Cholinergic innervation of the cat striate cortex: A choline acetyltransferase immunocytochemical analysis
Ana Dolabela De Lima
Max Planck Institut für Hirnforschung, 6000 Frankfurt am Main 71, Federal Republic of Germany
Search for more papers by this authorWolf Singer
Max Planck Institut für Hirnforschung, 6000 Frankfurt am Main 71, Federal Republic of Germany
Search for more papers by this authorAna Dolabela De Lima
Max Planck Institut für Hirnforschung, 6000 Frankfurt am Main 71, Federal Republic of Germany
Search for more papers by this authorWolf Singer
Max Planck Institut für Hirnforschung, 6000 Frankfurt am Main 71, Federal Republic of Germany
Search for more papers by this authorAbstract
In area 17 of adult cats the morphology, distribution, and synaptology of cholinergic elements were examined by immunocytochemical methods with a monoclonal antibody against choline acetyltransferase (ChAT). ChAT(+) fibers are present throughout the entire depth of the cortex but are particularly dense in layer I. Typically these fibers are very thin and possess numerous irregularly spaced varicosities. Except in layer I and deep layer VI, where the fibers tend to run parallel to the pial surface, they appear to be randomly oriented.
At the electron microscope level, immunolabeling was present in unmyelinated fibers of irregular contour and diameter. Most of the ChAT(+) varicose profiles contained mitochondria and round vesicles; Synaptic complexes were relatively infrequent and tended to be of the symmetrical type. They were located mostly on dendritic shafts and only rarely on cell bodies and dendritic spines. Both pyramidal and nonpyramidal cells were found to be innervated by cholinergic afferents.
These anatomical data are consistent with the known physiology of acetylcholine in the visual cortex, which indicates that it acts as a modulator of cortical excitability.
Literature Cited
- Armstrong, D. M., C. B. Saper, A. I. Levey, B. H. Wainer and R. D. Terry (1983) Distribution of cholinergic neurons in rat brain: Demonstrated by the immunocytochemical localization of choline acetyltransferase. J. Comp. Neurol. 216: 53–68.
- Bear, M. F., and W. Singer (1986) Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320: 172–176.
- Bear, M. F., K. M. Carnes and F. F. Ebner (1985) An investigation of cholinergic circuitry in cat striate cortex using acetylcholinesterase histochemistry. J. Comp. Neurol. 234: 411–430.
- Beaudet, A., and L. Descarries (1978) The monoamine innervation of rat cerebral cortex: Synaptic and nonsynaptic axon terminals. Neuroscience 3: 851–860.
- Colonnier, M. (1981) The electron microscopic analysis of the neuronal organization of the cerebral cortex. In F. O. Schmitt, F. G. Worden, G. Adelman, and S. G. Dennis (eds): The Organization of the Cerebral Cortex. Cambridge, MA: MIT Press, pp. 125–152.
- De Lima, A. D., and W. Singer (1985) The cholinergic innervation of the cat striate cortex. Neurosci. Lett. Suppl. 22: S440.
- De Lima, A. D., V. M. Montero, and W. Singer (1985) The cholinergic innervation of the visual thalamus: An EM immunocytochemical study. Exp. Brain Res. 59: 206–212.
- Descarries, L., A. Beaudet and K. C. Watkins (1975) Serotonin nerve terminals in adult rat neocortex. Brain Res. 100: 563–588.
- Descarries, L., K. C. Watkins, and Y. Lapierre (1977) Noradrenergic axon terminals in the cerebral cortex of rat. III. Topometric ultrastructural analysis. Brain Res. 133: 197–222.
- Eckenstein, F., and H. Thoenen (1982) Production of specific antisera and monoclonal antibodies to choline acetyltransferase: Characterization and use for identification of cholinergic neurons. EMBO J. 1: 363–368.
- Eckenstein, F., and H. Thoenen (1983) Cholinergic neurons in the rat cerebral cortex demonstrated by immunohistochemical localization of choline acetyltransferase. Neurosci. Lett. 36: 211–215.
- Fibiger, H. C. (1982) The organization and some projections of cholinergic neurons of the mammalian forebrain. Brain Res. Rev. 4: 327–388.
- Frotscher, M., and C. Leranth (1985) Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: A combined light and electron microscopic study. J. Comp. Neurol. 239: 237–246.
- Garey, L. J. (1971) A light and electron microscopic study of the visual cortex of the cat and monkey. Proc. R. Soc. Lond. B179: 21–40.
- Hedreen, J. C., G. R. Uhl, S. J. Bacon, D. M. Fambrough and D. L. Price (1984) Acetylcholinesterase-immunoreactive axonal network in monkey visual cortex. J. Comp. Neurol. 226: 246–254.
- Houser, C. R., G. D. Crawford, R. P. Barber, P. M. Salvaterra and J. E. Vaughn (1983) Organization and morphological characteristics of cholinergic neurons: An immunocytochemical study with a monoclonal antibody to choline acetyltransferase. Brain Res. 266: 97–119.
- Houser, C. R., G. D. Crawford, P. M. Salvaterra and J. E. Vaughn (1985) Immunocytochemical localization of choline acetyltransferase in rat cerebral dortex: A study of cholinergic neurons and synapses. J. Comp. Neurol. 234: 17–34.
- Kimura, H., P. L. McGeer, F. Peng and E. G. McGeer (1980) Choline acetyl-transferase-containing neurons in rodent brain demonstrated by immunohistochemistry Science 208: 1057–1059.
- Kimura, H., P. L. McGeer, J. H. Peng, and E. G. McGeer (1981) The central cholinergic system studied by choline acetyltransferase immunohistochemistry in the cat. J. Comp. Neurol. 200: 151–201.
- Krnjevic, K. (1984) Neurotransmitters in cerebral cortex. A general account. In E. G. Jones and A. Peters (eds): Cerebral Cortex, Vol. 2: Functional Properties of Cortical Cells. New York: Plenum, pp. 39–61.
- Krnjevic, K., and A. Silver (1965) A histochemical study of cholinergic fibres in the cerebral cortex. J. Anat. 99: 711–759.
- Krnjevic, K., R. Pumain, and L. Renaud (1971) The mechanism of excitation by acetylcholine in the cerebral cortex. J. Physiol. 215: 247–268.
- Leranth, C., and E. Feher (1983) Synaptology and sources of vasoactive intestinal polypeptide and substance P containing axons of the cat celiac ganglion. An experimental electron microscopic immunohistochemical study. Neuroscience 10: 947–958.
- Levey, A. I., B. H. Wainer, D. B. Rye, E. J. Mufson and M. M. Mesulam (1984) Choline acetyltransferase-immunoreactive neurons intrinsic to rodent, cortex and distinctions from acetylcholinesterase-positive neurons. Neuroscience 13: 341–353.
- Livingstone, M. S. and D. H. Hubel (1981) Effects of sleep and arousal on the processing of visual information in the cat. Nature 291: 554–561.
- McCormick, D. A. and D. A. Prince (1985) Two physiologically and pharmacologically distinct subclasses of muscarinic responses in cerebral cortical neurons. Soc. Neurosci. Abstr. 11: 1098.
- Mesulam, M. M., E. J. Mufson, A. I. Levey and B. H. Wainer (1984) Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Neuroscience 12: 669–686.
- Mesulam, M. M., E. J. Mufson, A. I. Levey and B. H. Wainer (1983a) 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.
- Mesulam, M. M., E. J. Mufson, B. H. Wainer and A. I. Levey (1983b) Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Chl-Ch6). Neuroscience 10: 1185–1201.
- Mitzdorf, U., and W. Singer (1978) Prominent excitatory pathway in the cat visual cortex (A17 and A18): A current source density analysis of electrically evoked potentials. Exp. Brain Res. 33: 371–394.
- Molliver, M. E., R. Grzanna, H. G. W. Lidov, J. H. Morrison, and J. A. Olschowka (1982) Monoamine systems in the cerebral cortex. In V. Chan-Palay and S. L. Palay (eds): Cytochemical Methods in Neuroanatomy. New York: Alan R. Liss, pp. 255–277.
- Otsuka, R., and R. Hassler (1962) Über Aufbau and Gliederung der corticalen Sehsphäre bei der Katze. Archiv Psychiatr. Z. Ges. Neurologie 203: 212–234.
- Parnavelas, J. G., H. C. Moises and S. G. Speciale (1985) The monoaminergic innervation of the rat visual cortex. Proc. R. Soc. Lond. B223: 319–329.
- Schmitt, F. O. (1984) Molecular regulators of brain function: A new view. Neuroscience 13: 991–1001.
- Shute, C. C. D. and P. R. Lewis (1967) The ascending cholinergic reticular system: Neocortical, olfactory and subcortical projections. Brain 90: 497–522.
- Sillito, A. M. and J. A. Kemp (1983) Cholinergic modulation of the functional organization of the cat visual cortex. Brain Res. 289: 143–155.
- Sillito, A. M., T. E. Salt and J. A. Kemp (1985) Modulatory and inhibitory processes in the visual cortex. Vision Res. 25: 375–381.
- Singer, W. (1979) Central-core control of visual-cortex functions. In F. O. Schmitt and F. G. Worden (eds): The Neurosciences Fourth Study Program. Cambridge, MA: MIT Press, pp. 1093–1110.
- Singer, W., F. Tretter, and M. Cynader (1976) The effect of reticular stimulation on spontaneous and evoked activity in the cat visual cortex. Brain Res. 102: 71–90.
- Stichel, C. C., and W. Singer (1995) Organization and morphological characteristics of choline acetyltransferase-containing fibers in the visual thalamus and striate cortex of the cat. Neurosci. Lett. 53: 155–160.
- Vacca, L. L., S. J. Abrahams and N. E. Naftchi (1980) A modified peroxidase-anti-peroxidase procedure for improved localization of tissue antigens: Localization of substance P in rat spinal cord. J. Histochem. Cytochem. 28: 297–307.
- Vincent, S. R., K. Satoh, D. M. Armstrong and H. C. Fibiger (1983) Substance P in the ascending cholinergic reticular system. Nature 306: 688–691.
- Wahle, P., C. Sanides-Buchholtz, F. Eckenstein, and K. Albus (1984) Concurrent visualization of choline acetyltransferase-like immunoreactivity and retrograde transport of neocortically injected markers in basal forebrain neurons of cat and rat. Neurosci. Lett. 44: 223–228.
- Wainer, B. H., J. P. Bolam, T. F. Freund, Z. Henderson, S. Totterdell and A. D. Smith (1984) Cholinergic synapses in the rat brain: A correlated light and electron microscopic immunohistochemical study employing a monoclonal antibody against choline acetyltransferase. Brain Res. 308: 69–76.
- Winfield, D. A., K. C. Gatter and T. P. S. Powell (1980) An electron microscopic study of the types and proportions of neurons in the cortex of the motor and visual areas of the cat and rat. Brain 103: 245–258.
- Woolf, N. J., F. Eckenstein and L. L. Butcher (1983) Cholinergic projections from the basal forebrain to the frontal cortex: A combined fluorescent tracer and immunohistochemical analysis in the rat. Neurosci. Lett. 40: 93–98.