Skip to main content
SpringerLink
Log in

Connections Between NO Synthase-Containing Neurons of the Pedunculopontine Tegmental Nucleus and the Substantia Nigra in Rats

  • Published:
Neurophysiology Aims and scope

Abstract

Experiments on rats with detection of the NADP-d-activity in neurons of the pedunculopontine tegmental nucleus (PPTg) and their processes demonstrated that between the substantia nigra (SN) and PPTg there are connections established by the neurons containing nitric oxide synthase (NOS). Two types of connections were observed. Axon-like collaterals of the neuronal pathways sent by PPTg neurons toward the forelimb penetrate the SN from its dorsal side. In addition, dendrites of the NOS-containing neurons localized within the rostral PPTg part penetrate the caudoventral region of the reticular SN (SNr). It is supposed that NO produced by these processes within the SN can exert modulating influences on synaptic transmission in this structure; when produced in excessive amounts under some pathological conditions, NO can be a factor evoking neurodegeneration in the midbrain.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  1. P. Mahachoklertwattana, S. M. Black, S. L. Kaplan, et al., “Ni-tric oxide synthesized by gonadotropin-releasing hormone neu-rons is a mediator of N-methyl-D-aspartate (NMDA)-induced GnRH secretion,” Endocrinology, 135, No. 4, 1709-1712 (1994).

    Google Scholar 

  2. M. Moretto, F. J. Lopez, and A. Negro-Vilar, “Nitric oxide regulates luteinizing hormone-releasing hormone secretion,” Endocrinology, 133, No. 5, 2399-2402 (1993).

    Google Scholar 

  3. J. J. Bonavera, P. S. Kalra, and S. P. Kalra, “Evidence in support of nitric oxide (NO) involvement in the cyclic release of prolactin and LH surges,” Brain Res., 660, No. 1, 175-179 (1994).

    Google Scholar 

  4. S. Hindley, B. H. Juurlink, J. W. Gysbers, et al., “Nitric oxide donors enhance neurotrophin-induced neurite outgrowth through a cGMP-dependent mechanism,” J. Neurosci. Res., 47, No. 4, 427-439 (1997).

    Google Scholar 

  5. F. Zang, S. Xu, and C. Iadecola, “Role of nitric oxide and ace-tylcholine in neocortical hyperemia elicited by basal forebrain stimulation: evidence for involvement of endothelial nitric oxide,” Neuroscience, 69, No. 4, 1195-2040 (1995).

    Google Scholar 

  6. J. L. Dinerman, T. M. Dawson, M. J. Schell, et al., “Endothe-lial nitric oxide synthase localized to hippocampal pyramidal cells: implications for synaptic plasticity,” Proc. Natl. Acad. Sci. USA, 91, No. 10, 4214-4218 (1994).

    Google Scholar 

  7. T. J. O'Dell, P. L. Huang, T. M. Dawson, et al., “Endothelial NOS and the blockade of LTP by NOS inhibitors in mice lack-ing neuronal NOS,” Science, 265, No. 5171, 542-546 (1994).

    Google Scholar 

  8. F. M. Faraci and J. E. Brian, Jr., “Nitric oxide and the cerebral circulation,” Stroke, 25, No. 3, 692-703 (1994).

    Google Scholar 

  9. P. Calabresi, D. Centonze, P. Gubellini, et al., “Glutamate-triggered events inducing corticostriatal long-term depression,” J. Neurosci., 19, No. 14, 6102-6110 (1999).

    Google Scholar 

  10. M. Reyes-Harde, B. V. Potter, A. Galione, et al., “Induction of hippocampal LTD requires nitric oxide-stimulated PKG activity and Ca 2+ release from cyclic ADP-ribose-sensitive stores,” J. Neurophysiol., 82, No. 3, 1569-1576 (1999).

    Google Scholar 

  11. D. B. Kantor, M. Lanzrein, S. J. Stary, et al., “A role for endothelial NO synthase in LTP revealed by adenovirus-mediated inhibition and rescue,” Science, 274, No. 5293, 1744-1748 (1996).

    Google Scholar 

  12. H. Daniel, C. Levenes, and F. Crepel, “Cellular mechanisms of cerebellar LTD,” Trends Neurosci., 21, No. 9, 401-407 (1998).

    Google Scholar 

  13. J. A. Gally, P. R. Montague, G. N. Reeke, Jr., et al., “The NO hypothesis: possible effects of a short-lived, rapidly diffusible signal in the development and function of the nervous sys-tem,” Proc. Natl. Acad. Sci. USA, 87, No. 9, 3547-3551 (1990).

    Google Scholar 

  14. M. Zhuo, S. A. Small, E. R. Kandel, et al., “Nitric oxide and carbon monoxide produce activity-dependent long-term synaptic enhancement in hippocampus,” Science, 260, No. 5116, 1946-1950 (1993).

    Google Scholar 

  15. E. M. Schuman and D. V. Madison, “Locally distributed synaptic potentiation in the hippocampus,” Science, 263, No. 5146, 532-536 (1994).

    Google Scholar 

  16. J. Bruhwyler, E. Chleide, J. F. Liegeois, et al., “Nitric oxide: a new messenger in the brain,” Neurosci. Biobehav. Rev., 17, No. 4, 373-384 (1993).

    Google Scholar 

  17. M. K. Meffert, B. A. Premack, and H. Schulman, “Nitric oxide stimulates Ca 2+-independent synaptic vesicle release,” Neu-ron, 12, No. 6, 1235-1244 (1994).

    Google Scholar 

  18. J. P. Kiss, E. C. Hennings, G. Zsilla, et al., “A possible role of nitric oxide in the regulation of dopamine transporter function in the striatum,” Neurochem. Int., 34, No. 4, 345-350 (1999).

    Google Scholar 

  19. T. Hanania and K. M. Johnson, “Regulation of neurotransmitter release by endogenous nitric oxide in striatal slices,” Eur. J. Pharmacol., 359, Nos. 2/3, 111-117 (1998).

    Google Scholar 

  20. Y. K. Sohn, N. Ganju, K. D. Bloch, et al., “Neuritic sprouting with aberrant expression of the nitric oxide synthase III gene in neurodegenerative diseases,” J. Neurol. Sci., 162, No. 2, 133-151 (1999).

    Google Scholar 

  21. T. Gonzalez-Hernandez, P. Abdala, and M. Rodriguez, “NOS expression in nigral cells after excitotoxic and non-excitotoxic lesion of the pedunculopontine tegmental nucleus,” Eur. J. Neurosci., 9, No. 12, 2658-2667 (1997).

    Google Scholar 

  22. S. R. Vincent and H. Kimura, “Histochemical mapping of nitric oxide synthase in the rat brain,” Neuroscience, 46, No. 4, 755-784 (1992).

    Google Scholar 

  23. G. Paxinos and C. Watson, The Rat Brain in Stereotaxic Coor-dinates, Academic Press, New York (1997).

    Google Scholar 

  24. K. Takakusaki, T. Shiroyama, and S. T. Kitai, “Two types of cholinergic neurons in the rat tegmental pedunculopontine nucleus: electrophysiological and morphological character-ization,” Neuroscience, 79, No. 4, 1089-1090 (1997).

    Google Scholar 

  25. M. A. Marletta, “Nitric oxide synthase structure and mecha-nism,” J. Biol. Chem., 268, No. 17, 12231-12234 (1993).

    Google Scholar 

  26. M. S. Lee, J. O. Rinne, and C. D. Marsden, “The peduncu-lopontine nucleus: its role in the genesis of movement disor-ders,” Yonsei Med. J., 41, No. 2. 167-184 (2000).

    Google Scholar 

  27. I. Grofova and M. Zhou, “Nigral innervation of cholinergic and glutamatergic cells in the rat mesopontine tegmentum: light and electron microscopic anterograde tracing and immunohistochemical studies,” J. Comp. Neurol., 395, No. 3, 359-379 (1998).

    Google Scholar 

  28. P. Buma, “Synaptic and nonsynaptic release of neuromediators in the central nervous system,” Acta Morphol. Neerl. Scand., 26, Nos. 2/3, 81-113 (1988-89).

    Google Scholar 

  29. M. B. Djamgoz, J. R. Cunningham, S. L. Davenport, et al., “Nitric oxide inhibits depolarization-induced release of endogenous dopamine in the rabbit retina,” Neurosci. Lett., 198, No. 1, 33-36 (1995).

    Google Scholar 

  30. S. Ohkuma, M. Katsura, D. Z. Chen, et al., “Nitric oxide-evoked [ 3 H] gamma aminobutyric acid release is mediated by two distinct release mechanisms,” Brain Res. Mol. Brain Res., 36, No. 1, 137-144 (1996).

    Google Scholar 

  31. M. Miyazaki and M. G. Lacey, “Presynaptic inhibition by dopamine of a discrete component of GABA release in rat substantia nigra pars reticulata,” J. Physiol., 513, Part 3, 805-817 (1998).

    Google Scholar 

  32. N. Kayadjanian, H. Gioanni, A. Menetrey, et al., “Muscarinic receptor stimulation increases the spontaneous [ 3 H] GABA release in the rat substantia nigra through muscarinic recep-tors localized on striatonigral terminals,” Neuroscience, 63, No. 4, 989-1002 (1994).

    Google Scholar 

  33. T. Futami, K. Takakusaki, and S. T. Kitai, “Glutamatergic and cholinergic inputs from the pedunculopontine tegmental nucleus to dopamine neurons in the substantia nigra pars com-pacta,” Neurosci. Res., 21, No. 4, 331-342 (1995).

    Google Scholar 

  34. N. J. Dun, S. L. Dun, L. L. Hwang, and U. Forstermann, “In-frequent co-existence of nitric oxide synthase andin and calretinin immunoreactivity in rat pontine neurons,” Neurosci. Lett., 191, No. 3, 165-168 (1995).

    Google Scholar 

  35. K. Aguan, J. Murotsuki, R. Gagnon, et al., “Effect of chronic hypoxemia on the regulation of nitric-oxide synthase in the fetal sheep brain,” Brain Res. Dev. Brain Res., 111, No. 2, 271-277 (1998).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. National Academy of Sciences of Ukraine, Bogomolets Institute of Physiology, Kyiv, Ukraine

    D. E. Duzhyi

Authors
  1. D. E. Duzhyi
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Duzhyi, D.E. Connections Between NO Synthase-Containing Neurons of the Pedunculopontine Tegmental Nucleus and the Substantia Nigra in Rats. Neurophysiology 33, 158–164 (2001). https://doi.org/10.1023/A:1012869619102

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1012869619102

Search

Navigation