Elsevier

Neuroscience

Volume 22, Issue 2, August 1987, Pages 425-439
Neuroscience

Excitatory amino acid projections to the nucleus accumbens septi in the rat: A retrograde transport study utilizingd[3H]aspartate and [3H]GABA

https://doi.org/10.1016/0306-4522(87)90345-9Get rights and content

Abstract

Afferents to the nucleus accumbens septi utilizing glutamate or aspartate have been investigated in the rat by autoradiography following injection and retrograde transport ofd[3H]aspartate. Parallel experiments with the intra-accumbal injection of [3H]GABA were employed to establish the transmitterselective nature of the retrograde labelling found withd[3H]aspartate.

The topography of cortical and thalamic perikarya labelled byd[3H]aspartate was extremely precise.d[3H]Aspartate labelled perikarya were found in layer V of agranular insular cortex; bilaterally within prelimbic and infralimbic subareas perikarya, but predominantly ipsilaterally. Ipsilateral labelling was observed in dorsal, ventral and posterior agranular insular cortices, and in perirhinal cortex. Injections into ventral accumbens labelled perikarya in ipsilateral entorhinal cortex, while infusion ofd[3H]aspartate into anterior caudate-putamen resulted in labelling of perikarya in ipsilateral cingulate and lateral precentral cortices. Following infusion ofd[3H]aspartate, ipsilateral midline thalamic nuclei contained the highest density of labelled perikarya; infusions centred on nucleus accumbens resulted in heavy retrograde labelling of the parataenial nucleus, but labelling was sparse from a lateral site and not observed after injection into anterior caudate-putamen. Less prominent labelling of perikarya was seen in other thalamic nuclei (mediodorsal, central medial, rhomboid, reuniens and centrolateral), mostly near the midline. Perikaryal labelling was also found in the ipsilateral amygdaloid complex, particularly in basolateral and lateral nuclei. Only weak labelling resulted in ventral subiculum. Numerous labelled cells were present bilaterally in anterior olfactory nucleus, although perikarya were more prominent ipsilaterally. Labelled perikarya were not consistently observed in other regions (ventral tegmental area, medial substantia nigra, raphe nuclei and locus coeruleus) known to innervate nucleus accumbens. Presumptive anterograde labelling was detected in ventral pallidum/substantia innominata, ventral tegmental area and medial substantia nigra. [3H]GABA was generally not retrogradely transported to the same regions labelled byd[3H]aspartate; an exception being the anterior olfactory nucleus, where large numbers of labelled perikarya were found. [3H]GABA failed to label perikarya in thalamus and amygdala, and a topographic distribution of label was absent in neocortex.

Overall our findings confirm the selectivity of the retrograde transport ofd[3H]aspartate and [3H]GABA, and provide the first evidence that thalamic and amygdaloid afferents to nucleus accumbens utilize glutamate and/or aspartate as their transmitter. They also confirm previous evidence that corticofugal afferents to nucleus accumbens utilize an excitatory amino acid. Afferents from anterior olfactory nucleus to nucleus accumbens have not been previously described.

Reference (56)

  • SwansonL.W. et al.

    A note on the connections and development of the nucleus accumbens

    Brain Res.

    (1975)
  • VeeningJ.G. et al.

    The topical organization of the afferents to the caudatoputamen of the rat. A horseradish peroxidase study

    Neuroscience

    (1980)
  • WalaasI. et al.

    The effects of surgical and chemical lesions on neurotransmitter candidates in the nucleus accumbens of the rat

    Neuroscience

    (1979)
  • BalcarV.J. et al.

    The structural specifity of the high affinity uptake ofl-glutamate andl-aspartate by rat brain slices

    J. Neurochem.

    (1972)
  • BecksteadR.M.

    An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal-projection (prefrontal) cortex in the rat

    J. comp. Neurol.

    (1979)
  • BroadwellR.D.

    Olfactory relationships of the telencephalon and diencephalon in the rat. II. An autoradiographic and horseradish peroxidase study of the efferent connections of the anterior olfactory nucleus

    J. comp. Neurol.

    (1975)
  • CarmanJ.B. et al.

    The organization of corticostriate connexions in the rabbit

    Brain

    (1963)
  • CarpenterM.B. et al.

    Study of methods for producing experimental lesions in the central nervous system with special reference to stereotaxic technique

    J. comp. Neurol.

    (1952)
  • ChristieM.J. et al.

    An excitant amino acid projection from the medial prefrontal cortex to the anterior part of the nucleus accumbens in the rat

    J. Neurochem.

    (1985)
  • ChristieM.J. et al.

    Autoradiographic mapping of excitatory amino acid projections to the rat nucleus accumbens by retrograde transport ofd[3H]aspartate

  • ChungJ.W. et al.

    Degenerated boutons in the Fundus striati (Nucleus accumbens septi) after lesion of the parafascicular nucleus in the cat

    Cell Tiss. Res.

    (1976)
  • ChronisterR.B. et al.

    The organization of nucleus accumbens

  • CuenodM. et al.

    Neuronal tracing using retrograde migration of labelled transmitter-related compounds

  • DaviesL.P. et al.

    Uptake and release ofd- andl-aspartate by rat brain slices

    J. Neurochem.

    (1976)
  • de OlmosJ.S. et al.

    The afferent connections of the main and the accessory olfactory bulb formations in the rat: an experimental HRP-study

    J. comp. Neurol.

    (1978)
  • DomesickV.B.

    Further observations on the anatomy of nucleus accumbens and caudatoputamen in the rat: similarities and contrasts

  • DonoghueJ.P. et al.

    Localization of glutaminase-like and aspartate aminotransferase-like immunoreactivity in neurons of cerebral neocortex

    J. Neurosci.

    (1985)
  • FonnumF.

    Glutamate: a neurotransmitter in mammalian brain

    J. Neurochem.

    (1984)
  • Cited by (289)

    • Striatal circuits

      2022, Neurocircuitry of Addiction
    View all citing articles on Scopus
    *

    Present address: Neuropharmacology Laboratory, Department of Applied Biological Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, U.S.A.

    View full text