Elsevier

Brain Research Bulletin

Volume 13, Issue 2, August 1984, Pages 269-285
Brain Research Bulletin

Ultrastructural morphology of dopaminergic nerve terminals and synapses in the striatum of the rat using tyrosine hydroxylase immunocytochemistry: A topographical study

https://doi.org/10.1016/0361-9230(84)90128-XGet rights and content

Abstract

Structures immunoreactive for TH were examined in the rat striatum (including caudateputamen, nucleus accumbens and globus pallidus) by electron microscopy using the indirect peroxidase-labeled antibody method. Axon profiles and nerve terminals were the only structures stained by DAB precipitates in the axoplasm. The reactive boutons frequently contained a population of large pleomorphic vesicles (40–60 nm in diameter) but their interiors remained free of reactions. The synaptic contacts formed belonged principally to the symmetric type 2 of Gray while asymmetric Gray's type 1 synapses were rarely observed. The former were mostly apposed to dendritic trunks (rarely to perikarya) and the latter to dendritic spines. In addition, numerous immunoreactive nerve terminals were often found in close contact with small structures identified as the neck of dendritic spines. The active zone of these presumed synapses was characterized by a prominent thickening of the presynaptic membrane but the post-synaptic thickening was lacking. For similar reasons, it was difficult to assert the existence of one axo-axonic synapse when a positive nerve terminal was closely apposed to another one (generally unreactive). The exact morphology of dopaminergic synapses, or even their existence, have not been firmly established owing to large discrepancies between previous reports. No synapses, or synaptic contacts of either asymmetric or symmetric type were described according to the technique used. Our work was undertaken to elucidate further this problem, and in particular, we thought that regional differences in the synaptic organization might explain the divergent data. However, regional quantitative analysis performed in this study did not show significant differences in the percentage of either kind of synapses in the various striatal regions.

References (91)

  • M. Goldstein et al.

    The effects of the ventromedial tegmental lesions on the disposition of dopamine in the caudate nucleus of the monkey

    Brain Res

    (1967)
  • P.M. Groves

    A theory of the functional organization of the neostriatum and the neostriatal control of voluntary movement

    Brain Res Rev

    (1983)
  • N. Halàsz et al.

    Transmitter histochemistry of the rat olfactory bulb. I. Immunocytochemical localization of monoamine synthesizing enzymes. Support for intrabulbar, periglomerular dopamine neurons

    Brain Res

    (1977)
  • L. Heimer et al.

    Ventral striatum and ventral pallidum components of the motor system

    Trends Neurosci

    (1982)
  • T. Hökfelt et al.

    A subpopulation of mesencephalic dopamine neurons projecting to limbic areas contains cholecystokinin like peptide: evidence from immunohistochemistry combined with retrograde tracing

    Neuroscience

    (1980)
  • B.H. Hwang et al.

    Characterisation of monoaminergic terminals in the neostriatum of neonatal rats: an electron microscopic morphometric analysis

    Dev Brain Res

    (1982)
  • T.H. Joh et al.

    Different forms of tyrosine hydroxylase in central dopaminergic and noradrenergic neurons and sympathetic ganglia

    Brain Res

    (1975)
  • H. Kaiya et al.

    Two types of dopaminergic nerve terminals in the rat neostriatum

    Neurosci Lett

    (1981)
  • G.F. Koob et al.

    Dopamine and norepinephrine levels in the nucleus accumbens olfactory tubercle and corpus striatum following lesions in the ventral tegmental area

    Brain Res

    (1975)
  • R.T. Kuczenski et al.

    Regulatory properties of soluble and particulate rat brain tyrosine hydroxylase

    J Biol Chem

    (1972)
  • W.D. Kuhlmann et al.

    A comparative study for ultrastructural localization of intra cellular immunoglobulins using peroxidase conjugates

    J Immunol Methods

    (1974)
  • O. Lindvall et al.

    Dopaminergic innervation of the globus pallidus by collaterals from the nigrostriatal pathway

    Brain Res

    (1979)
  • O. Lindvall et al.

    Organization of catecholamine neurons projecting to the frontal cortex in the rat

    Brain Res

    (1978)
  • A. Ljungdahl et al.

    Retrograde peroxidase tracing of neurons combined with transmitter histochemistry

    Brain Res

    (1975)
  • K. Norcross et al.

    A quantitative analysis of the excitatory and depressant effect of dopamine on the firing of caudate neurons: electrophysiological evidence for the existence of two distinct dopamine sensitive receptors

    Brain Res

    (1978)
  • V.M. Pickel et al.

    Ultrastructural immunocytochemical localization of tyrosine hydroxylase in the neostriatum

    Brain Res

    (1981)
  • V.M. Pickel et al.

    Immunohistochemical localization of tyrosine hydroxylase in brain by light and electron microscopy

    Brain Res

    (1975)
  • L.J. Poirier et al.

    Effect of amine precursors on the concentration of striatal dopamine and serotonin in cats with and without unilateral brainstem lesions

    Brain Res

    (1967)
  • H. Pollard et al.

    Localization of opiate receptors and enkephalins in the rat striatum in relationship with the nigrostriatal dopaminergic system: lesion studies

    Brain Res

    (1978)
  • P. Redgrave et al.

    Functional validation of projection topography in the nigrostriatal dopamine system

    Neurosci

    (1982)
  • H. Simon et al.

    Silver impregnation of dopaminergic systems after radiofrequency and 6-OH-DA lesions of the rat ventral tegmentum

    Brain Res

    (1976)
  • H. Simon et al.

    Efferents and afferents of the ventral tegmental region studied after injection of 3H-leucine and horseradish peroxidase

    Brain Res

    (1979)
  • L.A. Specht et al.

    Fine structure of the nigrostriatal anlage in foetal brain by immunocytochemical localization of tyrosine hydroxylase

    Brain Res

    (1981)
  • L.W. Swanson

    The projections of the ventral tegmental area and adjacent regions. A combined fluorescence retrograde tracer and immunofluorescence study in the rat

    Brain Res Bull

    (1982)
  • V.M. Tennyson et al.

    5-hydroxydopamine “tagged” neuronal boutons in rabbit neostriatum interrelationship between vesicles and axonal membrane

    Brain Res

    (1974)
  • J. Thibault et al.

    In vitro translation of m-RNA from rat pheochromocytoma tumors, characterization of tyrosine-hydroxylase

    Biochem Biophys Res Commun

    (1981)
  • U. Ungerstedt

    6-hydroxydopamine induced degeneration of central monoamine neurons

    Eur J Pharmacol

    (1968)
  • J.G. Veening et al.

    The typical organization of the afferents to the caudate-putamen of the rat. A horseradish peroxidase study

    Neuroscience

    (1980)
  • C. Verney et al.

    Development of the dopaminergic innervation of the rat cerebral cortex: a light microscopic immunocytochemical study using antityrosine hydroxylase antibodies

    Develop. Brain Res

    (1982)
  • P.F. Von Voigtlander et al.

    Nigro-striatal pathway: stimulation-evoked release of 3H-dopamine from caudate nucleus

    Brain Res

    (1971)
  • M. Arluison et al.

    Different localizations of met-enkephalin-like immunoreactivity in rat forebrain and spinal cord using hydrogen peroxide and Triton X-100. Ultrastructural study

    Brain Res Bull

    (1983)
  • M. Arluison et al.

    High-resolution radioautographic study of dopamine binding sites in the rat neostriatum using 3H-domperidone

    J Neural Transmi

    (1983)
  • I.J. Bak et al.

    The fine structural synaptic organization of the corpus striatum and substantia nigra in rat and cat

  • R.M. Beckstead et al.

    Efferent connections of the substantia nigra and ventral tegmental areas in the rat

    Brain Res

    (1979)
  • A. Bertler et al.

    On the distribution in brain of monoamines and of enzymes responsible for their formation

    Experientia

    (1959)
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