Elsevier

Neuroscience

Volume 76, Issue 2, January 1997, Pages 503-515
Neuroscience

Postnatal development of GABA-immunoreactive terminals in the reticular and ventrobasal nuclei of the rat thalamus: A light and electron microscopic study

https://doi.org/10.1016/S0306-4522(96)00376-4Get rights and content

Abstract

The postnatal development of inhibitory GABAergic circuits in the thalamic reticular and ventrobasal nuclei was studied in rats ranging from the day of birth to the end of the third postnatal week by means of a postembedding immunogold staining procedure to visualize GABA. In the reticular nucleus, GABA labeling was present from birth in cell bodies, dendrites, growth cones and a few synaptic terminals, whereas in the ventrobasal nucleus it was exclusively in axonal processes identifiable as growth cones, vesicle-rich profiles and synaptic terminals. In both nuclei, GABA-labeled synaptic terminals were, however, very scarce and immature in neonatal animals and they became numerous and morphologically mature only after the end of the second postnatal week.

These findings suggest that inhibitory synaptic responses in the somatosensory thalamus are not yet fully mature throughout the first two postnatal weeks and support the hypothesis that GABA may initially play trophic roles. The relatively late maturation of the thalamic GABAergic system may have important functional consequences, as the reticulothalamic circuits are responsible for the generation of spindle wave oscillations whose cellular mechanisms are also involved in the generation of spike-and-wave (absence) seizures in humans and in animal models.

References (54)

  • KillackeyH.P.

    The development of trigeminothalamic projections

  • KristtD.A.

    Acetylcholinesterase in immature thalamic neurons: relation to afferentation, development, regulation and cellular distribution

    Neuroscience

    (1989)
  • LauderJ.M. et al.

    Prenatal ontogeny of the GABAergic system in the rat brain: an immunocytochemical study

    Neuroscience

    (1986)
  • LoTurcoJ.J. et al.

    GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis

    Neuron

    (1995)
  • McCormickD.A.

    Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity

    Prog. Neurobiol.

    (1992)
  • McLaughlinB.J. et al.

    The fine structural localization of glutamate decarboxylase in developing axonal processes and presynaptic terminals of rodent cerebellum

    Brain Res.

    (1975)
  • MitrofanisJ. et al.

    New views of the thalamic reticular nucleus in the adult and the developing brain

    Trends Neurosci.

    (1993)
  • SaltT.E.

    Gamma-aminobutyric acid and afferent inhibition in the cat and rat ventrobasal thalamus

    Neuroscience

    (1989)
  • SpreaficoR. et al.

    Electrophysiological characteristics of morphologically identified reticular thalamic neurons from rat slices

    Neuroscience

    (1988)
  • SpreaficoR. et al.

    Distribution of AMPA selective glutamate receptors in the thalamus of adult rats and during postnatal development. A light and ultrastructural immunocytochemical study

    Devl Brain Res.

    (1994)
  • Van HuizenF. et al.

    Indications for a critical period for synapse elimination in developing rat cerebral cortex cultures

    Devl Brain Res.

    (1987)
  • WesaJ.M. et al.

    Synaptic contact curvature: effects of differential rearing on rat occipital cortex

    Devl Brain Res.

    (1982)
  • ZhangJ.H. et al.

    Different postnatal ontogenetic profiles of neurons containing β β1 β2 and β3) subunit mRNAs of GABAA receptor in the rat thalamus

    Devl Brain Res.

    (1991)
  • AsanumaC. et al.

    Light and electron microscopical evidence for a GABAergic projection from the caudal basal forebrain to the thalamic reticular nucleus in rats

    J. comp. Neurol.

    (1990)
  • BeharT. et al.

    GABA stimulates chemotaxis and chemokinesis of embryonic cortical neurons via calcium-dependent mechanisms

    J. Neurosci.

    (1996)
  • BentivoglioM. et al.

    Differential expression of the GABAA receptor complex in the dorsal thalamus and reticular nucleus: an immunohistochemical study in the adult and developing rat

    Eur. J Neurosci.

    (1991)
  • De BiasiS. et al.

    The intrinsic organization of the ventroposterolateral nucleus and related thalamic reticular nucleus of the rat: a double labeling ultrastructural investigation with gamma-amino butyric acid immunogold staining and lectin conjugated horseradish peroxidase

    Somatosensory Res.

    (1988)
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