Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

The cholinergic innervation of the visual thalamus: an EM immunocytochemical study

Summary

In this study we demonstrate at the ultrastructural level that both the dorsal lateral geniculate nucleus (dLGN), the visual relay of the thalamus, and the perigeniculate nucleus (PGN), the visual segment of the thalamic reticular nucleus (TRN), are densely innervated by fibres with Choline-Acetyl-Transferase (ChAT) like immuno-reactivity. These axons make synaptic contacts with interneurones considered to be inhibitory, both in the PGN and within the synaptic glomeruli of the dLGN. In addition, Chat positive terminals form intra- and extraglomerular synapses with dendrites thought to arise from relay cells. We interpret these results as evidence for direct cholinergic modulation of both relay cells and inhibitory interneurones.

This is a preview of subscription content, log in to check access.

References

  1. Ahlsen G, Lindström S, Lo F-S (1984) Inhibition from the brainstem of inhibitory interneurons of the cat dorsal lateral geniculate nucleus. J Physiol 347: 593–609

  2. Ahlsen G, Lo F-S (1982) Projections of the brain stem neurons to the perigeniculate nucleus and the lateral geniculate nucleus in the cat. Brain Res 238: 433–438

  3. Armstrong DM, Saper CB, LeVey AI, Wainer BH, Terry RD (1983) Distribution of cholinergic neurons in rat brain: demonstrated by the immunocytochemical localization of choline acetyltransferase. J Comp Neurol 213: 53–68

  4. Bear MF, Carnes KM, Ebner FF (1985) An investigation of cholinergic circuitry in cat striate cortex using acetylcholines-terase histochemistry. J Comp Neurol (in press)

  5. de Lima AD, Montero VM, Singer W (1984) The cholinergic innervation in the dosal lateral geniculate and perigeniculate nucleus of the cat. An EM-immunocytochemical study. Soc Neurosci Abstr 10: 55

  6. Dingledine R, Kelly JS (1977) Brain stem stimulation and the inhibition of neurones in the feline nucleus reticularis thalami. J Physiol 271: 135–154

  7. Dodd J, Dingledine R, Kelly JS (1981) The excitatory action of acetylcholine on hippocampal neurones of the guinea pig and rat maintained in vitro. Brain Res 207: 109–127

  8. 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

  9. Eckenstein F, Baughman RW (1984) Two types of cholinergic innervation in cortex, one co-localized with vasoactive intestinal polypeptide. Nature 309: 153–155

  10. Eckenstein F, Thoenen H (1982) Production of specific antisera and monoclonal antibodies to choline acetyltransferase: characterization and use for identification of cholinergic neurons. EMBO 1: 362–368

  11. Eckenstein F, Thoenen H (1983) Cholinergic neurons in the rat cerebral cortex demonstrated by choline acetyltransferase. Neurosci Lett 36: 211–215

  12. 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

  13. Fitzpatrick D, Penny GR, Schmechel DE (1984) Glutamic acid decarboxylase-immunoreactive neurons and terminals in the lateral geniculate nucleus of the cat. J Neurosci 4: 1809–1829

  14. Francesconi W, Müller C, Singer W (1984) Acetylcholine mediates the effects of mesencephalic reticular formation stimulation in the dorsal lateral geniculate nucleus of the cat. Neurosci Lett Suppl 18: S 309

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

  16. Hayden SA, Mills JW, Masland RM (1980) Acetylcholine synthesis by displaced amacrine cells. Science 210: 435–437

  17. Houser CR, Crawford GD, Barber RP, Salvaterra PM, Vaughn JE (1983) Organization and morphological characteristics of cholinergic neurons: an immunocytochemical study with a monoclonal antibody to choline acetyltransferase. Brain Res 266: 97–119

  18. Hubel DH (1960) Single unit activity in lateral geniculate body and optic tract of unrestrained cats. J Physiol (London) 150: 91–104

  19. Hughes HC, Mullikin WH (1984) Brainstem afferents to the lateral geniculate nucleus of the cat. Exp Brain Res 54: 253–258

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

  21. Kimura H, McGeer PL, Peng JH, McGeer EG (1981) The central cholinergic system studied by choline acetyltransferase immunohistochemistry in the cat. J Comp Neurol 200: 151–201

  22. Krnjevic K (1975) Acetylcholine receptors in vertebrate CNS. In: Iversen LL, Iversen SD, Snyder SH (eds) Handbook of psychopharmacology, Vol VI. Plenum Press, New York, pp 97–380

  23. LeVey AI, Wainer BH, Rye DB, Mufson EJ, Mesulam MM (1984) Choline acetyltransferase-immunoreactive neurons intrinsic to rodent cortex and distinction from acetylcholines-terase-positive neurons. Neuroscience 2: 341–353

  24. Livingstone MS, Hubel DH (1981) Effects of sleep and arousal on the processing of visual information in the cat. Nature 291: 554–561

  25. Mesulam MM, Mufson EJ, LeVey AI, Wainer BH (1984) Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase histochemistry. Neuroscience 12: 669–686

  26. 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

  27. Montero VM, Singer W (1984a) Ultrastructure and synaptic relations of GABAergic neural elements containing glutamic acid decarboxylase (GAD) in the perigeniculate nucleus of the cat: a light and electron microscopic immunocytochemical study. Exp Brain Res 56: 115–125

  28. Montero VM, Singer W (1984b) Ultrastructure and synaptic relations of glutamic acid decarboxylase (GAD) immunoreactive neural elements in the dorsal lateral geniculate nucleus of the cat. Soc Neurosci Abstr 10: 55

  29. Montero VM, Singer W (1985) Ultrastructural identification of somata and neural processes immunoreactive to antibodies against glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the cat. Exp Brain Res (in press)

  30. Moruzzi G, Magoun HW (1949) Brain stem reticular formation and activation of the EEG. Electroencephalogr Clin Neurophysiol 1: 455–473

  31. O'Hara 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

  32. Shute CCD, Lewis PR (1967) The ascending cholinergic reticular system: neocortical olfactory and subcortical projections. Brain 90: 497–520

  33. Sillito AM, Kemp JA, Berardi N (1983) The cholinergic influence on the function of the dorsal lateral geniculate nucleus (dLGN). Brain Res 280: 299–307

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

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

  36. Sternberger LA (1979) Immunocytochemistry, 2nd edn. John Wiley, New York

  37. Stichel C, Singer W (1985) Immunohistochemical investigation of cholinergic pathways in the visual system of the cat. A light microscopic investigation. Neurosci Lett 53: 155–160

  38. Vacca LL, Abrahams SJ, Naftchi NE (1980) A modified peroxidase-antiperoxidase procedure for improved localization of tissue antigens: localization of substance P in rat spinal cord. J Histochem Cytochem 28: 297–307

Download references

Author information

Correspondence to W. Singer.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

de Lima Dolabela, A., Montero, V.M. & Singer, W. The cholinergic innervation of the visual thalamus: an EM immunocytochemical study. Exp Brain Res 59, 206–212 (1985). https://doi.org/10.1007/BF00237681

Download citation

Key words

  • Lateral geniculate nucleus
  • ChAT-immunocyto-chemistry
  • Cholinergic pathways
  • Cat