Elsevier

Neuroscience

Volume 67, Issue 1, July 1995, Pages 125-134
Neuroscience

Changes in the pattern of glutamate-like immunoreactivity in rat superior colliculus following retinal and visual cortical lesions

https://doi.org/10.1016/0306-4522(95)00057-PGet rights and content

Abstract

We have investigated the pattern of glutamate-like immunoreactivity in the superficial layers of the rat superior colliculus by means of postembedding immunocytochemical methods for light and electron microscopy. At the light microscopic level, labelling was faintly to moderately intense in most perikarya of the stratum zonale, stratum griseum superficiale and stratum opticum. Furthermore, strong glutamate-immunoreactive terminal-like elements were accumulated most densely in stratum zonale, stratum griseum superficiale and stratum opticum. At the electron microscopic level, a postembedding immunogold method revealed that the vast majority of those labelled elements corresponded to retinal and visual cortical terminals. These profiles were about twice as heavily labelled as their postsynaptic partners.

To determine the contribution of retinal and cortical afferents to the pattern of glutamate-like immunoreactivity, rats were subjected to right retinal ablation, left cortical ablation or combined right retinal and left cortical ablations. After retinal ablation, strongly labelled perikarya were observed in the retinorecipient layers. Furthermore, a prominent loss of glutamate-immunoreactive terminal-like elements occurred in stratum zonale and stratum griseum superficiale. Ipsilateral superior colliculus to cortical ablation exhibited subtle changes characterized by a moderate increase in perikaryal immunostaining in stratum zonale, stratum griseum superficiale and stratum opticum and by an apparent discrete reduction of labelled dots in stratum griseum superficiale and stratum opticum. In cases with combined lesions, strongly immunoreactive cell bodies and dendrites were accompanied by a massive disappearance of labelled terminal-like elements in stratum zonale, stratum griseum superficiale and stratum opticum.

The effect of retinal and visual cortical ablations on the pattern of glutamate-like immunoreactivity suggests that these afferents are the major sources for glutamate-immunoreactive terminals in the rat superior colliculus. In addition, these findings provide further evidence for glutamate as neurotransmitter in the visual pathways studied.

References (43)

  • OlavarríaJ. et al.

    The projection from striate and extrastriate cortical areas to the superior colliculus in the rat

    Brain Res.

    (1982)
  • ReubiJ.C.

    Comparative study of the release of glutamate and GABA, newly synthesized from glutamate, in various regions of the central nervous system

    Neuroscience

    (1980)
  • RobertsW.A. et al.

    Excitatory amino acid receptors mediate synaptic responses to visual stimuli in superior colliculus neurones of the rat

    Neurosci. Lett.

    (1991)
  • SakuraiT. et al.

    Selective reduction of glutamate in the rat superior colliculus and dorsal lateral geniculate nucleus after contralateral enucleation

    Brain Res.

    (1992)
  • SeftonA.J. et al.

    Cortical projections to visual centres in the rat: an HRP study

    Brain Res.

    (1981)
  • SomogyiP. et al.

    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

    (1986)
  • TsaiG. et al.

    Selective release of N-acetylaspartylglutamate from rat optic nerve terminalsin vivo

    Brain Res.

    (1990)
  • VrensenG. et al.

    Quantitative aspects of the synaptic organization of the superior colliculus in control and dark-reared rabbits

    Brain Res.

    (1977)
  • BinnsK.E. et al.

    Excitatory amino acid receptors participate in synaptic transmission of visual responses in the superficial layers of the cat superior colliculus

    Eur. J. Neurosci.

    (1994)
  • Bliss TiemanS. et al.

    N-acetylaspartyglutamate immunoreactivity in neurons of the monkey's visual pathway

    J. comp. Neurol.

    (1991)
  • CanzekV. et al.

    In vivo release of glutamate and aspartate following optic nerve stimulation as determined by a mass fragmentographic technique

    Nature

    (1981)
  • Cited by (21)

    • Cholinergic nervous system and glaucoma: From basic science to clinical applications

      2019, Progress in Retinal and Eye Research
      Citation Excerpt :

      The neurotransmitter spectrum of RGCs is, in large part, unknown due to many reasons. RGCs have been verified to be immunoreactive to glutamate by many studies with its positive signals in the cell bodies (Crooks and Kolb, 1992; Davanger et al., 1991; Jojich and Pourcho, 1996; Kalloniatis and Fletcher, 1993; Sun and Crossland, 2000) as well as axon terminals (Beaudet et al., 1981; Ehinger, 1981; Mize and Butler, 1996; Montero, 1994; Ortega et al., 1995). These observations have strengthened the indication of glutamate excitotoxicity-mediated mechanism of glaucoma, despite the fact that the exact role of glutamate signaling in RGCs is still elusive.

    • Inflammatory responses in the rat superior colliculus after eye enucleation

      2014, Brain Research Bulletin
      Citation Excerpt :

      Several studies have suggested that ocular enucleation results in profound alterations in the SC. In the rat, it has been demonstrated that eye enucleation causes selective decrease in the immunoreactivity for glutamate receptors into the contralateral SC (Kim and Jeon, 1999; Ortega et al., 1995). The volume of stratum griseum superficiale (SGS), one of the superficial layers of the SC, was reduced by about 40% on the side contralateral to the enucleated eye, in the same way as the numerical density of neurons (Smith and Bedi, 1997).

    • Eye enucleation activates the transcription nuclear factor kappa-B in the rat superior colliculus

      2012, Neuroscience Letters
      Citation Excerpt :

      As this transcription factor acts broadly influencing gene expression events that impact cell survival, it is likely to contribute to the intense plastic activity occurring after such lesions, even in adult animals, a hypothesis that remains yet to be directly tested. Among a variety of different stimuli, it is particularly important to mention glutamate as well as reactive oxygen species (ROS) as relevant inducers of NF-κB activation [6], since they have been described in retinorecipient structures after retinal lesions [20,23,10]. Although this study did not include an attempt to establish a direct relationship between glutamate and ROS on NF-κB activation, these data may lead to the speculation that both could be involved in NF-κB activation after retinal removal.

    • Same-session functional assessment of rat retina and brain with manganese-enhanced MRI

      2011, NeuroImage
      Citation Excerpt :

      Data from negative control regions were tested in the same fashion. To coarsely relate functional data to histological boundaries, cortical and SC layer thicknesses were derived from previous literature and averaged as in Bissig and Berkowitz (2009) (cortex: Gabbot and Stewart, 1987; Kreig, 1946; Zilles, 1985; SC: Ortega et al., 1995; Pellegrino et al., 1979; Toga and Collins, 1981). As for the retina, tests for stimulation-dependent layer-specific retinal manganese uptake were combined across experiments using the weighted Z-transform method.

    View all citing articles on Scopus
    View full text