Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-23T05:20:24.076Z Has data issue: false hasContentIssue false
  • English
  • Français

Organization of the hamster intergeniculate leaflet: NPY and ENK projections to the suprachiasmatic nucleus, intergeniculate leaflet and posterior limitans nucleus

Published online by Cambridge University Press:  02 June 2009

Lawrence P. Morin  and
J. Blanchard
Lawrence P. Morin
Affiliation:
Department of Psychiatry, Health Sciences Center, University at Stony Brook, New York
J. Blanchard
Affiliation:
Department of Psychiatry, Health Sciences Center, University at Stony Brook, New York
Get access Rights & Permissions [Opens in a new window]

Abstract

The intergeniculate leaflet (IGL) is an integral part of the circadian visual system. It receives direct retinal input and relays photic information to the circadian clock in the suprachiasmatic nucleus (SCN) through a geniculohypothalamic tract (GHT). In both rat and hamster, neuropeptide Y immunoreactive (NPY-IR) IGL cells project through the GHT to the SCN. However, the hamster GHT also contains enkephalin-IR (ENK-IR) fibers, presumably of IGL origin. In the present investigations, the IGL was examined for NPY-, ENK-, or dual-IR cells. Their projections to the SCN, contralateral IGL and pretectum were also studied. The results show that the hamster IGL contains both NPY- and ENK-IR neurons and that about 50% of these are immunoreactive to both peptides. Double-label retrograde analysis indicates that cells of each peptide class project to the SCN. Similarly, IGL neurons, many of which are NPY- and ENK-IR, project to the pretectum, particularly the posterior limitans nucleus. While numerous IGL neurons project contralaterally, very few are NPY- or ENK-IR.The distribution of SCN- and pretectum-projecting cells, in conjunction with the distribution of peptide-IR neurons, allows expansion of the IGL definition to include the region medial to the ventral lateral geniculate nucleus (VLG). The VLG is ventrolateral to the IGL and does not contain either neurons projecting to the SCN nor NPY- or ENK-IR cells, but does have numerous neurons projecting to the pretectum. The results substantiate and expand the previous definition of the hamster IGL, elaborate the species difference in IGL organization, and demonstrate the increased breadth of the circadian visual system.

Keywords

Intergeniculate leafletSuprachiasmatic nucleusPosterior limitans nucleusCircadianEfferentHamsterNeuropeptide YEnkephalinRetrograde tracing
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 1 , January 1995 , pp. 57 - 67
Copyright
Copyright © Cambridge University Press 1995

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., Leeman, S.E. & Goldman, B.D. (1984). Avian pancreatic polypeptide phase shifts hamster circadian rhythms when microinjected into the suprachiasmatic region. Science 223, 833–835.CrossRefGoogle ScholarPubMed
Albers, H.E. & Ferris, C.F. (1984). Neuropeptide Y: Role in lightdark entrainment of hamster circadian rhythms. Neuroscience Letters 50, 163–168.CrossRefGoogle ScholarPubMed
Botchkina, G.I. & Morln, L.P. (1994). Specialized neuronal and glial contributions to development of the hamster lateral geniculate complex and circadian visual system. Journal of Neuroscience (in press).Google Scholar
Cadusseau, J. & Roger, M. (1991). Cortical and subcortical connections of the pars compacta of the anterior pretectal nucleus in the rat. Neuroscience Research 12, 83–100.CrossRefGoogle ScholarPubMed
Card, J.P., Whealy, M.E., Robbins, A.K., Moore, R.Y. & Enquist, A.K. (1991). Two α-herpesvirus strains are transported differentially in the rodent visual system. Neuron 6, 957–969.CrossRefGoogle ScholarPubMed
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, 390–396.CrossRefGoogle Scholar
Card, J.P. & Moore, R.Y. (1989). Organization of lateral geniculate-hypothalamic connections in the rat. Journal of Comparative Neurology 284, 135–147.CrossRefGoogle ScholarPubMed
Card, J.P. & Moore, R.Y. (1991). The organization of visual circuits influencing the circadian activity of the suprachiasmatic nucleus. In Suprachiasmatic Nucleus, ed. Klein, D.C., Moore, R.Y. & Reppert, S.M., pp. 51–106. New York: Oxford University Press.Google Scholar
Conley, M. & Friederich-Ecsy, B. (1993). Functional organization of the ventral lateral geniculate complex of the tree shrew (Tupaia belangeri): II. Connections with the cortex, thalamus, and brainstem. Journal of Comparative Neurology 328, 21–42.CrossRefGoogle ScholarPubMed
Decavel, C. & Van Den Pol, A.N. (1990). GABA: A dominant neuro-transmitter in the hypothalamus. Journal of Comparative Neurology 302, 1019–1037.CrossRefGoogle Scholar
Frost, D.O., So, K.-F. & Schneider, G.E. (1979). Postnatal development of retinal projections in Syrian hamsters: A study using auto-radiographic and anterograde degeneration techniques. Neuroscience 4, 1649–1677.CrossRefGoogle 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, 198–200.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, 275–282.CrossRefGoogle Scholar
Harrington, M.E. & Rusak, B. (1986). Lesions of the thalamic inter-geniculate leaflet alter hamster circadian rhythms. Journal of Biological Rhythms 1, 309–325.CrossRefGoogle Scholar
Hickey, T.L. & Spear, P.D. (1976). Retinogeniculate projections in hooded and albino rats: An autoradiographic study. Experimental Brain Research 24, 523–529.CrossRefGoogle ScholarPubMed
Hsu, S.-M., Raine, L. & Fanger, H. (1981). Use of avidin-biotin-perioxidase complex (ABC) in immunoperioxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. Journal of Histochemistry and Cytochemistry 29, 577–580.CrossRefGoogle Scholar
Johnson, R.F., Smale, L., Moore, R.Y. & Morin, L.P. (1988). Lateral geniculate lesions block circadian phase shift responses to a benzodiazepine. Proceedings of the National Academy of Sciences of the U.S.A. 85, 5301–5304.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, 411–422.CrossRefGoogle ScholarPubMed
Kalsbeek, A., Teclemariam-Mesbah, R. & Pevet, P. (1993). Efferent projections of the suprachiasmatic nucleus in the golden hamster (Mesocricetus auratus). Journal of Comparative Neurology 332, 293–314.CrossRefGoogle ScholarPubMed
Ledoux, J.E., Ruggiero, D.A., Forest, R., Stornetta, R. & Reis, D.J. (1987). Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat. Journal of Comparative Neurology 264, 123–146.CrossRefGoogle Scholar
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, 1626–1638.CrossRefGoogle ScholarPubMed
McLean, I.W. & Nakane, P.K. (1974). Periodate-lysine-paraformalde-hyde fixative: A new fixative for immunoelectron microscopy. Journal of Histochemistry and Cytochemistry 22, 1077–1083.CrossRefGoogle ScholarPubMed
Michels, K.M., Morin, L.P. & Moore, R.Y. (1990). GABAA/benzo-diazepine receptor localization in the circadian timing system. Brain Research 531, 16–24.CrossRefGoogle Scholar
Mikkelsen, J.D. (1990). A neuronal projection from the lateral geniculate nucleus to the lateral hypothalamus of the rat demonstrated with Phaseolus vulgaris leucoagglutinin tracing. Neuroscience Letters 116, 58–63.CrossRefGoogle Scholar
Mikkelsen, J.D., Cozzi, B. & Moixer, M. (1991). Efferent projections from the lateral beniculate nucleus to the pineal complex of the Mongolian gerbil (Meriones unguiculatus). Cell Tissue Research 264, 95–102.CrossRefGoogle Scholar
Mikkelsen, J.D. (1992). The organization of the crossed geniculogeniculate pathway of the rat: A Phaseolus vulgaris-leucoagglutinin study. Neuroscience 48, 953–962.Google Scholar
Mikkelsen, J.D. & Moller, M. (1990). A direct neural projection from the intergeniculate leaflet of the lateral geniculate nucleus to the deep pineal gland of the rat, demonstrated with Phaseolus vulgaris leu-coagglutinin. Brain Research 520, 342–346.CrossRefGoogle Scholar
Moore, R.Y. & Speh, J.C. (1993). GABA is the principal neurotrans-mitter of the circadian system. Neuroscience Letters 150, 112–116.CrossRefGoogle Scholar
Morin, L.P., Johnson, R.F. & Moore, R.Y. (1989). Two brain nuclei regulating circadian rhythms are identified by GFAP immunoreactivity in hamsters and rats. Neuroscience Letters 99, 55–60.CrossRefGoogle ScholarPubMed
Morin, L.P., Blanchard, J.H. & Moore, R.Y. (1992). Intergeniculate leaflet and suprachiasmatic nucleus organization and connections in the hamster. Visual Neuroscience 8, 219–230.CrossRefGoogle ScholarPubMed
Morin, L.P. (1994). The circadian visual system. Brain Research Review 67, 102–127.CrossRefGoogle Scholar
Morin, L.P., Goodless-Sanchez, N., Smale, L. & Moore, R.Y. (1994). Projections of the suprachiasmatic nuclei, subparaventricular zone and retrochiasmatic area in the golden hamster. Neuroscience 61, 391–410.CrossRefGoogle ScholarPubMed
Park, H.T., Baek, S.Y., Kim, B.S., Kim, J.B. & Kim, J.J. (1993). Calcitonin gene-related peptide-like immunoreactive (CGRPI) elements in the circadian system of the mouse: An immunohistochemistry combined with retrograde transport study. Brain Research 629, 335–341.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, 35–56.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, 151–154.CrossRefGoogle ScholarPubMed
Radel, J.D., Hankin, M.H. & Lund, R.D. (1990). Proximity as a factor in the innervation of host brain regions by retinal transplants. Journal of Comparative Neurology 300, 211–229.CrossRefGoogle ScholarPubMed
Ralph, M.R., Foster, R.G., Davis, F.C. & Menaker, M. (1990). Transplanted suprachiasmatic nucleus determines circadian period. Science 247, 975–978.CrossRefGoogle ScholarPubMed
Ritter, S. & Dinh, T.T. (1992). Age-related changes in capsaicin-induced degeneration in rat brain. Journal of Comparative Neurology 318, 103–116.Google 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, 145–164.CrossRefGoogle Scholar
Rusak, B., Meuer, J.H. & Harrington, M.E. (1989). Hamster circadian rhythms are phase-shifted by electrical stimulation of the geniculo-hypothalamic tract. Brain Research 493, 283–291.CrossRefGoogle ScholarPubMed
Schmued, L.C. & Fallon, J.H. (1986). Fluoro-Gold: A new fluorescent retrograde axonal tracer with numerous unique properties. Brain Research 377, 147–154.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 563, 77–86.CrossRefGoogle ScholarPubMed
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, 1583–1586.Google ScholarPubMed
Swanson, L.W., Simmons, D.M., Whiting, P.J. & Lindstrom, J. (1987). Immunohistochemical localization of neuronal nicotinic receptors in the rodent central nervous system. Journal of Neuroscience 7, 3334–3342.CrossRefGoogle ScholarPubMed
Taylor, A.M., Jeffery, G. & Lieberman, A.R. (1986). Subcortical afferent and efferent connections of the superior colliculus in the rat and comparisons between albino and pigmented strains. Experimental Brain Research 62, 131–142.CrossRefGoogle ScholarPubMed
Watts, A.G., Swanson, L.W. & Sanchez-Watts, G. (1987). Efferent projections of the suprachiasmatic nucleus: I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin in the rat. Journal of Comparative Neurology 258, 204–229.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, 230–252.CrossRefGoogle ScholarPubMed
Weis, R.P., Speh, J.C. & Moore, R.Y. (1992). Efferent projections of the rat intergeniculate leaflet (IGL): A Phaseolus vulgaris leucoagglutinin (PHA-L) study. Society for Neuroscience Abstracts 18, 876.Google Scholar
Winer, J.A., Morest, D.K. & Diamond, I.T. (1988). A cytoarchitectonic atlas of the medial geniculate body of the opossum, Didelphys viginiana, with a comment on the posterior intralaminar nuclei of the thalamus. Journal of Comparative Neurology 274, 422–448.CrossRefGoogle Scholar
Winer, J.A. & Morest, D.K. (1983). The neuronal architecture of the dorsal division of the medial geniculate body of the cat. A study with the rapid Golgi method. Journal of Comparative Neurology 221, 1–30.CrossRefGoogle Scholar