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Ultrastructure and synaptic relations of neural elements containing glutamic acid decarboxylase (GAD) in the perigeniculate nucleus of the cat

A light and electron microscopic immunocytochemical study

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Summary

The perigeniculate nucleus of the cat (PGN) was examined at light and electron microscopic levels after immunocytochemical labeling for the gamma-aminobutyric acid (GABA) synthesizing enzyme, glutamic acid decarboxylase (GAD). In light microscopic sections, virtually all perikarya were found to be labeled (GAD+), as well as proximal dendrites, fibres and punctiform elements. Cells in the thalamic reticular nucleus (TRN) dorsal to PGN were also labeled. Ultrastructural analysis of PGN showed immunoreactivity in all somata, in dendrites and in the following vesicle containing profiles: 1.) F1 terminals, which are characterized by large size, dark mitochondria, and pleomorphic vesicles. These terminals form symmetrical synaptic contacts with somata, somatic spines and with dendrites of GAD+ PGN cells. 2.) F2 terminals, which are smaller than F1 terminals, contain also pleomorphic vesicles and frequently make serial synapses of the symmetric type with other F2 terminals. Presumably, F1 terminals are formed by collaterals of PGN-cell axons and F2 terminals by vesicle containing dendrites of PGN cells. Terminals devoid of immunoreactivity included: 1.) RLD terminals characterized by large size, round vesicles, dark mitochondria, and by asymmetric synaptic contacts with somata, especially with somatic spines, and with dendrites of GAD+ perigeniculate neurons; 2.) RSD terminals, characterized by small size, round vesicles and dark mitochondria, which make asymmetric synapses with GAD+ dendrites of medium and small size; 3.) Multivesicular (MV) terminals with variably shaped vesicles including dense core vesicles synapsing on GAD+ dendrites. There are reasons to believe that RSD terminals belong to corticofugal axons and RLD terminals to collateral axons of LGN relay cells. The origin of MV terminals remains to be determined. The GABAergic nature of the PGN cells conforms with the presumed function of these cells as mediators of inhibition of LGN relay cells. The complex synaptic relations observed between GAD+ elements in the PGN would allow for reciprocal inhibition between perigeniculate cells.

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References

  • Ahlsen G, Lindström S (1978) Axonal branching of functionally identified neurones in the lateral geniculate body of the cat. Neurosci Lett Suppl 1: 156

    Google Scholar 

  • Ahlsen G, Lindström S (1982a) Excitation of perigeniculate neurones via axon collaterals of principal cells. Brain Res 236: 477–481

    Google Scholar 

  • Ahlsen G, Lindström S (1982b) Mutual inhibition between perigeniculate neurones. Brain Res 236: 482–486

    Google Scholar 

  • Ahlsen G, Lindström S, Sybirska E (1978) Subcortical axon collaterals of principal cells in the lateral geniculate body of the cat. Brain Res 156: 106–109

    Google Scholar 

  • Ahlsen G, Lindström S, Lo F-S (1980) Projection of brainstem neurones to the perigeniculate nucleus in the cat. Neurosci Lett Suppl 5: 292

    Google Scholar 

  • Ahlsen G, Grant K, Lindström S (1982a) Monosynaptic excitation of principal cells in the lateral geniculate nucleus by cortifugal fibers. Brain Res 234: 452–458

    Google Scholar 

  • Ahlsen G, Lindström S, Lo F-S (1982b) Functional distinction of perigeniculate and thalamic reticular neurons in the cat. Exp Brain Res 46: 118–126

    Google Scholar 

  • Barber RP, Saito K (1976) Light microscopic visualization of GAD and GABA-T in immunocytochemical preparations of rodent CNS. In: Roberts E, Chase TN, Tower DB (eds) Nervous System Function. Raven Press, New York, pp 113–132

    Google Scholar 

  • Berman AL, Jones EG (1982) The thalamus and basal telencephalon of the cat. A cytoarchitectonic atlas with stereotaxic coordinates. The University of Wisconsin Press, Madison, Wisconsin

    Google Scholar 

  • Burke W, Cole AM (1978) Extraretinal influences on the lateral geniculate nucleus. Rev Physiol Biochem Pharmacol 80: 105–166

    CAS  PubMed  Google Scholar 

  • Curtis DR, Tebecis AK (1972) Bicuculline and thalamic inhibition. Exp Brain Res 16: 210–218

    Google Scholar 

  • Dubin MW, Cleland BG (1977) The organization of visual inputs to interneurons of the lateral geniculate nucleus of the cat. J Neurophysiol 40: 410–427

    Google Scholar 

  • Famiglietti Jr. EV, Peters A (1972) The synaptic glomerulus and the intrinsic neuron in the dorsal lateral geniculate nucleus of the cat. J Comp Neurol 144: 285–334

    Google Scholar 

  • Ferster D, LeVay S (1978) The axonal arborization of lateral geniculate neurons in the striate cortex of the cat. J Comp Neurol 182: 923–944

    Google Scholar 

  • Friedlander MJ, Lin CS, Sherman SM (1979) Structure of physiologically identified X and Y cells in the cats' lateral geniculate nucleus. Science 204: 1114–1117

    Google Scholar 

  • Friedlander MJ, Lin CS, Stanford LR, Sherman M (1981) Morphology of functionally identified neurons in lateral geniculate nucleus of the cat. J Neurophysiol 46: 80–129

    Google Scholar 

  • Guillery RW (1969) The organization of synaptic interconnections in the dorsal lateral geniculate nucleus of the cat. Z Zellforsch 96: 1–38

    Google Scholar 

  • Hale PT, Jervie-Sefton A, Baur L, Cottee LJ (1982) Interrelations of the rats thalamic reticular and dorsal lateral geniculate nuclei. Exp Brain Res 45: 217–229

    Google Scholar 

  • Hendrickson AE, Hunt SP, Wu JY (1981) Immunocytochemical localization of glutamic acid decarboxylase in monkey striate cortex. Nature 292: 605–507

    Google Scholar 

  • Hendrickson AE, Ogren MP, Vaughn JE, Barber R, Wu JY (1983) Light and electron microscopic immunocytochemical localization of glutamic acid decarboxylase in monkey geniculate complex: Evidence for gabaergic neurons and synapses. J Neurosci 3: 1245–1266

    Google Scholar 

  • Houser CR, Vaughn JE, Barber R, Roberts E (1980) GABA neurons are the major cell type of the nucleus reticularis thalami. Brain Res 200: 341–354

    Google Scholar 

  • Houser CR, Hendry SHC, Jones EG, Vaughn JE (1983) Morphological diversity of immunocytochemically identified GABA neurons in the monkey sensory-motor cortex. J Neurocytol 12: 617–638

    Google Scholar 

  • Ide LS (1982a) The fine structure of the perigeniculate nucleus in the cat. J Comp Neurol 210: 317–334

    Google Scholar 

  • Ide LS (1982b) Fine structure of the thalamic reticular nucleus in the cat. Soc Neurosci Abstr 8: 261

    Google Scholar 

  • Laties AM, Sprague JM (1966) The projection of optic fibers to visual centers in the cat. J Comp Neurol 127: 35–70

    Google Scholar 

  • Lieberman AR (1973) Neurons with presynaptic perikarya and presynaptic dendrites in the rat lateral geniculate nucleus. Brain Res 59: 35–59

    Google Scholar 

  • Lindström S (1982) Synaptic organization of inhibitory pathways to principal cells in the lateral geniculate nucleus of the cat. Brain Res 234: 447–453

    Google Scholar 

  • McLaughlin BJ, Wood JG, Saito K, Barber R, Vaughn JE, Roberts E, Wu JY (1974) The fine structural localization of glutamate decarboxylase in synaptic terminals of rodent cerebellum. Brain Res 76: 377–391

    Google Scholar 

  • Montero VM (1983) Ultrastructural identification of axon terminals from the thalamic reticular nucleus in the medial geniculate body in the rat: An EM autoradiographic study. Exp Brain Res 51: 338–342

    Google Scholar 

  • Montero VM, Scott GL (1981) Synaptic terminals in dorsal lateral geniculate nucleus from neurons of the thalamic reticular nucleus. A light and electron microscope autoradiographic study. Neuroscience 6: 2561–2577

    Google Scholar 

  • Montero VM, Guillery RW, Woolsey CN (1977) Retinotopic organization within the thalamic reticular nucleus demonstrated by a double label autoradiographic technique. Brain Res 138: 407–421

    Google Scholar 

  • Morgan R, Sillito AM, Wolstencroft JH (1974) A pharmacological investigation of inhibition in the lateral geniculate nucleus. J Physiol (Lond) 246: 93–94

    Google Scholar 

  • Oertel WH, Schmechel DE, Mugnaini E, Tappaz ML, Kopin IJ (1981) Immunocytochemical localization of glutamate decarboxylase in rat cerebellum with a new antiserum. Neuroscience 6: 2715–2735

    Google Scholar 

  • Ohara PT, Liberman AR (1981) Thalamic reticular nucleus: anatomical evidence that cortico-reticular axons establish monosynaptic contact with reticulo-geniculate projection cells. Brain Rest 207: 153–156

    Google Scholar 

  • Ohara PT, Lieberman AR, Hunt SP, Wu JY (1983) Neural elements containing glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the rat; Immunohistochemical studies by light and electron microscopy. Neuroscience 8: 189–211

    Google Scholar 

  • Ribak CE, Vaughn JE, Barber R (1981) Immunocytochemical localization of GABAergic neurons at the electron microscopic level. Histochem J 13: 555–582

    Google Scholar 

  • Robson JA (1983) The morphology of corticofugal axons to the dorsal lateral geniculate nucleus in the cat. J Comp Neurol 216: 89–103

    Google Scholar 

  • Saito K, Wu JY, Matsuda T, Roberts E (1974) Immunocytochemical comparisons of vertebrate glutamic acid decarboxylase. Brain Res 65: 277–285

    Google Scholar 

  • Sanderson KJ (1971) The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat. J Comp Neurol 143: 101–118

    Google Scholar 

  • Sanderson KJ (1974) Lamination of the dorsal lateral geniculate nucleus in carnivores of the weasel (Mustelidae), raccoon (Procyonidae) and fox (Canidae) families. J Comp Neurol 153: 239–266

    Google Scholar 

  • Schmielau F (1979) Integration of visual and nonvisual information in nucleus reticularis thalami of the cat. In: Freeman RD (ed) Developmental Neurobiology of Vision. Plenum Press, New York, pp 205–266

    Google Scholar 

  • Schmielau F, Singer W (1977) The role of visual cortex for binocular interactions in the cat lateral geniculate nucleus. Brain Res 120: 354–361

    Google Scholar 

  • Singer W (1973) The effect of mesencephalic reticular stimulation on intracellular potentials of cat lateral geniculate neurons. Brain Res 61: 35–54

    Google Scholar 

  • Singer W (1977) Control of thalamic transmission by corticofugal and ascending reticular pathways in the visual system. Physiol Rev 57: 386–420

    Google Scholar 

  • So YT, Shapley R (1981) Spatial tuning of cells in and around lateral geniculate nucleus of the cat: X and Y relay cells and perigeniculate interneurons. J Neurophysiol 45: 107–119

    Google Scholar 

  • Somogyi P, Freund TF, Wu JY, Smith AD (1983) The section-Golgi impregnation procedure. 2. Immunocytochemical demonstration of glutamate decarboxylase in Golgi-impregnated neurons and in their afferent synaptic boutons in the visual cortex of the cat. Neuroscience 10: 261–294

    Google Scholar 

  • Sotelo C, Palay SL (1971) Altered axons and axon terminals in the lateral vestibular nucleus of the rat. Possible example of axonal remodeling. Lab Invest 25: 653–671

    Google Scholar 

  • Szentágothai J (1972) Lateral geniculate body structure and eye movement. Bibl Ophthalmol 82: 178–188

    Google Scholar 

  • Updyke BV (1975) The patterns of projection of cortical area 17, 18 and 19 onto the laminae of the dorsal lateral geniculate nucleus in the cat. J Comp Neurol 163: 377–396

    Google Scholar 

  • Updyke BV (1977) Topographic organization of the projections from cortical areas 17, 18 and 19 onto the thalamus, pretectum, and superior colliculus in the cat. J Comp Neurol 173: 81–122

    CAS  PubMed  Google Scholar 

  • Wood JG, McLaughlin BJ, Vaughn JE (1976) Immunocytochemical localization of GAD in electron microscopic preparations in rodent C.N.S. In: Roberts E, Chase TN, Tower DB (eds) GABA in Nervous System Function. Raven Press, New York, pp 133–148

    Google Scholar 

  • Wu JY, Matsuda T, Roberts E (1973) Purification and characterization of glutamate decarboxylase from mouse brain. J Biol Chem 248: 3029–3034

    Google Scholar 

  • Wu JY, Lin C-T, Brandon C, Chan T-S, Mohler H, Richards JG (1982) Regulation and immunocytochemical characterization of glutamic acid decarboxylase. In: Chan-Palay V, Palay SL (eds) Cytochemical Methods in Neuroanatomy. Alan R. Liss, Inc., New York, pp 279–296

    Google Scholar 

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Supported in part by NIH grants EY02877 to V.M. Montero and HD 03352 to the Waisman Center

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Montero, V.M., Singer, W. Ultrastructure and synaptic relations of neural elements containing glutamic acid decarboxylase (GAD) in the perigeniculate nucleus of the cat. Exp Brain Res 56, 115–125 (1984). https://doi.org/10.1007/BF00237447

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  • DOI: https://doi.org/10.1007/BF00237447

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