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Afferent Connections of the Habenular Nuclei in the Rat. A Horseradish Peroxidase Study, with a Note on the Fiber-of-Passage Problem

  • Chapter
Neuroanatomy

Part of the book series: Contemporary Neuroscientists ((CN))

Abstract

The afferent connections of the habenular complex in the rat were examined by injecting horseradish peroxidase (HRP) into discrete portions of the habenular nuclei by microelectrophoresis.

  1. 1.

    HRP deposits confined to the lateral half of the lateral habenular nucleus labeled a multitude of cells in the entopeduncular nucleus. Numerous labeled cells also appeared in such cases in the lateral hypothalamus, indicating that the lateral habenular nucleus is a major convergence point of projections from these otherwise apparently quite separate cell regions. Moderate-to-small numbers of labeled cells were also found in the nuclei of the diagonal band, substantia innominata, lateral preoptic area and, more caudally, in the ventral tegmental area, the region of the mesencephalic raphe, and the central gray substance.

  2. 2.

    HRP injected into the medial part of the lateral habenular nucleus labeled cells in the same regions, but more in the diagonal band and fewer in the entopeduncular nucleus than were labeled by more lateral injections. The contrast suggests that the projections from the basal forebrain and entopeduncular nucleus to the lateral habenular nucleus are somewhat topographically organized.

  3. 3.

    Injections of the medial habenular nucleus labeled an abundance of cells in the posterior parts of the supracommissural septum, but also a small number of cells in the diagonal band and mesencephalic raphe.

  4. 4.

    HRP injected into the stria medullaris labeled cells in all of the afore-mentioned areas and, in addition, cells in several olfactory structures, confirming that HRP may be taken up by fibers of passage and label their cells of origin, and suggesting that olfactory structures contribute fibers to the stria medullaris that do not terminate in the habenula.

Supported by PHS Grants NS 06542 and MH 25515 and NIH Fellowship NS 02101.

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Literature Cited

  • Ariens Kappers, C. U., G. C. Huber and E. C. Crosby 1960 The Comparative Anatomy of the Nervous System of Vertebrates, Including Man. Hafher, New York. Vol. I, pp. 1101–1103.

    Google Scholar 

  • Ban, T., and K. Zyo 1962 Experimental studies on the fiber connections of the rhinencephalon. I. Albino rat. Med. J. Osaka Univ., 12: 385–424.

    Google Scholar 

  • Björklund, A., Ch. Owman and K. A. West 1972 Peripheral sympathetic innervation and serotonin cells in the habenular region of the rat brain. Z. Zellforsch., 127: 570–579.

    Article  Google Scholar 

  • Bobillier, P., F. Petitjean, D. Salvert, M. Ligier and S. Seguin 1975 Differential projections of the nucleus raphe dorsalis and nucleus raphe centralis as revealed by autoradiography. Brain Res., 85: 205–210.

    Article  Google Scholar 

  • Bunt, A. H., A. E. Hendrickson, J. S. Lund, R. D. Lund and A. F. Fuchs 1975 Monkey retinal ganglion cells: morphometric analysis and tracing of axonal projections with a consideration of the peroxidase technique. J. Comp. Neur., 164: 265–286.

    Article  Google Scholar 

  • Cajal, S. RamĂłn y 1911 Histologie du Système Nerveaux de l’Homme et des VertĂ©brĂ©s. Maloine, Paris. Vol. II, pp. 415–426.

    Google Scholar 

  • Colman, D. R., F. Scalia and E. Cabrales 1976 Light and electron microscopic observations on the anterograde transport of horseradish peroxidase in the optic pathway in the mouse and rat. Brain Res., 102: 156–163.

    Article  Google Scholar 

  • Conrad, L. C. A., C. M. Leonard and D. W. Pfaff 1974 Connections of the median and dorsal raphe nuclei in the rat: an autoradiographic and degeneration study. J. Comp. Neur., 165: 179–206.

    Article  Google Scholar 

  • Conrad, L. C. A., and D. W. Pfaff 1976a Autoradiographic tracing of nucleus accumbens efferents in the rat. Brain Res., 113: 589–596.

    Article  Google Scholar 

  • Conrad, L. C. A., and D. W. Pfaff 1976b Efferents from medial basal forebrain and hypothalamus in the rat. II. An autoradiographic study of the anterior hypothalamus. J. Comp. Neur., 169: 221–262.

    Article  Google Scholar 

  • Cowan, W. M., G. Raisman and T. P. S. Powell 1965 The connexions of the amygdala. J. Neur. Neu-rosurg. Psychiat, 28: 137–151.

    Article  Google Scholar 

  • Cragg, B. G. 1961 The connections of the habenula in the rabbit. Exp. Neur., 3: 388–409.

    Article  Google Scholar 

  • Crosby, E. C., T. Humphrey and E. W. Lauer 1962 Correlative Anatomy of the Nervous System. Macmillan, New York, pp. 271–273.

    Google Scholar 

  • DeOlmos, J. S. 1972 The amygdaloid projection field in the rat as studied with the cupricsilver method. In: Neurobiology of the Amygdala. B. E. Eleftheriou, ed. Plenum, New York, pp. 145–204.

    Chapter  Google Scholar 

  • DeOlmos, J. S., and W. R. Ingram 1972 The projection field of the stria terminalis in the rat brain. An experimental study. J. Comp. Neur., 146: 303–334.

    Article  Google Scholar 

  • DeVito, J. L., K. W. Clausing and O. A. Smith 1974 Uptake and transport of horseradish peroxidase by cut end of the vagus nerve. Brain Res., 82: 269–271.

    Article  Google Scholar 

  • Divac, I. 1975 Magnocellular nuclei of the basal forebrain project to neocortex, brain stem, and olfactory bulb. Review of some functional correlates. Brain Res., 93: 385–398.

    Article  Google Scholar 

  • Domesick, V. B. 1976 Projections of the nucleus of the diagonal band of Broca in the rat. Anat. Rec., 184: 391–392 (Abstract).

    Google Scholar 

  • Filion, M, C. Harnois and G. Guano 1976 Electrophysiological study of the distribution of axonal branches of individual entopeduncular neurons in the cat. Neurosci. Abstr., 2: 63 (Abstract).

    Google Scholar 

  • Fox, C. A., A. N. Andrade, I. J. LuQui and J. Rafols 1974 The primate globus pallidus: a Golgi and electron microscopic study. J. fur Hirnfforschung, 15: 75–93.

    Google Scholar 

  • Furstman, L., S. Saporta and L. Kruger 1975 Retrograde axonal transport of horseradish peroxidase in sensory nerves and ganglion cells of the rat. Brain Res., 84: 320–324.

    Article  Google Scholar 

  • Graham, R. C., Jr., and M. J. Karnnovsky 1966 The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J. Histochem. Cytochem., 14: 291–302.

    Article  Google Scholar 

  • Graybiel, A. M., and M. Devor 1974 A microelectro-phoretic delivery technique for use with horseradish peroxidase. Brain Res., 68: 167–173.

    Article  Google Scholar 

  • Guillery, R. W. 1957 Degeneration in the hypothalamic connexions of the albino rat. J. Anat. (London), 91: 91–115.

    Google Scholar 

  • Guillery, R. W. 1959 Afferent fibers to the dorso-medial thalamic nucleus in the cat. J. Ant. (London), 93: 403–419.

    Google Scholar 

  • Gurdjian, E. S. 1925 Olfactory connections of the albino rat, with special reference to the stria medul-laris and the anterior commissure. J. Comp. Neur., 38: 127–163.

    Article  Google Scholar 

  • Halperin, J. J., and J. H. LaVail 1975 A study of the dynamics of retrograde transport and accumulation of horseradish peroxidase in injured neurons. Brain Res., 100: 253–269.

    Article  Google Scholar 

  • Hamilton, B. L. 1973 Projections of the nuclei of the periaqueductal gray matter in the cat. J. Comp. Neur., 152: 45–58.

    Article  Google Scholar 

  • Heimer, L. 1972 The olfactory connections of the diencephalon in the rat. Brain, Behav. and Evol., 6: 484–523.

    Article  Google Scholar 

  • Heimer, L., and R. D. Wilson 1975 The subcortical projections of the allocortex: similarities in the neural associations of the hippocampus, the piriform cortex, and the neocortex. In: Golgi Centennial Symposium. Proceedings. M. Santini, ed. Raven, New York, pp. 177–193.

    Google Scholar 

  • Herrick, C. J. 1948 The Brain of the Tiger Salamander. Univ. Chicago Press, Chicago, pp. 247–264.

    Google Scholar 

  • Huang, Y. H., and G. J. Mogenson 1972 Neural pathways mediating drinking and feeding in rats. Exp. Neur., 37: 269–286.

    Article  Google Scholar 

  • Johnston, J. B. 1923 Further contributions to the study of the evolution of the forebrain. J. Comp. Neur., 35: 337–481.

    Article  Google Scholar 

  • Jones, E. G., H. Burton, C. B. Saper and L. W. Swanson 1976 Midbrain, diencephalic and cortical relationships of the basal nucleus of Meynert and associated structures in primates. J. Comp. Neur., 167: 385–420.

    Article  Google Scholar 

  • Jones, E. G., and R. Y. Leavitt 1974 Retrograde axonal transport and the demonstration of nonspecific projections to the cerebral cortex and striatum from thalamic intralaminar nuclei in the rat, cat and monkey. J. Comp. Neur., 154: 349–377.

    Article  Google Scholar 

  • Kizer, J. S., M. Palkovits and M. J. Brownstein 1976 The projections of the A8, A9 and A10 dopaminergic cell bodies: evidence for a nigral-hy-pothalamic-median eminence dopaminergic pathway. Brain Res., 108: 363–370.

    Article  Google Scholar 

  • König, J. F. R., and R. A. Klippel 1963 The Rat Brain. Krieger, Huntington, New York.

    Google Scholar 

  • Krettek, J. E., and J. L. Price 1974 A direct input from the amygdala to the thalamus and the cerebral cortex. Brain Res., 67: 169–174.

    Article  Google Scholar 

  • Kristensson, K., and Y. Olsson 1971 Retrograde axonal transport of protein. Brain Res., 29: 363–365.

    Article  Google Scholar 

  • Kristensson, K., and Y. Olsson 1974 Retrograde transport of horseradish peroxidase in transected axons. 1. Time relationships between transport and induction of chromatolysis. Brain Res., 79: 101–109.

    Article  Google Scholar 

  • Kuhar, M. J., G. K. Aghajanian and R. H. Roth 1972 Tryptophan hydroxylase activity and synaptosomal uptake of serotonin in discrete brain regions after midbrain raphe lesions: correlations with serotonin levels and histochemical fluorescence. Brain Res., 44: 165–176.

    Article  Google Scholar 

  • Kusama, T., and N. Hagino 1961 Medial forebrain bundle and stria medullaris in rabbits. Folia psy-chiat. neurol. jap., 15: 229–245.

    Google Scholar 

  • Kuypers, H. G. J. M, and V. A. Maisky 1975 Retrograde axonal transport of horseradish peroxidase from spinal cord to brain stem cell groups in the cat. Neurosci. Letters, 1: 9–14.

    Article  Google Scholar 

  • Laursen, A. M. 1955 An experimental study of pathways from the basal ganglia. J. Comp. Neur., 102: 1–25.

    Article  Google Scholar 

  • LaVail, J. H., and M. M. LaVail 1972 Retrograde axonal transport in the central nervous system. Science, 176: 1416–1418.

    Article  Google Scholar 

  • LaVail, J. H., and M. M. LaVail 1974 The retrograde intraaxonal transport of horseradish peroxidase in the chick visual system: a light and electron microscopic study. J. Comp. Neur., 157: 303–358.

    Article  Google Scholar 

  • LaVail, J. H., K. R. Winston and A. Tish 1973 A method based on retrograde intraaxonal transport of protein for identification of cell bodies of origin of axons terminating within the CNS. Brain Res., 58: 470–477.

    Article  Google Scholar 

  • Leonard, C.M., and J. W. Scott 1971 Origin and distribution of the amygdalofugal pathways in the rat: an experimental neuroanatomical study. J. Comp. Neur., 141: 313–330.

    Article  Google Scholar 

  • Marburg, O. 1944 The structure and fiber connections of the human habenula. J. Comp. Neur., 80: 211–234.

    Article  Google Scholar 

  • Massopust, L. C., Jr., and R. Thompson 1962 A new interpedunculo-diencephalic pathway in rats and cats. J. Comp. Neur., 118: 97–105.

    Article  Google Scholar 

  • Mulhouse, O. E. 1969 S Golgi study of the descending medial forebrain bundle. Brain Res., 15: 341–363.

    Article  Google Scholar 

  • Mitchell, R. 1963 Connections of the habenula and of the interpeduncular nucleus in the cat. J. Comp. Neur., 121: 441–457.

    Article  Google Scholar 

  • Mizuno, N., C. D. ClĂ©mente and E. K. Sauerland 1969 Fiber projections from rostral basal forebrain structures in the cat. Exp. Neur., 25:220–237.

    Article  Google Scholar 

  • Mok, A. C. S., and G. J. Mogenson 1974 Effects of electrical stimulation of the lateral hypothalamus, hippocampus, amygdala and olfactory bulb on unit activity of the lateral habenular nucleus in the rat. Brain Res., 77: 417–429.

    Article  Google Scholar 

  • Nauta, H. J. W. 1974 Evidence of a pallidohabenu-lar pathway in the cat. J. Comp. Neur., 156: 19–28.

    Article  Google Scholar 

  • Nauta, H. J. W., M. B. Pritz and R. J. Lasek 1974 AffĂ©rents to the rat caudoputamen studied with horseradish peroxidase. An evaluation of a retrograde neuroanatomical research method. Brain Res., 67: 219–238.

    Article  Google Scholar 

  • Nauta, W. J. H. 1956 An experimental study of the fornix system in the rat. J. Comp. Neur., 104: 247–271.

    Article  Google Scholar 

  • Nauta, W. J. H. 1958 Hippocampal projections and related neural pathways to the mid-brain in the cat. Brain, 81: 319–341.

    Article  Google Scholar 

  • Nauta, W. J. H. and W. Haymaker 1969 Hypothalamic nuclei and fiber connections. In: The Hypothalamus. W. Haymaker, E. Anderson and W. J. H. Nauta, eds. Thomas, Springfield, Ill., pp. 136–209.

    Google Scholar 

  • Nauta, W. J. H., and H. G. J. M. Kuypers 1958 Some ascending pathways in the brain stem reticular formation. In: Reticular Formation of the Brain. H. H. Jasper, L. D. Proctor, R. S. Knighton, W. G Noshay and R. T. Costello, eds. Little-Brown, Boston, pp. 3–30.

    Google Scholar 

  • Palkovits, M., and D. M. Jacobowitz 1974 Topographic atlas of catecholamine and acetylcholines-terase-containing neurons in the rat brain. II. Hind-brain (Mesencephalon, rhombencephalon). J. Comp. Neur., 157: 29–42.

    Article  Google Scholar 

  • Parent, A. 1976 Striatal afferent connections in the turtle (Chrysemys picta) as revealed by retrograde axonal transport of horseradish peroxidase. Brain Res., 108: 25–36.

    Article  Google Scholar 

  • Pierce, E. T., W. W. Foote and J. A. Hobson 1976 The efferent connection of the nucleus raphe dor-salis. Brain Res., 107: 137–144.

    Article  Google Scholar 

  • Powell, E. W. 1968 Septohabenular connections in the rat, cat and monkey. J. Comp. Neur., 134: 145–150.

    Article  Google Scholar 

  • Powell, E. W. and R. B. Leman 1976 Connections of the nucleus accumbens. Brain Res., 105: 389–403.

    Article  Google Scholar 

  • Powell, T. P. S., W. M. Cowan and G. Raisman 1965 The central olfactory connections. J. Anat (London), 99: 791–813.

    Google Scholar 

  • Price, J. L. and T. P. S. Powell 1970a An experimental study of the origin and the course of the centrifugal fibers to the olfactory bulb in the rat. J. Anat. (London), 107: 215–237.

    Google Scholar 

  • Price, J. L. and T. P. S. Powell 1970b The afferent connexions of the nucleus of the horizontal limb of the diagonal band. J. Anat. (London), 107: 239–256.

    Google Scholar 

  • Price, J. L. and T. P. S. Powell 1971 Certain observations on the olfactory pathway. J. Anat. (London), 110: 105–126.

    Google Scholar 

  • Raisman, G. 1966 The connexions of the septum. Brain, 89: 317–348.

    Article  Google Scholar 

  • Raisman, G., W. M. Cowan and T. P. S. Powell 1966 An experimental analysis of the efferent projections of the hippocampus. Brain, 89: 83–108.

    Article  Google Scholar 

  • Scalia, F., and D. R. Colman 1974 Aspects of the central projection of the optic nerve in the frog as revealed by anterograde migration of horseradish peroxidase. Brain Res., 79: 496–504.

    Article  Google Scholar 

  • Smaha, L. A., and W. W. Kaelber 1973 Efferent fiber projections of the habenula and the interpeduncular nucleus. An experimental study in the opossum and cat. Exp. Brain Res., 16: 291–308.

    Article  Google Scholar 

  • Sprague, J. M., and M. Meyer 1950 An experimental study of the fornix in the rabbit. J. Anat. (London), 84: 354–368.

    Google Scholar 

  • Swanson, L. W. 1976 An autoradiographic study of the efferent connections of the preoptic region in the rat. J. Comp. Neur., 167: 227–256.

    Article  Google Scholar 

  • Swanson, L. W., and W. M. Cowan 1975 A note on the connections and development of the nucleus accumbens. Brain Res., 92: 324–330.

    Article  Google Scholar 

  • Turner, P. T., and A. B. Harris 1974 Ultrastructure of exogenous peroxidase in cerebral cortex. Brain Res., 74: 305–326.

    Article  Google Scholar 

  • Wilson, R. D. 1972 The neural associations of nucleus accumbens septi. Masters thesis, M.I.T., Cambridge, Mass.

    Google Scholar 

  • Wolf, G., and J. Sutin 1966 Fiber degeneration afterlateral hypothalamic lesions in the rat. J. Comp. Neur., 127: 137–156.

    Article  Google Scholar 

  • Zyo, K., T. Ă”ki and T. Ban 1963 Experimental studies on the medial forebrain bundle, medial longitudinal fasciculus and supraoptic decussations in the rabbit. Med. J. Osaka Univ., 13: 193–239.

    Google Scholar 

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  1. Miles Herkenham

    Present address: Laboratory of Neurophysiology, National Institute of Mental Health, Bethesda, Maryland, 20014, USA

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  1. Department of Psychology, Massachusetts Institute of Technology, Cambridge, Massachusetts, 02139, USA

    Miles Herkenham & Walle J. H. Nauta

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Herkenham, M., Nauta, W.J.H. (1977). Afferent Connections of the Habenular Nuclei in the Rat. A Horseradish Peroxidase Study, with a Note on the Fiber-of-Passage Problem. In: Neuroanatomy. Contemporary Neuroscientists. Birkhäuser, Boston, MA. https://doi.org/10.1007/978-1-4684-7920-1_16

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  • DOI: https://doi.org/10.1007/978-1-4684-7920-1_16

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