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Afferent connections of the forebrain cholinergic projection neurons, with special reference to monoaminergic and peptidergic fibers

  • Chapter
Central Cholinergic Synaptic Transmission

Part of the book series: Experientia Supplementum ((EXS,volume 57))

Summary

Earlier light microscopic data on afferent connections to the cholinergic forebrain neurons are reconsidered in the light of EM cross-identification of neurons and synapses by combinations of tracer and immunocytochemical techniques. Such studies suggest that brainstem monoaminergic afferents terminate on cholinergic forebrain neurons, and may modulate the activity of choline acetyltransferase levels in the postsynaptic neurons. A monosynaptic relationship between cholinergic forebrain neurons and neuropeptide Y and somatostatin containing axons is also supported by studies using double immunolabeling techniques at the EM level. These peptidergic afferents originate in part from locally arborizing neurons. Based upon the new data a circuit model for basal forebrain cholinergic neurons is proposed.

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References

  • Aggleton, J. P., Burton, M. J., and Passingham, R. E. (1980) Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca Mulatta). Brain Res. 190: 347–368.

    Article  Google Scholar 

  • Amaral, D. G., and Kurz, J. (1985) An analysis of the origins of the cholinergic and noncholinergic septal projections to the hippocampal formation. J. comp. Neurol. 240: 37–59.

    Article  Google Scholar 

  • Amaral, D. G., Veazey, R. B., and Cowan, W. M. (1982) Some observations on hypothalamo amygdaloid connections in the monkey. Brain Res. 252: 13–27.

    Article  Google Scholar 

  • Armstrong, D. M., Saper, C. B., Levey, A. I., Wainer, B. H., and Terry, R. D. (1983) Distribution of cholinergic neurons in rat brain: Demonstrated by the immunocytochemical localization of choline acetyltransferase. J. comp. Neurol. 216: 53–68.

    Article  Google Scholar 

  • Azmita, E. C., and Segal, M. (1978) An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J. comp. Neurol. 179: 641–688.

    Article  Google Scholar 

  • Beckstead, R. M. (1979) An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal-projection (prefrontal) cortex in the rat. J. comp. Neurol. 184: 43–62.

    Article  Google Scholar 

  • Beckstead, R. M., Domesick, V. B., and Nauta, W. J. H. (1979) Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res. 175: 191–217.

    Article  Google Scholar 

  • Berk, M. L., and Finkelstein, J. A. (1982) Efferent connections of the lateral hypothalamic area of the rat: An autoradiographic investigation. Brain Res. Bull. 8: 511–526.

    Article  Google Scholar 

  • Bolam, J. P., Ingham, C. A., Izzo, P. N., Levey, A. I., Rye, D. B., Smith, A. D., and Wainer, B. H. (1986) Substance P-containing terminalis in synaptic contact with cholinergic neurons in the neostriatum and basal forebrain: A double immunocytochemical study in the rat. Brain Res. 397: 279–289.

    Article  Google Scholar 

  • Buzsaki, G., Bickford, R. G., Ponomareff, G., Thai, L. J., Mandel, R., and Gage, F. H. (1988) Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J. Neurosci. 8: 4007–4026.

    Google Scholar 

  • Carlsen, J., Zaborszky, L., and Heimer, L. (1985) Cholinergic projections from the basal forebrain to the basolateral amygdaloid complex: A combined retrograde fluorescent and immunohistochemical study. J. comp. Neurol. 234: 155–167.

    Article  Google Scholar 

  • Chan, H. T., Penny, G. R., and Kitai, S. T. (1987) Enkephalinergic-cholinergic interaction in the rat globus pallidus: A pre-embedding double-labeling immunocytochemistry study. Brain Res. 426: 197–203.

    Article  Google Scholar 

  • Chronwall, B. M., Chase, T. N., and O’Donohue, T. L. (1984) Coexistence of neuropeptide Y and somatostatin in rat and human cortical and rat hypothalamic neurons. Neurosci. Lett. 52: 213–217.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Conrad, L. C. A., Leonard, C. M., and Pfaff, D. W. (1974) Connections of the median and dorsal raphe nuclei in the rat: An autoradiographic and degeneration study. J. comp. Neurol. 156: 179–206.

    Article  Google Scholar 

  • Constantinidis, J., Bouras, C., and Vellet, P. G. (1988) Neuropeptides in Alzheimer’s and in Parkinson’s Disease. Mt Sinai J. Med. 55: 102–115.

    Google Scholar 

  • Eberhart, J. A., Morell, J. I., Krieger, M. S., and Pfaff D. W. (1985) An autoradiographic study of projections ascending from the midbrain central gray, and from the region lateral to it in the rat. J. comp. Neurol. 241: 285–310.

    Article  Google Scholar 

  • Eckenstein, F. P., Baughman, R. W., and Quinn, J. (1988) An anatomical study of cholinergic innervation in rat cerebral cortex. Neuroscience 25: 457–474.

    Article  Google Scholar 

  • Edwards, S. B., and de Olmos, J. S. (1976) Autoradiographic studies of the projections of the midbrain reticular formation: Ascending projections of nucleus cuneiformis. J. comp. Neurol. 165: 417–432.

    Google Scholar 

  • Fallon, J. H., and Moore, R. Y. (1978) Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J. comp. Neurol. 180: 545–580.

    Article  Google Scholar 

  • Fisher, R. S., Buchwald, N. A., Hull, C. D., and Levine, M. S. (1988) GABAergic basal forebrain neurons project to the neocortex: The localization of glutamic acid decarboxylase and choline acetyltransferase in feline corticopetal neurons. J. comp. Neurol. 272: 489–502.

    Article  Google Scholar 

  • Foote, S. L., Bloom, F. E., and Aston-Jones, G. (1983) Nucleus locus ceruleus: New evidence of anatomical and physiological specificity. Physiol. Rev. 63: 844–914.

    Google Scholar 

  • Fuller, T. A., Carnes, K. M., and Price J. L. (1986) Afferents to the horizontal diagonal band of rat. Soc. Neurosci. Abstr. 12: 351.

    Google Scholar 

  • Groenewegen, H. J., and Russchen, F. T. (1984) Organization of the efferent projections of the nucleus accumbens to pallidal, hypothalamic and mesencephalic structures. A tracing and immunohistochemical study in the cat. J. comp. Neurol. 223: 347–368.

    Article  Google Scholar 

  • Grove, E. A., Domesick, V. B., Nauta, W. J. H. (1986) Light microscopic evidence of striatal input to intrapallidal neurons of cholinergic cell group Ch4 in the rat: A study employing the anterograde tracer Phaseolus vulgaris leucoagglutinin (PHAL). Brain Res. 367: 379–384.

    Article  Google Scholar 

  • Hallanger, A. E., Levey, A. L., Lee, H. J., Rye, D. B., and Wainer, B. H. (1987) The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J. comp. Neurol. 262: 105–124.

    Article  Google Scholar 

  • Haring, J. H., and Wang, R. Y. (1986) The identification of some sources of afferent input to the rat nucleus basalis magnocellularis by retrograde transport of horseradish peroxidase. Brain Res. 366: 152–158.

    Article  Google Scholar 

  • Herkenham, M., and Nauta, W. J. H. (1979) Efferent connections of the habenular nuclei in the rat. J. comp. Neurol. 187: 19–48.

    Article  Google Scholar 

  • Hobson, J. A., and Steriade, M. (1986) Neuronal basis of behavioral state control. In: Mountcastle, V. B., Bloom, F. E., and Geiger, S. R. (eds), Handbook of Physiology. The nervous system. Intrinsic regulatory systems of the brain, Sect. 1, Vol. 4. Am. physiol. Soc., Bethesda, pp. 701–823.

    Google Scholar 

  • Houser, C. R., Crawford, G. D., Salvaterra, P. M., and Vaughn, J. E. (1985) Immunocyto- chemical localization of choline acetyltransferase in rat cerebral cortex: A study of cholinergic neurons and synapses. J. comp. Neurol. 234: 17–34.

    Article  Google Scholar 

  • Ingham, C. A., Bolam, J. P., and Smith, A. D. (1988) GABA-immunoreactive synaptic boutons in the rat basal forebrain: Comparison of neurons that project to the neocortex with pallidosubthalamic neurons. J. comp. Neurol. 273: 263–282.

    Article  Google Scholar 

  • Irle, E., and Markowitsch, H. J. (1984) Basal forebrain efferents reach the whole cerebral cortex of the cat. Brain Res. Bull. 12: 493–512.

    Article  Google Scholar 

  • Irle, E., and Markowitsch, H. J. (1986) Afferent connections of the substantia innominata/basal nucleus of Meynert in carnivores and primates. J. Hirnforsch. 27: 343–367.

    Google Scholar 

  • Iversen, L. L. (1983) Amino acids and peptides: Fast and slow chemical signals in the nervous system? Proc. R. Soc. Lond. B 221: 245–260.

    Article  Google Scholar 

  • Jones, B. E., and Beaudet, A. (1987) Retrograde labeling of neurons in the brain stem following injections of [3H] choline into the forebrain of the rat. Exp. Brain Res. 65: 437–448.

    Google Scholar 

  • Jones, B. E., and Yang, T.-Z. (1985) The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. J. comp. Neurol. 242: 56–92.

    Article  Google Scholar 

  • Jones, B. E., and Moore, R. Y. (1977) Ascending projections of the locus coeruleus in the rat. II. Autoradigraphic study. Brain Res. 127: 23–53.

    Article  Google Scholar 

  • Kelley, A. E., Domesick, V. B., and Nauta, W. J. H. (1982) The amygdalostriatal projection in the rat—An anatomical study by anterograde and retrograde tracing methods. Neuroscience 7: 615–630.

    Article  Google Scholar 

  • Kow, L.-M., and Pfaff, D. W. (1988) Neuromodulatory actions of peptides. Ann Rev. Pharmac. Toxic. 28: 163–188.

    Google Scholar 

  • Krettek, J. E., and Price, J. L. (1978) Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J. comp. Neurol. 178: 225–254.

    Article  Google Scholar 

  • Krieger, M. S., Conrad, L. C. A., and Pfaff, D. W. (1979) An autoradiographic study of the efferent connections of the ventromedial nucleus of the hypothalamus. J. comp. Neurol. 183: 785–816.

    Article  Google Scholar 

  • Kristt, D. A., McGowan, R. A., Martin-MacKinnon, N., and Solomon, J. (1985) Basal forebrain innervation of rodent neocortex: Studies using acetylcholinesterase histochemistry, Golgi and lesion strategies. Brain Res. 337: 19–39.

    Article  Google Scholar 

  • Leichnetz, G. R., and Astruc, J. (1977) The course of some prefrontal corticofugals to the pallidum, substantia innominata, and amygdaloid complex in monkeys. Exp. Neurol. 54: 104–109.

    Article  Google Scholar 

  • Leman, W., and Saper, C. B. (1985) Evidence for a cortical projection to the magnocellular basal nucleus in the rat: An electron microscopic axonal transport study. Brain Res. 334: 339–343.

    Article  Google Scholar 

  • Leranth, C., MacLusky, N. J., Shanabrough, M., and Naftolin, F. (1988) Catecholaminergic innervation of LHRH and GAD immunopositive neurons in the rat medial preoptic area: An electron microscopic double immunostaining and degeneration study. Neuroendocrinol- ogy 48: 591–602.

    Google Scholar 

  • Levey, A. I., Bolam, J. P., Rye, D. B., Hallanger, A. E., Demuth, R. M., Mesulam, M.-M., and Wainer, B. H. (1986) A light and electron microscopic procedure for sequential double antigen localization using diaminobenzidine and benzidine dihydrochloride. J. Histochem. Cytochem. 34: 1449–1457.

    Google Scholar 

  • Levine, M. S., Cepeda, C., and Buchwald, N. A. (1968) Electrophysiological properties of basal forebrain neurons: Responses to microphoretic application of putative neurotransmitters. Soc. Neurosci. Abstr. 12: 1468.

    Google Scholar 

  • Loewy, A. D., Wallach, J. H., and McKellar, S. (1981) Efferent connections of the ventral medulla oblongata in the rat. Brain Res. Rev. 3: 63–80.

    Google Scholar 

  • Luiten, P. G. M., Gaykema, R. P. A., Traber, J., and Spencer, D. G. (1987) Cortical projection patterns of magnocellular basal nucleus subdivisions as revealed by anterogradely transported Phaseolus vulgaris leucoagglutinin. Brain Res. 413: 229–250.

    Article  Google Scholar 

  • Martinez-Murillo, R., Semenenko, F., and Cuello, A. C. (1988) The origin of tyrosine hydroxylase immunoreactive fibers in the regions of the nucleus basalis magnocellularis of the rat. Brain Res. 451: 227–236.

    Article  Google Scholar 

  • McKellar, S., and Loewy, A. D. (1982) Efferent projections of the Al catecholamine cell group in the rat: An autoradiographic study. Brain Res. 241: 11–29.

    Article  Google Scholar 

  • McLean, J. H., Nickell, W. T., and Shipley, M. T. (1986) Afferent connections to the horizontal limb of diagonal band. Soc. Neurosci. Abstr. 12: 351.

    Google Scholar 

  • Melander, T., Staines, W. A., Hökfelt, T., Rokaeus, A., Eckenstein, F., Salvaterra, P. M., and Wainer, B. H. (1985) Galanin-like immunoreactivity in cholinergic neurons of the septum- basal forebrain complex projecting to the hippocampus of the rat. Brain Res. 360: 130–138.

    Article  Google Scholar 

  • Mesulam, M.-M., Mufson, E. J., Wainer, B. H., and Levey, A. I. (1983a) Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Chl-Ch6). Neuroscience 10: 1185–1201.

    Article  Google Scholar 

  • Mesulam, M.-M., Mufson, E. J., Levey, A. I., and Wainer, B. H. (1983b) Cholinergic innervation of cortex by the basal forebrain: Cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J. comp. Neurol. 214: 170–197.

    Article  Google Scholar 

  • Mesulam, M.-M., and Mufson, E. J. (1984) Neural inputs into the nucleus basalis of the substantia innominata (Ch4) in the rhesus monkey. Brain 107: 253–274.

    Article  Google Scholar 

  • Mesulam, M.-M., Rosen, A. D., and Mufson, E. J. (1984) Regional variations in cortical cholinergic innervation: Chemoarchitectonics of acetylcholinesterase-containing fibers in the macaque brain. Brain Res. 311: 245–258.

    Article  Google Scholar 

  • Moroni, F., Bianchi, C., Moneti, G., Tanganelli, S., Spidelieri, G., Guandalini, P., and Beani, L. (1982) Release of GABA from the guinea-pig neocortex induced by electrical stimulation of the locus coeruleus or by norepinephrine. Brain Res. 232: 216–221.

    Article  Google Scholar 

  • Nakai, Y., and Takaori, S. (1974) Influence of norepinephrine containing neurons derived from the locus coeruleus on lateral geniculate neuronal activities of cats. Brain Res. 71: 47–60.

    Article  Google Scholar 

  • Nauta, W. J. H., Smith, G. P., Faull, R. L. M., and Domesick, V. B. (1978) Efferent connections and nigral afferents of the nucleus accumbens septi in the rat. Neuroscience 3: 385–401.

    Article  Google Scholar 

  • Norgren, R. (1976) Taste pathways to hypothalamus and amygdala. J. comp. Neurol. 166: 17–30.

    Article  Google Scholar 

  • Okamoto, M., and Wada, J. A. (1984) Reversible suppression of amygdaloid kindled convulsion following unilateral gabaculine injection in to the substantia innominata. Brain Res. 305: 389–392.

    Article  Google Scholar 

  • Oshima, T. (1983) Intracortical organization of arousal as a model of dynamic neuronal processes that may involve a set for movements. In: Desmedt, J. E. (ed.), Motor Control Mechanisms in Health and Disease. Raven Press, New York, pp. 287–300.

    Google Scholar 

  • Palkovits, M. (1984) Distribution of neuropeptides in the central nervous system: A review of biochemical mapping studies. Prog. Neurobiol. 23: 151–189.

    Google Scholar 

  • Price, D. L., Whitehouse, P. J., and Struble, R. G. (1986) Cellular pathology in Alzheimer’s and Parkinson’s Diseases. TINS 9: 29–33.

    Google Scholar 

  • Price, J. L., and Stern, R. (1983) Individual cells in the nucleus basalis-diagonal band complex have restricted axonal projections to the cerebral cortex in the rat. Brain Res. 269: 352–356.

    Article  Google Scholar 

  • Price, J. L., and Amaral, D. G. (1981) An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J. Neurosci. 1: 1242–1259.

    Google Scholar 

  • Rao, Z. R., Shiosaka, S., and Tohyama, M. (1987) Origin of cholinergic fibers in the basolateral nucleus of the amygdaloid complex by using sensitive double-labeling technique of retrograde biotinized tracer and immunocytochemistry. J. Hirnforsch. 28: 553–560.

    Google Scholar 

  • Ricardo, J. A. (1981) Efferent connections of the subthalamic region in the rat. II. The zona incerta. Brain Res. 214: 43–60.

    Article  Google Scholar 

  • Ricardo, J. A., and Koh, E. T. (1978) Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala and other forebrain structures in the rat. Brain Res. 153: 1–26.

    Article  Google Scholar 

  • Richardson, R. T., and DeLong, M. R. (1988) A reappraisal of the functions of the nucleus basalis of Meynert. TINS 11: 264–267.

    Google Scholar 

  • Robinson, S. E., Malthe-Sorenssen, D., Wood, P. L., and Commissiong, J. (1979) Dopaminergic control of the septal-hippocampal cholinergic pathway. J. Pharm. exp. Ther. 476–479.

    Google Scholar 

  • Rye, D. B., Wainer, B. H., Mesulam, M. M., Mufson, E. J., and Saper, C. B. (1984) Cortical projections arising from the basal forebrain: A study of cholinergic and non-cholinergic components employing combined retrograde tracing and immunohistochemical localization of choline acetyltransferase. Neuroscience 13: 627–643.

    Article  Google Scholar 

  • Russchen, F. T., Amaral, D. G., and Price, J. L. (1985) The afferent connections of the substantia innominata in the monkey, Macaca Fascicularis. J. comp. Neurol. 242: 1–27.

    Article  Google Scholar 

  • Russchen, F. T., and Price, J. L. (1984) Amygdalostriatal projections in the rat. Topographical organization and fiber morphology shown using the lectin PHA-L as an anterograde tracer. Neurosci. Lett. 47: 15–22.

    Article  Google Scholar 

  • Saper, C. B. (1987) Diffuse cortical projection systems: Anatomical organization and role in cortical function. In: Mountcastle, V. B., Plum, F., and Geiger, S. (eds), Handbook of Physiology, Section 1. The nervous system, Vol. 5, part 1. Am. physiol. Soc., Bethesda, pp. 169–210.

    Google Scholar 

  • Saper, C. B. (1984) Organization of cerebral cortical afferent systems in the rat. I. Magnocellular basal nucleus. J. comp. Neurol. 222: 1–30.

    Article  Google Scholar 

  • Saper, C. B. (1985) Organization of cerebral cortical afferent systems in the rat. II. Hypotha- lamocortical projections. J. comp. Neurol. 237: 21–46.

    Article  Google Scholar 

  • Saper, C. B., and Loewy, A. D. (1980) Efferent connections of the parabrachial nucleus in the rat. Brain Res. 197: 291–317.

    Article  Google Scholar 

  • Saper, C. B., Swanson, I. W., and Cowan, W. M. (1979) An autoradiographic study of the efferent connections of the lateral hypothalamic area in the rat. J. comp. Neurol. 183: 689–706.

    Article  Google Scholar 

  • Saper, C. B., Swanson, L. H., and Cowan, W. M. (1976) The efferent connections of the ventromedial nucleus of the hypothalamus of the rat. J. comp. Neurol. 169: 408–442.

    Article  Google Scholar 

  • Satoh, K., and Fibiger, H. C. (1986) Cholinergic neurons of the laterodorsal tegmental nucleus: Efferent and afferent connections. J. comp. Neurol. 253: 277–302.

    Article  Google Scholar 

  • Semba, K, Reiner, P. B., McGeer, E. G., and Fibiger, H. C. (1987) Morphology of cortically projecting basal forebrain neurons in the rat as revealed by intracellular iontophoresis of horseradish peroxidase. Neuroscience 20: 637–651.

    Article  Google Scholar 

  • Semba, K., Reiner, P. B., McGeer, E. G., and Fibiger, H. C. (1988a) Non-cholinergic basal forebrain neurons project to the contralateral basal forebrain in the rat. Neurosci. Lett. 84: 23–28.

    Article  Google Scholar 

  • Semba, K., Reiner, P. B., McGeer, E. G., and Fibiger, H. C. (1988b) Brainstem afferents to the magnocellular basal forebrain studied by axonal transport, immunohistochemistry, and electrophysiology in the rat. J. comp. Neurol. 267: 433–453.

    Article  Google Scholar 

  • Shen, C. I. (1983) Efferent projections from the mammillary complex of the guinea pig: An autoradiographic study. Brain Res. Bull. 11: 43–59.

    Article  Google Scholar 

  • Simon, H., Le Moal, M., and Calas A. (1979) Efferents and afferents of the ventral tegmental-AlO region studied after local injection of [3H] leucin and horseradish peroxidase. Brain Res. 178: 17–40.

    Article  Google Scholar 

  • Sofroniew, M. V., Eckenstein, F., Thoenen, H., and Cuello, A. C. (1982) Topography of choline acetyltransferase-containing neurons in the forebrain of the rat. Neurosci. Lett. 33: 7–12.

    Article  Google Scholar 

  • Somogyi, P., Hodgson, A. J., Smith, A. D., Nunzi, M. G., Gorio, A., and Wu, J.-Y. (1984) Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin- or cholecystokinin-immunoreactive material. J. Neurosci. 4: 2590– 2603.

    Google Scholar 

  • Steinbusch, H. W. M. (1981) Distribution of serotonin-immunoreactivity in the central nervous system of the rat—cell bodies and terminals. Neuroscience 6: 557–618.

    Article  Google Scholar 

  • Steriade, M., and Llinas, R. R. (1988) The functional states of the thalamus and the associated neuronal interplay. Physiol. Rev. 68: 649–742.

    Google Scholar 

  • Steriade, M., Domich, L., Oakson, G., and Deschenes, M. (1987) The deafferented reticular thalamic nucleus generates spindle rhythmicity. J. Neurophysiol. 57: 260–273.

    Google Scholar 

  • Steriade, M., Parent, A., Pare, D., and Smith, Y. (1987) Cholinergic and noncholinergic neurons of cat basal forebrain project to reticular and mediodorsal thalamic nuclei. Brain Res. 408: 372–376.

    Article  Google Scholar 

  • Swanson, L. W. (1983) Neuropeptides—new vistas on synaptic transmission. TINS 6: 294–295.

    Google Scholar 

  • Swanson, L. W., and Cowan, W. M. (1979) The connections of the septal region in the rat. J. comp. Neurol. 186: 621–656.

    Article  Google Scholar 

  • Swanson, L. W., and Hartman, B. K. (1975) The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-ft-hydroxylase as a marker. J. comp. Neurol. 163: 467–506.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Takagi, H., Shiosaka, S., Tohyama, M., Senba, E., and Sakanaka, M. (1980) Ascending components of the medial forebrain bundle from the lower brain stem in the rat, with special reference to raphe and catecholamine cell groups. A study by the HRP method. Brain Res. 193: 315–337.

    Article  Google Scholar 

  • Troiano, R., and Siegel, A. (1978) Efferent connections of the basal forebrain in the cat: The nucleus accumbens. Exp. Neurol. 61: 185–197.

    Article  Google Scholar 

  • Van Hoesen, G. W., and Damasio, A. R. (1987) Neuroal correlates of cognitive impairment in Alzheimer’s disease. In: Mountcastle, V. B., Plum, F., and Geiger, S. R. (eds), Handbook of Physiology, Sect. 1, vol. 5, Part 2. Am. physiol. Soc., Bethesda, pp. 871–898.

    Google Scholar 

  • Vertes, R. P. (1984a) A lectin horseradish peroxidase study of the origin of ascending fibers in the medial forebrain bundle of the rat. The lower brainstem. Neuroscience 11: 651–668.

    Article  Google Scholar 

  • Vertes, R. P. (1984b) A lectin horseradish peroxidase study of the origin of ascending fibers in the medial forebrain bundle of the rat. The upper brainstem. Neuroscience 11: 669–690.

    Article  Google Scholar 

  • Vertes, R. P. (1988) Brainstem afferents to the basal forebrain in the rat. Neuroscience 24: 907–935.

    Article  Google Scholar 

  • Vertes, R. P., and Martin, G. F. (1988) Autoradiographic analysis of ascending projections from the pontine and mesencephalic reticular formation and the median raphe nucleus in the rat. J. comp. Neurol. 275: 511–541.

    Article  Google Scholar 

  • Wainer, B. H., Levey, A. I., Rye, D. B., Mesulam, M.-M., and Mufson, E. J. (1985) Cholinergic and non-cholinergic septohippocampal pathways. Neurosci. Lett. 54: 45–52.

    Article  Google Scholar 

  • Walker, L. C., Kitt, C. A., DeLong, M. R., and Price, D. L. (1985) Noncollateral projections of basal forebrain neurons to frontal and parietal neocortex in primates. Brain Res. Bull. 15: 307–314.

    Article  Google Scholar 

  • Whitlock, D. C., and Nauta, W. J. H. (1956) Subcortical projections from the temporal neocortex in Macaca mulatta. J. comp. Neurol. 106: 183–212.

    Article  Google Scholar 

  • Williams, D. I., Crossman, A. R., and Slater, P. (1977) The efferent projections of the nucleus accumbens in the rat. Brain Res. 130: 217–227.

    Article  Google Scholar 

  • Wood, P. L., and McQuade, P. (1986) Substantia innominata—cortical cholinergic pathway: Regulatory afferents. Adv. Behav. Biol. 30: 999–1006.

    Google Scholar 

  • Woolf, N. J., Eckenstein, F., and Butcher, L. L. (1984) cholinergic systems in the rat brain. I. projections to the limbic telencephalon. Brain Res. Bull. 13: 751–784.

    Google Scholar 

  • Zaborszky, L., Leranth, Cs., and Heimer, L. (1984) Ultrastructural evidence of amygdalofugal axons terminating on cholinergic cells of the rostral forebrain. Neurosci. Lett. 52: 215–225.

    Article  Google Scholar 

  • Zaborszky, L., Carlsen, J., Brashear, H. R., and Heimer, L. (1986a) Cholinergic and GABAergic afferents to the olfactory bulb in the rat with special emphasis on the projection neurons in the nucleus of the horizontal limb of the diagonal band. J. comp. Neurol. 243: 488–509.

    Article  Google Scholar 

  • Zaborszky, L., Heimer, L., Eckenstein, F., and Leranth, Cs. (1986b) GABAergic input to cholinergic forebrain neurons: An ultrastructural study using retrograde tracing of HRP and double immunolabeling. J. comp. Neurol. 250: 282–295.

    Article  Google Scholar 

  • Zaborszky, L., and Cullinan, W. E. (1989) Hypothalamic axons terminate on forebrain cholinergic neurons: An ultrastructural double-labeling study using PHA-L tracing and ChAT immunocytochemistry. Brain Res., 479: 177–184.

    Article  Google Scholar 

  • Zaborszky, L., and Heimer, L. (1989) Combinations of tracer techniques, especially HRP and PHA-L, with transmitter identification for correlated light and electron microscopic studies. In: Heimer, L., and Zaborszky, L. (eds), Neuroanatomical Tract-Tracing Methods II: Recent Progress. Plenum Press, in press.

    Google Scholar 

  • Zaborszky, L., Luine, V. N., Cullinan, W. E., Allen, D. L., and Heimer, L. (1989) Catecholaminergic-cholinergic interactions in the basal forebrain: Morphological and biochemical studies. Neuroscience, submitted.

    Google Scholar 

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Authors and Affiliations

  1. Department of Otolaryngology, University of Virginia Medical Center, Box 430, Charlottesville, VA, 22908, USA

    Laszlo Zaborszky

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  1. Laszlo Zaborszky
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Editors and Affiliations

  1. Anatomisches Institut, J.W. Goethe-Universität, Theodor-Stern-Kai 7, 6000, Frankurt a.M 70, Federal Republic of Germany

    Michael Frotscher

  2. Max-Planck-Institut fĂĽr Psychiatrie, Am Klopferspitz 18A, 8033, Planegg-Martinsried, Federal Republic of Germany

    Ulrich Misgeld

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© 1989 Birkhäuser Verlag

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Zaborszky, L. (1989). Afferent connections of the forebrain cholinergic projection neurons, with special reference to monoaminergic and peptidergic fibers. In: Frotscher, M., Misgeld, U. (eds) Central Cholinergic Synaptic Transmission. Experientia Supplementum, vol 57. Birkhäuser Basel. https://doi.org/10.1007/978-3-0348-9138-7_2

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  • DOI: https://doi.org/10.1007/978-3-0348-9138-7_2

  • Publisher Name: Birkhäuser Basel

  • Print ISBN: 978-3-0348-9922-2

  • Online ISBN: 978-3-0348-9138-7

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