Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-26T08:01:23.412Z Has data issue: false hasContentIssue false
  • English
  • Français

Cholinergic terminals in the cat visual cortex: Ultrastructural basis for interaction with glutamate-immunoreactive neurons and other cells

Published online by Cambridge University Press:  02 June 2009

Chiye Aoki  and
Shara Kabak
Chiye Aoki
Affiliation:
Center for Neural Science, New York University, New York
Shara Kabak
Affiliation:
Center for Neural Science, New York University, New York
Get access Rights & Permissions [Opens in a new window]

Abstract

Acetylcholine (ACh) is one of the transmitters utilized by extrathalamic afferents to modulate stimulus-driven neurotransmission and experience-dependent plasticity in the visual cortex. Since these processes also depend on the activation of glutamatergic receptors, cholinergic terminals may exert their effects via direct modulation of excitatory neurotransmission. The objective of this study was to determine whether the ultrastructural relationships between cholinergic terminals, glutamate-immunoreactive neurons, and other unlabeled cells support this idea. Sections from aldehyde-fixed visual cortex (area 17) of adult cats were immunolabled for the following molecules: (1) choline acetyltransferase (ChAT), the acetylcholine-synthesizing enzyme; (2) L-glutamate; or (3) ChAT simultaneously with L-glutamate by combining electron-microscopic immunogold and immunoperoxidase techniques. None of the cortical terminals were dually labeled, suggesting that (1) the labeling procedure was free of chemical or immunological cross reactions; and (2) glutamate immunoreactivity probably reflects the transmitter, and not metabolic, pool of L-glutamate. Comparisons between cholinergic and noncholinergic axons revealed that (1) ChAT-immunoreactive axons formed fewer identifiable synaptic contacts within single ultrathin sections (P < 0.01 using chi-square test); and (2) more of the cholinergic axons occurred directly opposed to other terminals (P < 0.0015 by chi-square test), including 21% of which resided directly across asymmetric, axo-spinous junctions. Dual labeling showed that a third of the synaptic targets for cholinergic terminals contained detectable levels of glutamate immunoreactivity. Some of the axo-spinous junctions juxtaposed to cholinergic axons also exhibited glutamate immunoreactivity presynaptically. These observations provide ultrastructural evidence for direct, cholinergic modulation of glutamatergic pyramidal neurons within the mammalian neocortex. Prevalence of juxtapositions between cholinergic terminals and axo-spinous synapses supports the following ideas: (1) ACh may modulate the release of noncholinergic transmitters, including Glu; (2) Glu may modulate ACh release; and (3) these processes may be concurrent with cholinergic modulation of glutamatergic synapses at postsynaptic sites.

Keywords

UltrastructureAcetylcholineGlutamateVisual cortexAxo-axonic contactsNonsynaptic junctionsSynaptic junctions
Type
Research Articles
Information
Visual Neuroscience , Volume 8 , Issue 3 , March 1992 , pp. 177 - 191
Copyright
Copyright © Cambridge University Press 1992

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

Aoki, C. (1989). Ultrastructural localization of cholinergic terminals and their relations to glutamatergic neurons in cat visual cortex. Association for Research in Vision and Ophthalmology Abstract 31, 40.Google Scholar
Aoki, C. & Pickel, V.W. (1989). Neuropeptide Y in the cerebral cortex and the caudate-putamen nuclei: Ultrastructural basis for inter-actions with GABAergic and non-GABAergic neurons. Journal of Neuroscience 9, 4333–4354.CrossRefGoogle Scholar
Aoki, C., Starr, A. & Kaneko, T. (1991). Identification of mitochondrial and non-mitochondrial glutaminase within select neurons and glia of rat forebrain by electron microscopic immunocytochemistry. Journal of Neuroscience Research 28, 531–548.CrossRefGoogle ScholarPubMed
Beani, L., Bianchi, C., Giacomelli, A. & Tamberi, F. (1978). Nor-adrenaline inhibition of acetylcholine release from guinea-pig brain. European Journal of Pharmacology 48, 179–193.CrossRefGoogle ScholarPubMed
Bear, M.F., Carne, K.M. & Ebner, F.F. (1985). An investigation of cholinergic circuitry in cat striate cortex using acetylcholinesterase histochemistry. Journal of Comparative Neurology 234, 411–430.CrossRefGoogle ScholarPubMed
Bear, M.F., Kleinschmidt, A., Gu, O. & Singer, W. (1990). Disruption of experience-dependent synaptic modification in striate cortex by infusion of an NMDA receptor antagonist. Journal of Neuroscience 10, 909–925.CrossRefGoogle ScholarPubMed
Beaudet, A. & Descarries, L. (1979). The monoamine innervation of rat cerebral cortex: Synaptic and nonsynaptic axon terminals. Neuroscience 8, 851–860.Google Scholar
Beaulieu, C. & Somocyi, P. (1991). Enrichment of cholinergic synaptic terminals on GABAergic neurons and coexistence of immunoreactive GABA and choline acetyltransferase in the same synaptic terminals in the striate cortex of the cat. Journal of Comparative Neurology 304, 666–680.CrossRefGoogle ScholarPubMed
Bernardo, L.S. & Prince, D.A. (1982a). Cholinergic excitation of mammalian hippocampal cells. Brain Research 249, 315–331.CrossRefGoogle Scholar
Bernardo, L.S. & Prince, D.A. (1982b). Ionic mechanisms of cholinergic excitation in mammalian hippocampal pyramidal cells. Brain Research 249, 333–344.CrossRefGoogle Scholar
Brown, D.A. & Adams, P.R. (1980). Muscarinic suppression of a novel voltage sensitive K+-current in a vertebrate neurone. Nature 283, 673–676.CrossRefGoogle Scholar
Chan, J., Aoki, C. & Pickel, V.M. (1990). Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. Journal of Neuroscience Methods 33, 113–127.CrossRefGoogle ScholarPubMed
Chesselet, M.-F. (1984). Presynaptic regulation of neurotransmitter re-lease in the brain. Neuroscience 12, 347–375.CrossRefGoogle Scholar
Conti, F.A., Rustioni, P., Petrusz, P. & Towle, A.C. (1987). Glutamate-positive neurons in the somatic sensory cortex of rats and monkeys. Journal of Neuroscience 7, 1887–1901.CrossRefGoogle ScholarPubMed
Delima, A.D. & Singer, W. (1986). Cholinergic innervation of the cat striate cortex: A choline acetyltransferase immunocytochemical analysis. Journal of Comparative Neurology 250, 324–338.CrossRefGoogle Scholar
Descarries, L., Seguela, P. & Watkins, K.C. (1991). Nonjunctional relationships of monoamine axon terminals in the cerebral cortex of adult rat. In Advances in Neuroscience I: Volume Transmission in the Brain, ed. Fuxe, K. & Agnati, L.F. pp. 53–62. New York: Raven.Google Scholar
Dinopoulos, A., Dori, I., Davies, S.W. & Parnavelas, J.G. (1989). Neurochemical heterogeneity among corticofugal and callosal projections. Experimental Neurology 105, 36–44.CrossRefGoogle ScholarPubMed
Eckenstein, F. & Baughman, R.W. (1987). Cholinergic innervation in cerebral cortex. In Cerebral Cortex, Vol 6: Further Aspects of Cortical Function, Including Hippocampus, ed. Jones, E.G. & Peters, A., pp. 129–160. New York: Plenum.CrossRefGoogle Scholar
Fagg, G.E. & Foster, A.C. (1983). Amino acid neurotransmitters and their pathways in the mammalian central nervous system. Neuroscience 9, 701–719.CrossRefGoogle ScholarPubMed
Fonnum, F. (1984). Glutamate: A neurotransmitter in mammalian brain. Journal of Neurochemistry 42, 1–11.CrossRefGoogle ScholarPubMed
Foote, S.L. & Morrison, J.H. (1987). Extrathalamic modulation of cortical function. Annual Review of Neuroscience 10, 67–95.CrossRefGoogle ScholarPubMed
Freund, T.F., Martin, K.A.C., Smith, A.D. & Somogyi, P. (1983). Glutamate decarboxylase-immunoreactive terminals of Golgiimpregnated axo-axonic cells and of presumed basket cells in synaptic contact with pyramidal neurons of the cat's visual cortex. Journal of Comparative Neurology 221, 263–278.CrossRefGoogle Scholar
Giuffrida, R. & Rustioni, A. (1989). Glutamate and aspartate immunoreactivity in cortico-cortical neurons of the sensorimotor cortex of rats. Experimental Brain Research 74, 41–46.CrossRefGoogle ScholarPubMed
Gordon, B., Mitchell, B., Mohtadi, K., Roth, E., Tseng, Y. & Turk, F. (1990). Lesions of nonvisual inputs affect plasticity, norepinephrine content and acetylcholine content of visual cortex. Journal of Neurophysiology 64, 1851–1860.CrossRefGoogle ScholarPubMed
Gray, E.G. (1959). Axo-somatic and axo-dendritic synapses of the cerebral cortex. Journal of Anatomy 93, 420–433.Google ScholarPubMed
Greul, J.M., Luhmann, H.J. & Singer, W. (1988). Pharmacological induction of use-dependent receptive field modification in the visual cortex. Science 242, 74–77.CrossRefGoogle Scholar
Halliwell, J.V. & Adams, P.R. (1982). Voltage-clamp analysis of muscarinic excitation in hippocampal neurons, Brain Research 250, 71–92.CrossRefGoogle ScholarPubMed
Hertz, L., Kvamme, E., McGeer, E.G. & Schousboe, A., ed. (1983). Glutamine, Glutamate and GABA in the Central Nervous System. New York: Liss.Google Scholar
Hokfelt, T., Martensson, R., Bjorklund, A., Kleinau, S. & Goldstein, M. (1984). Distributional maps of tyrosine-hydroxylaseimmunoreactive in the rat brain. In Handbook of Chemical Neuroanatomy: Classical Transmitters in the CNS, Part I, ed. Bjorklund, A. & Hokfelt, T., pp. 277–379. Amsterdam: Elsevier.Google Scholar
Houser, C.R., Crawford, G.D., Salvaterra, P.M. & Vaughn, V.E. (1985). Immunocytochemical localization of choline acetyltransferase in rat cerebral cortex: A study of cholinergic neurons and synapses. Journal of Comparative Neurology 234, 17–34.CrossRefGoogle ScholarPubMed
Hsu, S.M., Raine, L. & Fanger, H. (1980). Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase technique: A comparison between ABC and unlabeled antibody (PAP) procedures. Journal of Histochemistry and Cytochemistry 29, 577–580.CrossRefGoogle Scholar
Ingham, C.A., Bolam, J.O., Wainer, B.H. & Smith, A.D. (1985). A correlated light and electron microscopic study of identified cholinergic basal forebrain neurons that project to the cortex in the rat. Journal of Comparative Neurology 239, 176–192.CrossRefGoogle Scholar
Kaneko, T., Urade, Y., Watanabe, Y. & Mizuno, N. (1987). Production, characterization, and immunohistochemical applications of monoclonal antibodies to glutaminase purified from rat brain. Journal of Neuroscience 7, 302–309.CrossRefGoogle ScholarPubMed
Kimura, H., McGeer, P.L. & Peng, J.-H. (1984). Choline acetyltransferase-containing neurons in the rat brain. In Handbook of Chemical Neuroanatomy: Classical Transmitters and Transmitter Receptors in the CNS, Part II, ed. Bjorklund, A., Hokfelt, T. & Kuhar, M.J., pp. 51–67. Amsterdam: Elsevier.Google Scholar
King, J.C., Lechan, R.M., Kugel, G. & Anthony, E.L.P. (1983). Acrolein: A fixative for immunocytochemical localization of peptides in the central nervous system. Journal of Histochemistry and Cytochemistry 31, 62–68.CrossRefGoogle ScholarPubMed
Kleinschmidt, A., Bear, M.F. & Singer, W. (1987). Blockade of “NMDA” receptors disrupts experience-dependent plasticity of kitten striate cortex. Science 238, 355–358.CrossRefGoogle ScholarPubMed
Krnjevic, K. (1984). Neurotransmitters in cerebral cortex. In Cerebral Cortex, Vol. 2: Functional Properties of Cortical Cells, ed. Jones, E.G. & Peters, A., pp. 39–62. New York: Plenum.CrossRefGoogle Scholar
Krnjevic, K. & Phillis, J.W. (1963). Acetylcholine-sensitive cells in the cerebral cortex. Journal of Physiology (London) 166, 296–327.CrossRefGoogle ScholarPubMed
Larsson, L.I. (1981). A novel immunocytochemical model system for specificity and sensitivity screening of antisera against multiple antigens. Journal of Histochemistry and Cytochemistry 29, 408–410.CrossRefGoogle ScholarPubMed
Masurovsky, E.R. & Bunge, R.P. (1968). Fluoroplastic coverslips for long-term nerve tissue culture. Stain Technology 43, 161–165.CrossRefGoogle ScholarPubMed
McCormick, D. (1989). Cholinergic and noradrenergic modulation of thalamocortical processing. Trends in Neuroscience 12, 215–221.CrossRefGoogle ScholarPubMed
McDermott, A.B. & Dale, N. (1987). Receptors, ion channels and synaptic potentials underlying the integrative actions of excitatory amino acids. Trends in Neuroscience 10, 280–284.CrossRefGoogle Scholar
Moore, R.Y. & Card, J.P. (1984). Noradrenaline-containing neuron systems. In Handbook of Chemical Neuroanatomy: Classical Transmitters in the CNS, Part I, ed. Bjorklund, A. & Hokfelt, T., pp. 123–156. Amsterdam: Elsevier.Google Scholar
Mugnaini, E. & Oertel, W.H. (1985). An atlas of the distribution of GABAergic neurons and terminals in the rat CNS as revealed by GAD immunohistochemistry. In Handbook of Chemical Neuro-anatomy: GABA and Neuropeptides in the CNS, Part I, ed. Bjork-Lund, A. & Hokfelt, T. pp. 436–608. Amsterdam: Elsevier.Google Scholar
Oertel, W.H., Mugnaini, E., Schmechel, D.E., Tappaz, M.L. & Kopin, L.J. (1982). Immunocytochemical demonstration of gamma aminobutyric acid-ergic neurons—methods and application. In Cytochemical Methods in Neuroanatomy, pp. 297–329. New York: Liss.Google Scholar
O'Malley, D.M. & Masland, R.H. (1989). Co-release of acetylcholine and gamma-aminobutyric acid by a retinal neuron. Proceedings of the National Academy of Sciences of the U.S.A. 86, 3414–3418.CrossRefGoogle ScholarPubMed
Ottersen, O.P. & Storm-Mathisen, J. (1984). Glutamate and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique. Journal of Comparative Neurology 229, 374–392.CrossRefGoogle ScholarPubMed
Palay, S.L. (1991). The meaning of synaptic architecture. In Advances in Neuroscience I: Volume Transmission in the Brain, ed. Fuxe, K. & Agnati, L.F., pp. 49–52. New York: Raven.Google Scholar
Peters, A., Palay, S.L. & Webster, H.De F. (1991). The Fine Structure of the Nervous System, 3rd ed., Oxford: Oxford University Press.Google Scholar
Phelps, P.E., Houser, C.F. & Vaughn, J.F. (1985). Immunocytochemical localization of choline acetyltransferase within the rat neostriatum: A correlated light and electron microscopic study of cholinergic neurons and synapses. Journal of Comparative Neurology 238, 286–307.CrossRefGoogle ScholarPubMed
Pickel, V.M. (1981). Immunocytochemical methods. In Neuroanatomical Tract-Tracing Methods, ed. Heimer, L. & Robards, M.J. pp. 483–509. New York: Plenum.CrossRefGoogle Scholar
Sato, H., Hata, Y., Masui, H. & Tsumoto, T. (1987). A functional role of cholinergic innervation to neurons in the cat visual cortex. Journal of Neurophysiology 58, 765–780.CrossRefGoogle ScholarPubMed
Schousboe, A., Larsson, O.M., Drejer, J., Krogsgaard-Larsen, P. & Hertz, L. (1983). Uptake and release process for glutamine, glutamate and GABA in cultured neurons and astrocytes. In Glutamine, Glutamate and GABA in the Central Nervous System, ed. Hertz, L., Kvamme, E., McGeer, E.G. & Schousboe, A., pp. 297–315. New York: Liss.Google Scholar
Shaw, C., Wilkinson, W., Cynader, M., Needler, M.C., Aoki, C. & Hall, S.E. (1986). The laminar distributions and postnatal development of neurotransmitter and neuromodulator receptors in cat visual cortex. Brain Research Bulletin 16, 661–671.CrossRefGoogle ScholarPubMed
Sherrington, C.S. (1906). The Integrative Action of the Nervous System, New Haven, Connecticut: Yale University Press.Google Scholar
Sillito, A.M. & Kemp, J.A. (1983). Cholinergic modulation of the functional organization of the cat visual cortex. Brain Research 289, 143–155.CrossRefGoogle ScholarPubMed
Sillito, A.M. & Murphy, P.C. (1987). The cholinergic modulation of cortical function. In Cerebral Cortex, Vol. 6: Further Aspects of Cortical Function, Including Hippocampus, ed. Jones, E.G. & Peters, A., pp. 161–185. New York: Plenum.CrossRefGoogle Scholar
Snell, L.D. & Johnson, K.M. (1986). Characterization of the inhibition of excitatory amino acid-induced neurotransmitter release in the rat striatum of phencyclidine-like drugs. Journal of Pharmacology and Experimental Therapeutics 238, 938–946.Google ScholarPubMed
Somogyi, P. & Soltesz, I. (1986). Immunogold demonstration of GABA in synaptic terminals of intracellularly recorded, horseradish peroxidase-filled basket cells and clutch cells in the cat's visual cortex. Neuroscience 19, 1051–1065.CrossRefGoogle ScholarPubMed
Somogyi, P., Freund, T.F., Wu, J.Y. & Smith, A.D. (1983). The section-Golgi impregnation procedure: 2. Immunocytochemical demonstration of glutamate decarboxylase in Golgi-impregnated neurons and in their afferent synaptic boutons in the visual cortex of the cat. Neuroscience 9, 475–490.CrossRefGoogle ScholarPubMed
Spehlmann, R. (1971). Acetylcholine and the synaptic transmission of non-specific impulses to the visual cortex. Brain Research 94, 139–150.Google Scholar
Sternberger, L.A. (1981). Immunocytochemistry. New York: Wiley.Google Scholar
Stichel, C.C. & Singer, W. (1985). Organization and morphological characteristics of ChAT-containing fibers in the visual thalamus and striate cortex of the cat. Neuroscience Letters 53, 155–160.CrossRefGoogle Scholar
Streit, P. (1984). Glutamate and aspartate as transmitter candidates for systems of the cerebral cortex. In Cerebral Cortex, Vol. 2: Functional Properties of Cortical Cells, ed. Jones, E.G. & Peters, A., pp. 119–143. New York: Plenum.CrossRefGoogle Scholar
Tigges, J. & Tigges, M. (1985). Subcortical sources of direct projections to visual cortex. In Cerebral Cortex, Vol. 3: Visual Cortex, ed. Jones, E.G. & Peters, A., pp. 351–378. New York: Plenum.Google Scholar
Tsumoto, T. (1990). Excitatory amino acid transmitters and their receptors in neural circuits of the cerebral cortex. Neuroscience Research 9, 79–102.CrossRefGoogle Scholar
Tsumoto, T., Masui, H. & Sato, H. (1986). Excitatory amino acid transmitters in neuronal circuits of the cat visual cortex. Journal of Neurophysiology 55, 469–483.CrossRefGoogle ScholarPubMed
Tusa, R., Palmer, L.A. & Rosenquist, A.L. (1981). Multiple cortical visual areas: Visual field topography in the cat. In Cortical Sensory Organization, Vol. 2, ed. Woolsey, C.N., pp. 1–31. New Jersey: Humana.Google Scholar
Vizi, E.S. (1980). Modulation of cortical release of acetylcholine by nor-adrenaline released from nerve arising from the rat locus coeruleus. Neuroscience 5, 2139–2144.CrossRefGoogle ScholarPubMed
Vizi, E.S. (1991). Nonsynaptic inhibitory signal transmission between axon terminals: Physiological and pharmacological evidence. In Volume Transmission in the Brain: Novel Mechanisms for Neural Transmission, ed. Fuxe, K. & Agnati, L.F., pp. 89–96. New York: Raven.Google Scholar
White, E.L. (1989). Cortical Circuits: Synaptic Organization of the Cerebral Cortex; Structure, Function, and Theory. Boston: Birkhäuser.CrossRefGoogle Scholar