Elsevier

Journal of Chemical Neuroanatomy

Volume 5, Issue 1, January–February 1992, Pages 39-50
Journal of Chemical Neuroanatomy

Afferent connections of the rat substantia nigra pars lateralis with special reference to peptide-containing neurons of the amygdalo-nigral pathway

https://doi.org/10.1016/0891-0618(92)90032-LGet rights and content

Abstract

The afferent connections of the rat substantia nigra pars lateralis have been studied using the retrograde axonal transport of fluorescent latex microspheres. The most numerous groups of retrogradely labelled nerve cell bodies were observed bilaterally in the parabrachial complex and several hypothalamic nuclei, whereas the parietal neocortex, the fundus striati, the central nucleus of the amygdala and the bed nucleus of the stria terminalis were labelled on the injected side only. The neuronal projections from the central amygdaloid nucleus to the substantia nigra pars lateralis and lateral part of the rostral pars compacta have additionally been confirmed by anterograde tracing using wheat-germ agglutinin coupled to horseradish peroxidase. The presence of some peptides in this pathway was studied by combining the use of the same retrograde tracer with immunofluorescence after intra-amygdaloid injections of colchicine. With this method, we have demonstrated that Met-enkephalin, dynorphin and neurotensin are probably utilized as neurotransmitters or co-transmitters in the neurons of the amygdalo-nigral pathway.

References (47)

  • T.P. Ma

    Identification of the substantia nigra pars lateralis in the macaque using cytochrome oxidase and fibers stains

    Brain Res.

    (1989)
  • P.J. May et al.

    The sources of the nigrotectal pathway

    Neuroscience

    (1986)
  • S. McLean et al.

    Comparison of the substance P- and dynorphin-containing projections to the substantia nigra: a radioimmunocytochemical and biochemical study

    Brain Res.

    (1985)
  • G.M. Peterson et al.

    Direct neurotoxic effects of colchicine on cholinergic neurons in medial septum and striatum

    Neurosci. Lett.

    (1988)
  • L.J. Poirier et al.

    Comparative morphology of the substantia nigra and ventral tegmental area in the monkey, cat and rat

    Brain Res. Bull.

    (1983)
  • B.B. Sandrew et al.

    Amygdalospinal projections in the cat

    Brain Res.

    (1986)
  • C.B. Saper et al.

    Efferent connections of the parabrachial nucleus in the rat

    Brain Res.

    (1980)
  • J.M. Studler et al.

    Extensive colocalization of neurotensin with dopamine in rat meso-cortico-frontal dopaminergic neurons

    Neuropeptides

    (1988)
  • L.T. Weiss-Wunder et al.

    Heterogeneous distribution of cytochrome oxidase activity in the rat substantia nigra: correlation with tyrosine hydroxylase and dynorphin immunoreactivities

    Brain Res.

    (1990)
  • R.J. Adams et al.

    Rapid transport of foreign particles microinjected into crab axons

    Nature

    (1983)
  • J. De Olmos et al.

    Amygdala

  • J. Engel et al.

    Anatomical correlates of electrical and behavioral events related to amygdaloid kindling

    Ann. Neurol.

    (1978)
  • C.R. Gerfen et al.

    Crossed connections of the substantia nigra in the rat

    J. Comp. Neurol.

    (1982)
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