Hostname: page-component-76fb5796d-25wd4 Total loading time: 0 Render date: 2024-04-27T03:20:08.869Z Has data issue: false hasContentIssue false

Intergeniculate leaflet and suprachiasmatic nucleus organization and connections in the golden hamster

Published online by Cambridge University Press:  02 June 2009

L.P. Morin
Affiliation:
Department of Psychiatry, State University of New York, Stony Brook
J. Blanchard
Affiliation:
Department of Psychiatry, State University of New York, Stony Brook
R.Y. Moore
Affiliation:
Departments of Psychiatry, Neurology and Behavioral Neuroscience, and the Center for Neuroscience, University of Pittsburgh, Pittsburgh

Abstract

The intergeniculate leaflet (IGL) is a distinct subdivision of the lateral geniculate complex which receives retinal input and projects upon a circadian pacemaker, the suprachiasmatic nucleus (SCN). In the present study, we have analyzed the organization of the IGL and its connections in the hamster, a species commonly used in circadian rhythm studies. The location of the IGL is defined by the presence of retinal afferents demonstrated by anterograde transport of cholera toxin-HRP, neuropeptide Y-containing neurons and axons, cells retrogradely labeled from the regions of the SCN and contralateral IGL, and substance P-containing axons. It is a long nucleus extending the entire rostrocaudal axis of the geniculate. The most rostral IGL lies between the lateral dorsal thalamus, ventrolateral part, and the horizontal cerebral fissure. It then enlarges ventral to the rostral dorsal lateral geniculate, medial to the optic tract. The mid-portion of the leaflet is a thin lamina intercalated between the dorsal and ventral geniculate nuclei. The extended caudal portion of the nucleus lies lateral and ventral to the medial geniculate and is contiguous with the zona incerta and the lateral terminal nucleus. The IGL contains populations of neuropeptide Y (NPY+) and enkephalin (ENK+) neurons which project to the retinorecipient portion of the SCN. In addition to the immunoreactive perikarya, the IGL contains plexuses of NPY+, ENK +, substance P-, serotonin-, and glutamic acid decarboxylase-immunoreactive axons.

Retrograde transport studies demonstrate that, in addition to the NPY+ neurons, there is a population of non-NPY+ neurons projecting upon the SCN. There is also a reciprocal projection upon the IGL from neurons in the SCN region, particularly the retrochiasmatic area. The hamster SCN differs from the rat in containing a distinct subdivision of substance P-immunoreactive neurons.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1992

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albers, H.E. & Ferris, C.F. (1984). Neuropeptide Y: role in light-dark entrainment of hamster circadian rhythms. Neuroscience Letters 50, 163168.CrossRefGoogle ScholarPubMed
Albers, H.E., Ferris, C.F., Leeman, S.E. & Goldman, B.D. (1984). Microinjection of neuropeptides into the suprachiasmatic region of the hypothalamus phase shifts circadian activity rhythms of Syrian hamsters. Science 223, 833835.CrossRefGoogle Scholar
Azmitia, E.C. & Segal, M. (1978). An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat Journal of Comparative Neurology 179, 641668.CrossRefGoogle ScholarPubMed
Belin, M.F., Nanopoulos, D., Didier, M., Aguera, M., Steinbusch, H., Verhofstad, A., Maitre, M. & Pujol, J.F. (1983). Immunohistochemical evidence for the presence of gamma-aminobutyric acid and serotonin in one nerve cell. A study on the raphe nuclei of the rat using antibodies to glutamate decarboxylase and serotonin. Brain Research 275, 329339.CrossRefGoogle ScholarPubMed
Bennett-Clarke, C., Mooney, R.D., Chiaia, N.L. & Rhoades, R.W. (1989). A substance P projection from the superior colliculus to the parabigeminal nucleus in the rat and hamster. Brain Research 500, 111.CrossRefGoogle Scholar
Card, J.P. & Moore, R.Y. (1982). Ventral lateral geniculate nucleus efferents to the rat suprachiasmatic nucleus exhibit avian pancreatic polypeptide-like immunoreactivity. Journal of Comparative Neurology 206, 390396.CrossRefGoogle Scholar
Card, J.P. & Moore, R.Y. (1984). The suprachiasmatic nucleus of the golden hamster: immunohistochemical analysis of cell and fiber distribution. Neuroscience 13, 390396.CrossRefGoogle ScholarPubMed
Card, J.P. & Moore, R.Y. (1989). Organization of lateral geniculatehypothalamic connections in the rat. Journal of Comparative Neurology 284, 135147.CrossRefGoogle ScholarPubMed
Cosenza, R.M. & Moore, R.Y. (1984). Afferent connections of the ventral lateral geniculate nucleus in the rat: an HRP study. Brain Research 310, 367370.CrossRefGoogle ScholarPubMed
Cropper, E.C.Eisenman, J.S. & Azmitia, E.C. (1984). An immunocytochemical study of the serotonergic innervation of the thalamus of the rat. Journal of Comparative Neurology 224, 3850.CrossRefGoogle ScholarPubMed
Eichler, V.B. & Moore, R.Y. (1974). The primary and accessory optic systems in the golden hamster, Mesocricetus auratus. Ada Anatomica 89, 359371.Google ScholarPubMed
Frost, D.O., So, K.-F. & Schneider, G.E. (1979). Postnatal development of retinal projections in Syrian hamsters: a study using autoradiographic and anterograde degeneration techniques. Neuroscience 4, 16491677.CrossRefGoogle ScholarPubMed
Goodless, N.L., Moore, R.Y. & Morin, L.P. (1989). The efferent projections of the hamster SCN revealed by PHA-L. Society for Neuroscience Abstracts 15, 1058.Google Scholar
Green, D.J. & Gillette, R. (1982). Circadian rhythms of firing rate recorded from single cells in the rat suprachiasmatic brain slice. Brain Research 245, 198200.CrossRefGoogle ScholarPubMed
Groos, G. & Hendriks, J. (1982). Circadian rhythms in electrical discharge of rat suprachiasmatic neurones recorded in vitro. Neuroscience Letters 34, 283288.CrossRefGoogle ScholarPubMed
Hamassaki, D.E. & Britto, L.R.G. (1990). Thalamic origin of neuropeptide Y innervation of the accessory optic nucleus of the pigeon (Columba livia). Visual Neuroscience 5, 249259.CrossRefGoogle ScholarPubMed
Harrington, M.E., Nance, D.M. & Rusak, B. (1985 ). Neuropeptide Y immunoreactivity in the hamster geniculo-suprachiasmatic tract. Brain Research Bulletin 15, 465472.CrossRefGoogle ScholarPubMed
Harrington, M.E. & Rusak, B. (1986). Lesions of the thalamic intergeniculate leaflet alter hamster circadian rhythms. Journal of Biological Rhythms 1, 309325.CrossRefGoogle ScholarPubMed
Harrington, M.E., Nance, D.M. & Rusak, B. (1987 ). Double-labeling of neuropeptide Y-immunoreactive neurons which project from the geniculate to the suprachiasmatic nuclei. Brain Research 410, 275282.CrossRefGoogle Scholar
Harrington, M.E. & Rusak, B. (1989). Photic responses of geniculohypothalamic tract neurons in the Syrian hamster. Visual Neuroscience 2, 367375.CrossRefGoogle ScholarPubMed
Hendrickson, A.E., Wagoner, N. & Cowan, W.M. (1972). An autoradiographic and electron microscopic study of retinohypothalamic connections. Zeitschrift für Zellforschung 135, 126.CrossRefGoogle Scholar
Hickey, T.L. & Spear, P.D. (1976). Retinogeniculate projections in hooded and albino rats: an autoradiographic study. Experimental Brain Research 24, 523529.CrossRefGoogle ScholarPubMed
Hsu, S.-M., Raine, L. & Fanger, H. (1981). Use of avidin-biotinperioxidase complex (ABC) in immunoperioxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. Journal of Histochemistry and Cytochemistry 29, 577580.CrossRefGoogle Scholar
Inouye, S.T. & Kawamura, H. (1979). Persistence of circadian rhythmicity in a mammalian hypothalamic “island” containing the suprachiasmatic nucleus. Proceedings of the National Academy of Sciences of the U.S.A. 76, 59625966.CrossRefGoogle Scholar
Johnson, R.F., Morin, L.P. & Moore, R.Y. (1988a). Retinohypothalamic projections in the hamster and rat demonstrated using cholera toxin. Brain Research 462, 301312.CrossRefGoogle ScholarPubMed
Johnson, R.F., Morin, L.P. & Moore, R.Y. (1988b). Loss of entrainment and anatomical plasticity after lesions of the hamster retinohypothalamic tract. Brain Research 460, 297313.CrossRefGoogle ScholarPubMed
Johnson, R.F., Smale, L., Moore, R.Y. & Morin, L.P. (1988c). Lateral geniculate lesions block circadian phase shift responses to a benzodiazepine. Proceedings of the National Academy of Sciences of the U.S.A. 85, 53015304.CrossRefGoogle ScholarPubMed
Johnson, R.F., Moore, R.Y. & Morin, L.P. (1989). Lateral geniculate lesions alter activity rhythms in the hamster. Brain Research Bulletin 22, 411422.CrossRefGoogle ScholarPubMed
Lehman, M.N., Silver, R., Gladstone, W.R., Kahn, R.M., Gibson, M. & Bittman, E.L. (1987). Circadian rhythmicity restored by neural transplant. Immunocytochemical characterization of the graft and its integration with the host brain. Journal of Neuroscience 7, 16261638.CrossRefGoogle ScholarPubMed
Mantyh, P.W. & Kemp, J.A. (1983). The distribution of putative neurotransmitters in the lateral geniculate nucleus of the rat. Brain Research 288, 344348.CrossRefGoogle ScholarPubMed
McLean, I.W. & Nakane, P.K. (1974). Periodate-lysine-paraformaldehyde fixative: a new fixative for immunoelectron microscopy. Journal of Histochemistry and Cytochemistry 22, 10771083.CrossRefGoogle ScholarPubMed
Mesulam, M. (1978). Tetramethyl benzidine for horseradish peroxidase neurochemistry: a non-carcinogenic blue reaction-product with superior sensitivity for visualizing neuronal afferents and efferents. Journal of Histochemistry and Cytochemistry 26, 106117.CrossRefGoogle Scholar
Michels, K.M., Morin, L.P. & Moore, R.Y. (1990). GABAA/benzodiazcpine Receptor Localization In The Circadian Timing System. Brain Research 531, 1624.CrossRefGoogle ScholarPubMed
Moore, R.Y. & Eichler, V.B. (1972). Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Research 42, 201206.CrossRefGoogle ScholarPubMed
Moore, R.Y., Halaris, A.E. & Jones, B.E. (1978 ). Serotonin neurons of the midbrain raphe: Ascending projections. Journal of Comparative Neurology 180, 417438.CrossRefGoogle ScholarPubMed
Moore, R.Y. & Lenn, N.J. (1972). A retinohypothalamic projection in the rat. Journal of Comparative Neurology 146, 114.CrossRefGoogle ScholarPubMed
Newman, G.C. & Hospod, F.E. (1986). Rhythm of suprachiasmatic nucleus 2-deoxyglucose uptake in vitro. Brain Research 381, 245250.CrossRefGoogle ScholarPubMed
Oertel, W.H., Schmechel, D.E., Mugnaini, E., Tappaz, M.L. & Kopin, I.J. (1981). Immunocytochemical localization of glutamate decarboxylase in rat cerebellum with a new antiserum. Neuroscience 6, 17151735.CrossRefGoogle ScholarPubMed
O'Hara, P.Y., Liberman, A.R., Hunt, S.P. & Wu, J.-Y. (1983). Neural elements containing glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the rat: immunohistochemical studies by light and electron microscopy. Neuroscience 8, 189211.CrossRefGoogle Scholar
Pickard, G.E. & Silverman, A.J. (1981). Direct retinal projections to hypothalamus piriform cortex and accessory optic nuclei in the golden hamster as demonstrated by a sensitive anterograde horse-radish peroxidase technique. Journal of Comparative Neurology 196, 155172.CrossRefGoogle Scholar
Pickard, G.E. (1982). The afferent connections of the suprachiasmatic nucleus of the golden hamster with emphasis on the retinohypothalamic projection. Journal of Comparative Neurology 211, 6583.CrossRefGoogle ScholarPubMed
Pickard, G.E., Ralph, M.R. & Menaker, M. (1987). The intergeniculate leaflet partially mediates effects of light on circadian rhythms. Journal of Biological Rhythms 2, 3556.CrossRefGoogle ScholarPubMed
Pickard, G.E. (1989). Entrainment of the circadian rhythm of wheel-running activity is phase shifted by ablation of the intergeniculate leaflet. Brain Research 494, 151154.CrossRefGoogle ScholarPubMed
Ralph, M.R. & Menaker, M. (1987). Bicuculline blocks circadian phase delays but not advances. Neurochemistry International 11, 5562.Google Scholar
Ralph, M.R. & Menaker, M. (1989). GABA regulation of circadian responses to light. 1. Involvement of GABAA-benzodiazepine and GABAB receptors. Journal of Neuroscience 9, 28582865.CrossRefGoogle Scholar
Ralph, M.R., Foster, R.G., Davis, F.C. & Menaker, M. (1990). Transplanted suprachiasmatic nucleus determines circadian periods. Science 247, 975978.CrossRefGoogle Scholar
Ribak, C.E. & Peters, A. (1975). An autoradiographic study of the projections from the lateral geniculate body of the rat. Brain Research 92, 341368.CrossRefGoogle ScholarPubMed
Rusak, B. (1977). The role of the suprachiasmatic nuclei in the generation of circadian rhythms in the golden hamster, Mesocricetus auratus. Journal of Comparative Physiology 118, 145164.CrossRefGoogle Scholar
Schmued, L.C. & Fallon, J.H. (1986). Fluoro-Gold: a new fluorescent retrograde axonal tracer with numerous unique properties. Brain Research (Abstract) 377, 147154.CrossRefGoogle ScholarPubMed
Shibata, S. & Moore, R.Y. (1988). Electrical and metabolic activity of suprachiasmatic nucleus neurons in hamster hypothalamic slices. Brain Research 438, 374378.CrossRefGoogle ScholarPubMed
Smale, L., Blanchard, J., Moore, R.Y. & Morin, L.P. (1991). Immunocytochemical characterization of the suprachiasmatic nucleus and the intergeniculate leaflet in the diurnal ground squirrel, Spermophilus lateralis. Brain Research (in press).CrossRefGoogle Scholar
Speh, J.C. & Moore, R.Y. (1989). Organization of the cat intergeniculate leaflet demonstrated by neuropeptide Y-immunoreactivity. Society for Neuroscience Abstracts 15, 727.Google Scholar
Stephan, F.K. & Zucker, I. (1972). Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proceedings of the National Academy of Sciences of the U.S.A. 69, 15831586.CrossRefGoogle ScholarPubMed
Swanson, L.W., Cowan, W.M. & Jones, E.G. (1974). An autoradiographic study of the efferent projections of the ventral lateral geniculate nucleus in the albino rat and cat. Journal of Comparative Neurology 156, 143164.CrossRefGoogle Scholar
Takatsuji, K. & Tohyama, M. (1989). The organization of the rat lateral geniculate body by immunohistochemical analysis of neuroactive substances. Brain Research 480, 198209.CrossRefGoogle ScholarPubMed
Terubayashi, H. & Fujisawa, H. (1984). The accessory optic system of rodents: a whole-mount HRP study. Journal of Comparative Neurology 227, 285295.CrossRefGoogle ScholarPubMed
Ueda, S., Kawata, M. & Sano, Y. (1983). Identification of serotonin and vasopressin immunoreactivities in the suprachiasmatic nucleus of four mammalian species. Cell and Tissue Research 234, 237248.CrossRefGoogle ScholarPubMed
Van De Kar, L.D. & Lorens, S.A. (1979). Differential serotonergic innervation of individual hypothalamic nuclei and other forebrain regions by the dorsal and median midbrain raphe nuclei. Brain Research 162, 4554.CrossRefGoogle ScholarPubMed
Van Den Pol, A.N. & Tsujimoto, K.L. (1985). Neurotransmitters of the hypothalamic suprachiasmatic nucleus: immunocytochemical analysis of 25 neuronal antigens. Neuroscience 15, 10491086.CrossRefGoogle ScholarPubMed
Watts, A.G. & Swanson, L.W. (1987). Efferent projections of the suprachiasmatic nucleus: II. Studies using retrograde transport of fluorescent dyes and simultaneous peptide immunohistochemistry in the rat. Journal of Comparative Neurology 258, 230252.CrossRefGoogle ScholarPubMed
Watts, A.G., Swanson, L.W. & Sanchez-Watts, G. (1987). Efferent projections of the suprachiasmatic nucleus: I. Studies using antero-grade transport of Phaseolus vulgaris leucoagglutinin in the rat. Journal of Comparative Neurology 258, 204229.CrossRefGoogle Scholar