Summary
The dopaminergic innervation of the rat primary (area 17) and secondary (areas 18 and 18a) visual cortical areas was examined immunocytochemically using an antiserum directed against dopamine. This innervation was characterized by the differential density of the respective afferents within individual visual areas. Area 18, especially its rostral part, was observed to receive a considerable amount of dopaminergic axons, whereas areas 17 and 18a were sparsely innervated. The innervation of all layers of area 18 seemed to consist to a considerable extent of axonal branches of radial fibres ascending from layer VI to layer I. At the ultrastructural level, dopamine profiles were found to display similar characteristics in all visual areas. Dopamine labelled axon-terminals and axonal varicosities, examined in single and serial ultrathin sections, were seen to form primarily asymmetrical synaptic contacts with dendritic profiles. These observations suggest a ‘specific’ innervation of cytoarchitectonically distinct cortical regions by dopaminergic axons.
Similar content being viewed by others
References
Ajika, K. &Hökfelt, T. (1973) Ultrastructural identification of catecholamine neurones in the hypothalmic periventricular — arcuate nucleus — median eminence complex with special reference to quantitative aspects.Brain Research 57, 97–117.
Arluison, M., Dietl, M. &Thibault, J. (1984) Ultrastructural morphology of dopaminergic nerve terminals and synapses in the striatum of the rat using tyrosine hydroxylase immunocytochemistry: A topographical study.Brain Research Bulletin 13, 268–85.
Beaudet, A. &Descarries, L. (1978) The monoamine innervation of rat cerebral cortex: Synaptic and nonsynaptic axon terminals.Neuroscience 3, 851–60.
Berger, B., Tassin, J. P., Blanc, G., Moyne, M. A. &Scthierry, A. M. (1974) Histochemical confirmation for dopaminergic innervation of the rat cerebral cortex after destruction of the noradrenergic ascending pathways.Brain Research 81, 332–7.
Berger, B., Thierry, A. M., Tassin, J. P. &Moyne, M. A. (1976) Dopaminergic innervation of the rat prefrontal cortex: A fluorescence histochemical study.Brain Research 106, 133–45.
Berger, B., Trottier, S., Verney, C., Gaspar, P. &Alvarez, C. (1988) Regional and laminar distribution of the dopamine and serotonin innervation of the macaque cerebral cortex: A radioautographic study.Journal of Comparative Neurology 273, 99–119.
Berger, B., Verney, C., Alvarez, C., Vigny, A. &Helle, K. B. (1985) New dopaminergic terminal fields in the motor, visual (area 18b) and retrosplenial cortex in the young and adult rat. Immunocytochemical and catecholamine histochemical analyses.Neuroscience 15, 983–98.
Björklund, A. &Lindvall, O. (1984) Dopaminecontaining system in the CNS. InHandbook of Chemical Neuroantomy, Vol. 2: Classical Neurotransmitters in the CNS, Part I (edited byBjörklund, A. &Hökfelt, T.), pp. 55–122. Amsterdam: Elsevier.
Bouyer, J. J., Joh, T. H. &Pickel, V. M. (1984) Ultrastructural localization of tyrosine hydroxylase in rat nucleus accumbens.Journal of Comparative Neurology 227, 92–103.
Buijs, R. M., Geffard, M., Pool, C. W. &Hoorneman, E. M. D. (1984) The dopminergic innervation of the supraoptic and para ventricular nucleus. A light and electron microscopical study.Brain Research 323, 65–72.
Carter, D. A. &Fibiger, H. C. (1977) Ascending projections of presumed dopamine-containing neurons in the ventral tegmentum of the rat as demonstrated by horseradish peroxidase.Neuroscience 2, 569–76.
Chetverukhin, V. K., Belenky, M. A. &Polenov, A. L. (1979) Quantitative radioautographic light and electron microscopic analysis of the localization of monoamines in the median eminence of the rat. I. Catecholamines.Cell and Tissue Research 203, 469–85.
Cuello, A. C. &Iversen, L. L. (1973) Localization of tritiated dopamine in the median eminence of the rat hypothalamus by electron microscope autoradiography.Brain Research 63, 474–8.
Descarries, L., Bosler, O., Berthelet, F. &Des Rosiers, M. H. (1980) Dopaminergic nerve endings visualised by high resolution autoradiography in adult rat neostriatum.Nature 284, 620–2.
Descarries, L., Lemay, B., Doucet, G. &Berger, B. (1987) Regional and laminar density of the dopamine innervation in adult rat cerebral cortex.Neuroscience 21, 807–24.
Doucet, G., Descarries, L. &Garcia, S. (1986) Quantification of the dopamine innervation in adult rat neostriatum.Neuroscience 19, 427–45.
Doucet, G., Descarries, L., Audet, M. A., Garcia, S. &Berger, B. (1988) Radioautographic method for quantifying regional monoamine innervations in the rat brain. Application to the cerebral cortex.Brain Research 441, 233–59.
Emson, P. C. &Koob, G. F. (1978) The origin and distribution of dopamine-containing afferents to the rat frontal cortex.Brain Research 142, 249–67.
Emson, P. C. &Lindvall, O. (1979) Distribution of putative neurotransmitters in the neocortex.Neuroscience 4, 1–30.
Espinoza, S. G. &Thomas, H. C. (1983) Retinotopic organization of striate and extrastriate visual cortex in the hooded rat.Brain Research 272, 137–44.
Fallon, J. H., Koziell, D. A. &Moore, R. Y. (1978) Catecholamine innervation of the basal forebrain. II. Amygdala, suprarhinal cortex and entorhinal cortex.Journal of Comparative Neurology 180, 509–32.
Fuxe, K. Hökfelt, T., Johansson, O., Jonsson, G., Lidbrink, P. &Ljungdahl, A. (1974) The origin of the dopamine nerve terminals in limbic and frontal cortex. Evidence for meso-cortico dopamine neurons.Brain Research 82, 349–55.
Geffard, M., Buijs, R. M., Séguéla, P., Pool, C. W. &Le Moal, M. (1984) First demonstration of highly specific and sensitive antibodies against dopamine.Brain Research 294, 161–5.
Harik, S. I. (1984) Locus coeruleus lesion by local 6-hydroxydopamine infusion causes marked and specific destruction of noradrenergic neurons, long-term depletion of norepinephrine and the enzymes that synthetize it, and enhanced dopaminergic mechanisms in the ipsilateral cerebral cortex.Journal of Neuroscience 4, 699–707.
Herkenham, M. (1980) Laminar organization of thalamic projections to the rat neocortex.Science 207, 532–5.
Hökfelt, T., Fuxe, K., Johansson, O. &Ljungdahl, A. (1974a) Pharmaco-histochemical evidence of the existence of dopamine nerve terminals in the limbic cortex.European Journal of Pharmacology 25, 108–12.
Hökfelt, T., Ljungdahl, A., Fuxe, K. &Johansson, O. (1974b) Dopamine nerve terminals in the rat limbic cortex: Aspects of the dopamine hypothesis of schizophrenia.Science 184, 177–9.
Levitt, P. &Moore, R. Y. (1978) Noradrenaline neuron innervation of the neocortex in the rat.Brain Research 139, 219–31.
Levitt, P., Rakic, P. &Goldman-Rakic, P. (1984) Regionspecific distribution of catecholamine afferents in primate cerebral cortex: A fluorescence histochemical analysis.Journal of Comparative Neurology 227, 23–36.
Lewis, M. S., Molliver, M. E,., Morrison, J. H. &Lidov, H. G. W. (1979) Complementarity of dopaminergic and noradrenergic innervation in anterior cingulate cortex of the rat.Brain Research 164, 328–33.
Lindvall, O. &Björklund, A. (1984) General organization of cortical monoamine systems. InMonoamine Innervation of Cerebral Cortex (edited byDescarries, L., Reader, T. R. &Jasper, H. H.), pp. 9–40. New York: Alan R. Liss.
Lindvall, O., Björklund, A. &Divac, I. (1978) Organization of catecholamine neurons projecting to the frontal cortex in the rat.Brain Research 142, 1–24.
Lindvall, O., Björklund, A., Moore, R. Y. &Steveni, U. (1974) Mesencephalic dopamine neurons projecting to neocortex.Brain Research 81, 325–31.
Miller, M. W. &Vogt, B. A. (1984a) Direct connections of rat visual cortex with sensory, motor, and association cortices.Journal of Comparative Neurology 226, 184–202.
Miller, M. W. &Vogt, B. A. (1984b) Heterotopic and homotopic callosal connections of rat visual cortex.Brain Research 297, 75–89.
Montero, V. ML, Rojas, A. &Torrealba, F. (1973) Retinotopic organization of striate and peristriate visual cortex in the albino rat.Brain Research 53, 197–201.
Moore, R. Y. &Card, J. P. (1984) Noradrenaline-containing neuron systems. InChemical Neuroanatomy, Vol. 2: Classical Transmitters in the CNS, Part I.(edited byBjÖrklund, A. &HÖkfelt, T.), pp. 123–56. Amsterdam: Elsevier.
Morrison, J. H. &Foote, S. L. (1986) Noradrenergic and serotonergic innervation of cortical, thalamic, and tectal visual structures in old and new world monkeys.Journal of Comparative Neurology 243, 117–38.
Nguyen-Legros, J., Berger, B. &Alvarez, C. (1981) High resolution radioautography of central dopaminergic fibers labelled in vitro [3H]dopamine or [3H]norepinephrine.Brain Research 213, 265–76.
Onteniente, B., Geffard, M. &Calas, A. (1984) Ultrastructural immunocytochemical study of the dopaminergic innervation of the rat lateral septum With anti-dopamine antibodies.Neuroscience 13, 385–93.
Paekovits, M., Zaborsky, L., Brownstein, M. J., Fekete, M. I. K., Hernan, J. P. &Kanyicska, B. (1979) Distribution of norepinephrine and dopamine in cerebral cortical areas of the rat.Brain Research Bulletin 4, 593–601.
Papadopoueos, G. C., Parnavelas, J. G. &Buijs, R. M. (1987) Light and electron microscopic immunocytochemical analysis of the serotonin innervation of the rat visual cortex.Journal of Neurocytology 16, 883–92.
Papadopoueos, G. C., Parnavelas, J. G. &Buijs, R. M. (1989) Light and electron microscopic immunocytochemical analysis of the noradrenaline innervation of the rat visual cortex.Journal of Neurocytology 18, 1–10.
Pelletier, G. (1983) Identification of endings containing dopamine and vasopressin in the rat posterior pituitary by a combination of radioautography and immunocytochemistry at the ultrastructural level.Journal of Histochemistry and Cytochemistry 31, 562–4.
Reader, T. A. (1981) Distribution of catecholamines and serotonin in the rat cerebral cortex: absolute levels and relative proportions.Journal of Neural Transmission 50, 13–27.
Séguéla, P., Watkins, K. C. &Descarries, L. (1988) Ultrastructural features of dopamine axon terminals in the anteromedial and the suprarhinal cortex of adult rat.Brain Research 442, 11–22.
Sukekawa, K. (1988) Interconnections of the visual cortex with the frontal cortex in the rat.Journal für Hirnforschung 29, 83–93.
Swanson, L. W. (1982) The projections of the ventral tegmental area and adjacent regions: A combined fluorescent retrograde tracer and immunofluorescence study in the rat.Brain Research Bulletin 9, 321–53.
Tassin, J. P., Bockaert, J., Blanc, G., Stinus, L., Thierry, A. M., Lavielle, S., Prémont, J. &Glowinski, J. (1978) Topographical distribution of dopaminergic innervation and dopaminergic receptors of the anterior cerebral cortex of the rat.Brain Research 154, 241–51.
Tassin, J. P., Lavielle, S., Hervé D., Blanc, G., Thierry, A. M., Alvarez, C., Berger, B. &Glowinski, J. (1979) Collateral sprouting and reduced activity of the rat mesocortical dopaminergic neurons after selective destruction of the ascending noradrenergic bundles.Neuroscience 4, 1569–82.
Thierry, A. M., Blanc, G., Sobel, A., Stinus, L. &Glowinski, J. (1973a) Dopaminergic terminals in the rat cortex.Science 182, 499–501.
Thierry, A. M., Stinus, L., Blanc, G. &Glowinski, J. (1973b) Some evidence for the existence of dopaminergic neurons in the rat cortex.Brain Research 50, 230–4.
Törk, I. &Turner, S. (1981) Histochemical evidence for a catecholaminergic (presumably dopaminergic) projection from the ventral mesencephalic tegmentum to visual cortex in the cat.Neuroscience Letters 24, 215–9.
Torrealba, F., Olavarria, J. &Carrasco, M. A. (1984) Cortical connections of the anteromedial extrastriate visual cortex in the rat.Experimental Brain Research 56, 543–9.
Van Eden, C. G., Hoorneman, E. M. D., Buijs, R. M., Matthijssen, M. A. H., Geffard, M. &Uylings, H. B. M. (1987) Immunocytochemical localization of dopamine in the prefrontal cortex of the rat at the light and electron microscopical level.Neuroscience 22, 849–62.
Voorn, P., Jorritsma-Byham, B., Van Dijk, C. &Buijs, R. M. (1986) The dopaminergic innervation of the ventral striatum in the rat: A light- and electron-microscopical study with antibodies against dopamine.Journal of Comparative Neurology 251, 84–99.
Wilson, C. J., Groves, P. M. &Fifkova, E. (1977) Monoaminergic synapses, including dendro-dendritic synapses in the rat substantia nigra.Experimental Brain Research 30, 161–74.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Papadopoulos, G.C., Parnavelas, J.G. & Buijs, R.M. Light and electron microscopic immunocytochemical analysis of the dopamine innervation of the rat visual cortex. J Neurocytol 18, 303–310 (1989). https://doi.org/10.1007/BF01190833
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01190833