strominger and G. J. Royce (1980) Ascending pathways from the monkey superior colliculus: An autoradiographic analysis. J. Comp. Neurol. 192: 853–882.
- Hicks, T. P., S. Watanabe, A. Miyake, and K. Shomura (1984) Organization and properties of visually responsive neurones in the suprageniculate nucleus of the cat. Exp. Brain Res. 55: 359–367.
- Hodos. W.. S. R. B. Weiss and B. B. Bessette (1986) Size-threshold changes after lesions of the visual telencephalon in pigeons. Behav. Brain Res. (in press).
- Holstege, G., and H. Collewijn (1982) The efferent connections of the nucleus of the optic tract and the superior colliculus in the rabbit. J. Comp. Neurol. 209: 139–175.
- Hunt, S. P. and K. E. Webster (1975) The projection of the retina upon the optic tectum of the pigeon. J. Comp. Neurol. 162: 433–446.
- Hunt, S. P., and H. Kunzle (1976a) Observations on the projections and intrinsic organization of the pigeon optic tectum: An autoradiographic study based on anterograde and retrograde, axonal and dendritic flow. J. Comp. Neurol. 170: 153–172.
- Hunt, S. P., and H. Kunzle (1976b) Selective uptake and transport of label within three identified neuronal systems after injections of 3H-GABA into the pigeon optic tectum: An autoradiographic study. J. Comp. Neurol. 170: 173–190.
- Hunt, S. P., P. Streit, H. Kunzle, and M. Cuenod (1977) Characterization of the pigeon isthmo-tectal pathway by selective uptake and retrograde movement of radioactive compounds and by Golgi-like horseradish peroxidase labeling. Brain Res. 129: 197–212.
- Karten, H. J. (1963) Ascending pathways from the spinal cord in the pigeon Columba livia. Proc. 16th Inter. Cong. Zool. 2: 23.
- Karten, H. J. (1979) Visual lemniscal pathways in birds. In A. M. Granda and J. H. Maxwell (eds): Neural Mechanisms of Behavior in the Pigeon. New York: Plenum Press, pp. 409–430.
- Karten, H. J. and A. M. Revzin (1966) The afferent connections of the nucleus rotundus in the pigeon. Brain Res. 2: 368–377.
- Karten, H. J., and W. Hodos (1967) A Stereotaxic Atlas of the Brain of the Pigeon (Columba livia). Baltimore: Johns Hopkins Press.
- Karten, H. J., and W. Hodos (1970) Telencephalic projections of the nucleus rotundus in the pigeon (Columba livia). J. Comp. Neurol. 140: 35–52.
- Karten, H. J., W. Hodos, W. J. H. Nauta and A. M. Revzin (1973) Neural connections of the “visual wulst” of the avian telencephalon. Experimental studies in the pigeon (Columba livia) and Owl (Speotyto cunicularia). J. Comp. Neurol. 150: 253–278.
- Kitt, C. A. and S. E. Brauth (1982) A paleostriatal-thalamic-telencephalic path in pigeons. Neuroscience 11: 2735–2751.
- Krupa, M., E. Maire-Lepoivre, and M. Imbert (1984) Visual properties of neurons in the suprageniculate nucleus of the cat. Neurosci. Lett. 51: 13–18.
- Meier, R. E., J. Mihailovic, and M. Cuenod (1974) Thalamic Organization of the Retino-Thalamo-Hyperstriatal pathway in the Pigeon (Colum'ba livia). Exp. Brain Res. 19: 351–364.
- Mesulam, M. M. (1978) Tetramethyl benzidine for horseradish peroxidase histochemistry: A non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J. Histochem. Cytochem. 26: 106–117.
- Micelli, D., J. Peyrichoux, and J. Repérant (1975) The retino-thalamo-hyperstriatal pathway in the pigeon (Columba livia). Brain Res. 100: 125–131.
- Micelli, D., J. Peyrichoux, J. Repérant, and C. Weidner (1980) Etude anatomique des afferences du telencephale rostral chez le poussin de Gallus domesticus L. J. Hirnforsch. 21: 627–646.
- Pritz, M. B. (1975) Anatomical identification of a telencephalic visual area in crocodiles: Ascending connections of nucleus rotundus in Caiman crocodilus. J. Comp. Neurol. 164: 323–338.
- Pritz, M. B. and R. G. Northcutt (1980) Anatomical evidence for an ascending somatosensory pathway to the telencephalon in crocodiles, (Caiman crocodilus). Exp. Brain Res. 40: 342–345.
- Raczkowski, D. and A. C. Rosenquist (1983) Connections of the multiple visual cortical areas with the lateral posterior-pulvinar complex and adjacent thalamic nuclei in the cat. J. Neurosci. 3: 1912–1942.
- Reiner, A. and H. J. Karten (1982) Laminar distribution of the cells of origin of the descending tectofugal pathways in the pigeon (Columba livia). J. Comp. Neurol. 204: 165–187.
- Repérant, J. (1973) Nouvelles donnees sur les projections visuelles chez le Pigeon (Columba livia). J. Hirnforsch. 14: 151–187.
- Ritchie, T. C. and D. H. Cohen (1977) The avian tectofugal visual pathway: Projections of its telencephalon target ectostriatal complex. Soc. Neurosci. Abstr. 3: 94.
- Ulinski, P. S. (1983) Dorsal Ventricular Ridge: A Treatise on Forebrain Organization in Reptiles and Birds. New York: John Wiley and Sons.
- Wall, J. T., C. M. Gibbs, J. L. Broyles and D. H. Cohen (1985) Modification of neuronal discharge along the ascending tectofugal pathway during conditioning. Brain Res. 342: 67–76.
- Watanabe, M., H. Ito, and M. Ikushima (1985) Cytoarchitecture and ultrastructure of the avian ectostriatum: afferent terminals from the dorsal telencephalon and some nuclei of the thalamus. J. Comp. Neurol. 236: 241–257.
- Wild, J. M. (1983) Connectional anatomy of the somatosensory system of the pigeon. Soc. Neurosci. Abstr. 9: 244.