Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-26T16:07:31.810Z Has data issue: false hasContentIssue false

The histaminergic innervation of the lateral geniculate complex in the cat

Published online by Cambridge University Press:  02 June 2009

Daniel J. Uhlrich
Affiliation:
Department of Anatomy, University of Wisconsin Medical School, Madison
Karen A. Manning
Affiliation:
Department of Anatomy, University of Wisconsin Medical School, Madison
Thomas P. Pienkowski
Affiliation:
Department of Anatomy, University of Wisconsin Medical School, Madison

Abstract

The histaminergic innervation of the thalamic dorsal and ventral lateral geniculate nuclei and the perigeniculate nucleus of the cat was examined immunohistochemically by means of an antibody to histamine.

We find histamine-immunoreactive neurons in the cat brain are concentrated in the ventrolateral portion of the posterior hypothalamus, confirming a previous report. However, this cell group also spreads into medial, dorsal, and extreme lateral regions of the posterior hypothalamus and extends as far rostral as the optic chiasm.

Histamine-labeled fibers cover all regions of the lateral geniculate complex, but the density of labeling varies. The ventral lateral geniculate nucleus (vLGN) is most densely labeled, the A laminae of the dorsal lateral geniculate are sparsely labeled, and the geniculate C laminae and the perigeniculate nucleus show intermediate amounts of label. Thus, histaminergic fibers demonstrate a predilection for zones innervated by the W-cell system. Labeled fibers exhibit few branchings and numerous en passant swellings, lending a beaded appearance. The vLGN showed more instances of fibers with larger-sized swellings (up to 2 μm).

Following injections of biotinylated tracers into the hypothalamus, we find labeled fibers throughout the lateral geniculate complex. The anterogradely labeled fibers resemblethe histaminergic fibers in morphology, distribution, and relative bouton size. Thus, the hypothalamus appears to be the source of the histaminergic fibers in the lateral geniculate complex.

Histamine-labeled fibers in the dorsal lateral geniculate nucleus (dLGN) exhibit uncommon ultrastructural morphology. Many extremely large, round, or elliptical vesicles fill the fiber swellings. Swellings are directly apposed to a variety of other dendritic and axonal profiles, but thus far no convincing synaptic contacts have been seen. The distribution and appearance of these histaminergic fibers resembles those reported for serotonergic fibers.

Our results support the idea that histamine works nonsynaptically as a neuromodulator in the lateral geniculate complex, affecting the level of visual arousal.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

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

Airaksinen, M.S., Flugge, G., Fuchs, E. & Panula, P. (1989). Histaminergic system in the tree shrew brain. Journal of Comparative Neurology 286, 289310CrossRefGoogle ScholarPubMed
Airaksinen, M.S. & Panula, P. (1988). The histaminergic system in the guinea pig central nervous system: An immunocytochemical mapping study using an antiserum against histamine. Journal of Comparative Neurology 273, 163186CrossRefGoogle ScholarPubMed
Berman, A.L. & Jones, E.G. (1982). The Thalamus and Basal Telencephalon of the Cat. A Cytoarchitectonic Atlas with Stereotaxic Co-ordinates. Madison, Wisconsin: The University of Wisconsin Press.Google Scholar
Bleier, R. (1961). The Hypothalamus of the Cat. Baltimore, Maryland: The Johns Hopkins Press.Google Scholar
Bouthenet, M.L., Ruat, M., Sales, N., Garbarg, M. & Schwartz, J.C. (1988). A detailed mapping of histamine H1-receptors in guinea-pig central nervous system established by autoradiography with [125I]iodobolpyramine. Neuroscience 26, 553600CrossRefGoogle ScholarPubMed
Burke, W. & Cole, A.M. (1978). Extraretinal influences on the lateral geniculate nucleus. Reviews of Physiology, Biochemistry, and Pharmacology 80, 105166CrossRefGoogle ScholarPubMed
Cucchiaro, J.B., Uhlrich, D.J. & Sherman, S.M. (1988). Brainstem innervation to the cat’s lateral geniculate nucleus: An electron microscopic study using the tracer Phaseolus vulgaris leucoagglutinin (PHA-L). Journal of Neuroscience 8, 45764588CrossRefGoogle Scholar
DeLima, A.D. & Singer, W. (1987). The serotonergic fibers in the dorsal lateral geniculate nucleus of the cat: Distribution and synaptic connections demonstrated with immunocytochemistry. Journal of Comparative Neurology 258, 339351CrossRefGoogle Scholar
Eldred, W.D., Zucker, C., Karten, H.J. & Yazulla, S. (1983). Comparison of fixation and penetration enhancement techniques for use in ultrastructural immunocytochemistry. Journal of Hislochemistry and Cytochemistry 31, 285292CrossRefGoogle ScholarPubMed
Ericson, H., Watanabe, T. & Köhler, C. (1987). Morphological analysis of the tuberomammillary nucleus in the rat brain: Delineation of subgroups with antibody against L-histidine decarboxylase as a marker. Journal of Comparative Neurology 229, 233241Google Scholar
Fink, K., Schlicker, E., Neise, A. & Göthert, M. (1990). Involvement of presynaptic H3 receptors in the inhibitory effect of histamine on serotonin release in the rat brain cortex. Archives of Pharmacology 342, 513519CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Diamond, I.R. & Raczkowski, D. (1989). Cholinergic and monoaminergic innervation of the cat’s thalamus: Comparison of the lateral geniculate nucleus with other principal sensory nuclei. Journal of Comparative Neurology 288, 647675CrossRefGoogle ScholarPubMed
Foote, W.E., Maciewicz, R.J. & Mordes, J.P. (1974). Effect of mid-brain raphe and lateral mesencephalic stimulation on spontaneous and evoked activity in the lateral geniculate of the cat. Experimental Brain Research 19, 124130CrossRefGoogle ScholarPubMed
Guillery, R.W. (1969 a). The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat. Zeitschrift fur Zellforschung und Mikroskopische Anatomie 96, 138CrossRefGoogle ScholarPubMed
Guillery, R.W. (1969 b). A quantitative study of Golgi preparations from the dorsal lateral geniculate nucleus of the adult cat. Zeitschrift fur Zellforschung und Mikroskopische Anatomie 96, 3948CrossRefGoogle Scholar
Guillery, R.W. (1971). Patterns of synaptic interconnections in the dorsal lateral geniculate nucleus of cat and monkey: A brief review. Vision Research (Suppl.) 3, 211227CrossRefGoogle Scholar
Gunluk, A.E., Bickford, M.E., Guido, W. & Sherman, S.M. (1992). A nitric oxide synthetase colocalizes with ACh in brainstem inputs to the cat’s LGN. Society for Neuroscience Abstracts 212.Google Scholar
Hayashi, H., Takagi, H., Takeda, N., Kubota, Y., Tohyama, M., Watanabe, T. & Wada, H. (1984). Fine structure of histaminergic neurons in the caudal magnocellular nucleus of the rat as demonstrated by immunocytochemistry using histidine decarboxylase as a marker. Journal of Comparative Neurology 229, 233241CrossRefGoogle ScholarPubMed
Hough, L.B. & Green, J.P.(1984). Histamine and its receptors in the nervous system. In Handbook of Neurochemistry, Vol. 6. Receptors in the Nervous System, ed. Lajtha, A., pp. 145211. New York: Plenum Press.CrossRefGoogle Scholar
Inagaki, N., Panula, P., Yamatodani, A. & Wada, H. (1990). Organization of the histaminergic system in the brain of the turtle Chinemys reevesii. Journal of Comparative Neurology 297, 132140CrossRefGoogle ScholarPubMed
Inagaki, N., Yamatodani, A., Ando-Yamamoto, M., Tohyama, M., Watanabe, T. & Wada, H. (1988). Organization of histaminergic fibers in the rat brain. Journal of Comparative Neurology 273, 283300CrossRefGoogle ScholarPubMed
Kemp, J.A., Roberts, H.C. & Sillito, A.M. (1982). Further studies on the action of 5-hydroxy-tryptamine in the dorsal lateral geniculate nucleus of the cat. Brain Research 246, 334337CrossRefGoogle ScholarPubMed
Köhler, C., Swanson, L.W., Haglund, L. & Wu, J.-Y. (1985). The cytoarchitecture, histochemistry and projections of the tuberomam-millary nucleus in the rat. Neuroscience 16, 85110CrossRefGoogle ScholarPubMed
Lin, J.-S., Luppi, P.-H., Salvert, D., Sakai, K. & Jouvet, M. (1986). Neurones immunoréactifs à l’histamine dans l’hypothalamus chez le chat. Comptes Rendu Academie des Sciences (Paris) 303, 371376Google Scholar
Lin, J.-S., Sakai, K. & Jouvet, M. (1988). Evidence for histaminergic arousal mechanisms in the hypothalamus of cat. Neuropharmacology 27, 111122CrossRefGoogle ScholarPubMed
Maley, B.E., Engle, M.G., Humphreys, S., Vascik, D.A., Howes, K.A., Newton, B.W. & Elde, R.P. (1990). Monoamine synaptic structure and localization in the central nervous system. Journal of Electron Microscopy Technique 15, 2033CrossRefGoogle ScholarPubMed
McCormick, D.A. (1989). Cholinergic and noradrenergic modulation of thalamocortical processing. Trends in Neuroscience 12, 215221CrossRefGoogle ScholarPubMed
McCormick, D.A. & Pape, H.-C. (1990). Noradrenergic and serotonergic modulation of a hyperpolarization-activated cation current in thalamic relay neurones. Journal of Physiology 431, 319342CrossRefGoogle ScholarPubMed
McCormick, D.A. & Williamson, A. (1991). Modulation of neuronal firing mode in cat and guinea pig LGNd by histamine: Possible cellular mechanisms of histaminergic control of arousal. Journal of Neuroscience 11, 31883199CrossRefGoogle Scholar
Mize, R.R. & Horner, L.H. (1989). Origin, distribution, and morphology of serotonergic afferents to the cat superior colliculus: A light and electron microscope immunocytochemistry study. Experimental Brain Research 75, 8398CrossRefGoogle Scholar
Mize, R.R. & Payne, M.P. (1987). The innervation density of serotonergic (5-HT) fibers varies in different subdivision of the cat lateral geniculate nucleus complex. Neuroscience Letters 82, 133139CrossRefGoogle ScholarPubMed
Mizuguchi, H., Fukui, H., Yabumoto, M. & Wada, H. (1991). Synaptic and extra-synaptic distribution of histamine H1-receptors in rat and guinea pig brains. Biochemical and Biophysical Research Communications 174, 10431047CrossRefGoogle ScholarPubMed
Morgan, L.O. (1930). The cell groups of the tuber cinereum of the dog with a discussion of their function. Journal of Comparative Neurology 51, 271297CrossRefGoogle Scholar
Panula, P., Airaksinen, M.S., Pirvola, U. & Kotilatnen, E. (1990). A histamine-containing neuronal system in human brain. Neuroscience 34, 127132CrossRefGoogle ScholarPubMed
Panula, P., Häppölä, O., Airaksinen, M.S., Auvinen, S. & Virkamäki, A. (1988). Carbodiimide as a tissue fixative in histamine immunohistochemistry and its application in developmental neurobiology. Journal of Histochemistry and Cytochemistry 36, 259269CrossRefGoogle ScholarPubMed
Panula, P., Pirvola, U., Auvinen, S. & Airaksinen, M.S. (1989). Histamine-immunoreactive nerve fibers in the rat brain. Neuroscience 28, 585610CrossRefGoogle ScholarPubMed
Panula, P., Yang, H.-Y.T. & Costa, E. (1984). Histamine containing neurons in the rat hypothalamus. Proceedings of the National Academy of Sciences of the U.S.A. 81, 25722576CrossRefGoogle ScholarPubMed
Reiner, P.B. & McGeer, E.G. (1987). Electrophysiological properties of cortically projecting histamine neurons of the rat hypothalamus. Neuroscience Letters 73, 4347CrossRefGoogle ScholarPubMed
Ruat, M., Traiffort, E., Bouthenet, M.L., Schwartz, J.C., Hirschfeld, J., Buschauer, A. & Schunack, W.(1990). Reversible and irreversible labeling and autoradiographic localization of the cerebral histamine H2-receptor using [125I]iodinated probes. Proceedings of the National Academy of Sciences of the U.S.A. 87, 16581662CrossRefGoogle ScholarPubMed
Sakai, K., Leger, L., Salvert, D., Touret, M. & Jouvet, M. (1975). Mise en évidence d’une projection directe des aires hypothalamiques vers le corps genouillé latéral et le cortex visuel chez le chat par la technique de peroxydase. Experientia 31, 13501352CrossRefGoogle Scholar
Schwartz, J.-C, Arrang, J.-M., Garbarg, M., Pollard, H. & Ruat, M. (1991). Histaminergic transmission in the mammalian brain. Physiological Reviews 71, 151CrossRefGoogle ScholarPubMed
Schwartz, J.-C, Barbin, G., Duchemin, A.-M., Garbarg, M., Llorens, C., Pollard, H., Quach, T.T. & Rose, C. (1982). Histamine receptors in the brain and their possible functions. In Pharmacology of Histamine Receptors, ed. Gannellin, C.R. & Parsons, M.E., pp. 351391. Bristol, England: Wright.CrossRefGoogle Scholar
Sherman, S.M. & Koch, C. (1986). The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus. Experimental Brain Research 63, 120CrossRefGoogle ScholarPubMed
Singer, W. (1977). Control of thalamic transmission by corticofugal and ascending reticular pathways in the visual system. Physiological Reviews 57, 386420CrossRefGoogle ScholarPubMed
Smits, R.P.J.M., Steinbusch, H.W.M. & Mulder, A.H.(1990). The localization of histidine decarboxylase-immunoreactive cell bodies in the guinea-pig brain. Journal of Chemical Neuroanatomy 3, 85100Google ScholarPubMed
Staines, W.A., Daddona, P.E. & Nagy, J.I. (1987). The organization and hypothalamic projections of the tuberomammillary nucleus in the rat: An immunohistochemical study of adenosine deaminase-positiveneurons and fibers. Neuroscience 23, 571596CrossRefGoogle ScholarPubMed
Steriade, M. & Deschênes, M. (1984). The thalamus as a neuronal oscillator. Brain Research Reviews 8, 163CrossRefGoogle Scholar
Steriade, M. & Llinas, R. (1988). The functional states of the thalamus and the associated neuronal interplay. Physiological Reviews 68, 649742CrossRefGoogle ScholarPubMed
Takagi, H., Morishima, Y., Matsuyama, T., Hayashi, H., Watanabe, T. & Wada, H. (1986). Histaminergic axons in the neostriatum and cerebral cortex of the rat: A correlated light and electron microscopic immunocytochemical study using histidine decarboxylase as a marker. Brain Research 364, 114123CrossRefGoogle Scholar
Takeda, N., Inagaki, S., Taguchi, Y., Tohyama, M., Watanabe, T. & Wada, H. (1984). Origins of histamine-containing fibers in the cerebral cortex of rats studied by immunohistochemistry with histidine decarboxylase as a marker and transection. Brain Research 323, 5563CrossRefGoogle ScholarPubMed
Uhlrich, D.J. & Cucchiaro, J.B. (1992). GABAergic circuits in the lateral geniculate nucleus of the cat. In Progress in Brain Research, Vol. 90, ed. Mize, R.R., Marc, R.E. & Sillito, A.M., pp. 171192. Amsterdam: Elsevier.Google Scholar
Vanni-Mercier, G., Sakai, K. & Jouvet, M. (1984). Neurones spécifiques de l’éveil dans l’hypothalamus postérieu du chat. Comptes Rendu Acadamie des Sciences (Paris) 298, 195200Google Scholar
Wilson, J.R., Friedlander, M.J. & Sherman, S.M. (1984). Fine structural morphology of identified X- and Y-cells in the cat’s lateral geniculate nucleus. Proceedings of the Royal Society B (London) 221, 411436Google ScholarPubMed
Wilson, J.R. & Hendrickson, A.E. (1988). Serotonergic axons in the monkey’s lateral geniculate nucleus. Visual Neuroscience 1, 125133CrossRefGoogle ScholarPubMed
Wouterlood, F.G., Sauren, Y.M.H.F. & Steinbusch, H.W.M. (1986). Histaminergic neurons in the rat brain: Correlative immunocytochemistry, Golgi impregnation, and electron microscopy. Journal of Comparative Neurology 252, 227244CrossRefGoogle ScholarPubMed