Skip to main content
SpringerLink
Log in

Effects of Activation and Blockade of GABAA Receptors on the Activity of the Nitrergic System of the Nucleus Accumbens

  • Published:
Neuroscience and Behavioral Physiology Aims and scope Submit manuscript

Studies in Sprague–Dawley rats using vital intracerebral microdialysis showed that administration of GABAA receptor antagonist bicuculline (20, 60, and 120 μM) into the nucleus accumbens induced dose-dependent increases in extracellular citrulline (a coproduct of NO synthesis) levels in this structure, and this was almost completely prevented by administration of 7-nitroindazole (0.5 mM), an inhibitor of neuronal NO synthase, into the nucleus accumbens. Administration of the GABAA receptor agonist muscimol into the nucleus accumbens at doses of 10 and 50 μM had no effect on the citrulline level in this structure, while a dose of 150 μM produced a decrease. Administration of NMDA receptor agonist NMDA (100 μM) into this nucleus led to an increase in the citrulline level in the nucleus accumbens, while administration of muscimol (10, 50, and 150 μM) produced dose-dependent decreases. These data provide the first evidence that GABAA receptors control baseline and NMDA receptor stimulation-evoked evoked levels of activity in the nitrergic system of the nucleus accumbens.

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. S. A. Savel’eva, N. S. Repkina, and N. B. Saul’skaya, “A sensitive method for assaying citrulline for vital monitoring of nitric oxide production in the central nervous system,” Ros. Fiziol. Zh., 91, No. 5, 587–591 (2005).

    Google Scholar 

  2. N. B. Saul’skaya and P. V. Sudorgina, “Effects of blockade of D2 dopamine receptors on the activity of the nitrergic system of the nucleus accumbens in the rat brain,” 98, No. 3, 14–20 (2012).

  3. N. B. Saul’skaya and E. A. Terekhova, “Synergistic activation of the nitrergic system of the nucleus accumbens by dopamine D1 and D2 receptor agonists,” Ros. Fiziol. Zh., 98, No. 7, 819–826 (2012).

    Google Scholar 

  4. M. D. Bevan, P. A. Booth, S. A. Eaton, and J. P. Bolam, “Selective innervation of neostriatal interneurons by a subclass of neurons in the globus pallidus of the rat,” J. Neurosci., 18, No. 22, 9438–9452 (1998).

    PubMed  CAS  Google Scholar 

  5. P. DeBoer and B. H. Westerink, “GABAergic modulation of striatal cholinergic interneurons: an in vivo microdialysis study,” J. Neurochem., 62, No. 1, 70–75 (1994).

    Article  PubMed  CAS  Google Scholar 

  6. S. J. French and H. Hartung, “Nitrergic tone influences activity of both ventral striatum projection neurons and interneurons,” in: The Basal Ganglia IX, H. J. Groenewegen et al. (eds.), Springer-Verlag, Berlin (2009), pp. 337–350.

    Chapter  Google Scholar 

  7. S. J. French, G. P. Ritson, S. Hidaka, and S. Totterdell, “Nucleus accumbens nitric oxide immunoreactive interneurons receive nitric oxide and ventral subicular afferents in rats,” Neuroscience, 135, No. 1, 121–131 (2005).

  8. J. Garthwaite, Glutamate, nitric oxide and cell-cell signaling in the nervous system,” Trends Neurosci., 14, No. 1, 60–67 (1991).

    Article  PubMed  CAS  Google Scholar 

  9. H. Hartung, S. Threlfell, and S. J. Cragg, “Nitric oxide donors enhance the frequency dependence of dopamine release in nucleus accumbens,” Neuropsychopharmacology, 36, No. 9, 1811–1822 (2011).

  10. 10, S. Hidaka and S. Totterdell, “Ultrastructural features of the nitric oxide synthase-containing interneurons in the nucleus accumbens and their relationship with tyrosine hydroxylase containing terminals,” J. Comp. Neurol., 431, No. 2, 139–154 (2001).

    Article  PubMed  CAS  Google Scholar 

  11. R. A. Hopper and J. Garthwaite, “Tonic and phasic nitric oxide signals in hippocampal long-term potentiation,” J. Neurosci., 26, No. 45, 11,513–11,521 (2006).

    Article  CAS  Google Scholar 

  12. M. D. Humphries and T. J. Prescott, “The ventral basal ganglia, a selection mechanism at the crossroads of space, strategy and reward,” Progr. Neurobiol., 90, No. 4, 385–417 (2010).

    Article  Google Scholar 

  13. Y. Kawaguchi, C. J. Wilson, S. J. Augood, and P. C. Emson, “Striatal interneurons: chemical, physiological and morphological characterization,” Trends Neurosci., 18, No. 12, 527–535 (1995).

    Article  PubMed  CAS  Google Scholar 

  14. M. M. Graus and H. Prast, “Involvement of nitric oxide, cyclic GMP and phosphodiesterase 5 in excitatory amino acid and GABA release in the nucleus accumbens evoked by activation of the hippocampal fimbria,” J. Neurosci., 112, No. 2, 331–342 (2002).

    Article  Google Scholar 

  15. A. P. Lopes, L. Ganzer, A. C. Borges, et al., “Effects of GABA ligands injected into the nucleus accumbens shell on fear/anxiety-like and feeding behaviours in food-deprived rats,” Pharmacol. Biochem. Behav., 101, No. 1, 41–48 (2012).

    Article  PubMed  CAS  Google Scholar 

  16. E. P. Maguire, T. Macpherson, J. D. Swinny, et al., “Tonic inhibition of accumbal spiny neurons by extrasynaptic α4βσ GABAa receptors modulates the action of psychostimulant,” J. Neurosci., 34, No. 3, 823–838 (2014).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  17. G. E. Meredith and S. Totterdell, “Microcircuits in the nucleus accumbens’ shell and core involvement in cognition and reward,” Psychobiology, 27, No. 2, 165–186 (1999).

  18. S. Newman, L. Pascal, K. Sedeghian, and B. A. Baldo, “Sweetened-fat intake sensitizes gamma-aminobutyric acid-mediated feeding responses elicited from the nucleus accumbens shell,” Biol. Psychiatry, 73, No. 9, 843–850 (2013).

    Article  PubMed  CAS  Google Scholar 

  19. H. Nie, M. Rewal, M. Gill, DS. Ron, and P. H. Janac, “Extrasynaptic σ-containing GABAa receptors in the nucleus accumbens dorsomedial shell contribute to alcohol intake,” Proc. Natl. Acad. Sci. USA, 108, No. 11, 4459–4464 (2011).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  20. P. V. Rada, G. P. Mark, and B. G. Hoebel, “In vivo modulation of acetylcholine in the nucleus accumbens of freely moving rats: II. Inhibition by gamma-aminobutyric acid,” Brain Res., 619, No. 1–2, 105–110 (1993).

    Article  PubMed  CAS  Google Scholar 

  21. S. Reynolds and K. C. Berridge, “Positive and negative motivation in nucleus accumbens shell: bivalent rostrocaudal gradients for GABAelicited eating, taste ‘liking’/’disliking’ reactions, place preference/ avoidance and fear,” J. Neurosci., 22, No. 16, 7308–7320 (2002).

    PubMed  CAS  Google Scholar 

  22. N. B. Saulskaya and N. V. Fofonova, “Effects of N-Methyl-D-aspartate on extracellular citrulline level in the rat nucleus accumbens,” Neurosci. Lett., 407, No. 1, 91–95 (2006).

    Article  PubMed  CAS  Google Scholar 

  23. N. B. Saulskaya, N. V. Fofonova, P. V. Sudorghina, and S. A. Saveliev, “Dopamine D1 receptor-dependent regulation of extracellular citrulline level in the rat nucleus accumbens during conditioned fear response,” Neurosci. Lett., 440, No. 2, 185–189 (2008).

    Article  PubMed  CAS  Google Scholar 

  24. J. M. Tepper, F. Tecuapetla, T. Koos, and O. Ibanez-Sandoval, “Heterogeneity and diversity of striatal GABAergic interneurons,” Front. Neuroanat., 4, Article No. 150, 1–18 (2010).

  25. A. R. West, M. P. Galloway, and A. Grace, “Regulation of striatal dopamine neurotransmission by nitric oxide: effector pathways and signaling mechanisms,” Synapse, 44, No. 2, 227–245 (2002).

  26. M. Yoshida, H. Yokoo, K. Nakahara, et al., “Local muscimol disinhibits mesolimbic dopaminergic activity by brain microdialysis and Fos immunohistochemistry,” Brain Res., 767, No. 2, 356–360 (1997).

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Pavlov Institute of Physiology, Russian Academy of Sciences, St. Petersburg, Russia

    N. B. Saul’skaya & E. V. Vinogradova

Authors
  1. N. B. Saul’skaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. V. Vinogradova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. B. Saul’skaya.

Additional information

Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 100, No. 7, pp. 791–801, July, 2014.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saul’skaya, N.B., Vinogradova, E.V. Effects of Activation and Blockade of GABAA Receptors on the Activity of the Nitrergic System of the Nucleus Accumbens. Neurosci Behav Physi 46, 146–152 (2016). https://doi.org/10.1007/s11055-015-0211-8

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11055-015-0211-8

Keywords

Search

Navigation