Skip to main content
Log in

Danger Signals Inhibit Nitrergic Activation of the Nucleus Accumbens Induced by Exploratory Behavior

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

Studies on male Sprague–Dawley rats using vital intracranial microdialysis and high-performance liquid chromatography showed that exploratory behavior in a novel context was accompanied by increases in extracellular citrulline (a co-product of NO synthesis) in the medial part of the nucleus accumbens, and these were blocked by local administration of the neuronal NO synthase inhibitor 7-nitroindazole (0.5 mM). Presentation during exploratory activity of a tone which had previously been combined with electrocutaneous stimulation decreased exploratory behavior and, secondly, inhibited the increase in the nucleus accumbens citrulline level induced by exploratory behavior. These effects were not seen in control animals in which the tone had not been associated with electrocutaneous stimulation. These data provide the first evidence for the involvement of the medial part of the nucleus accumbens in transferring the effects of fear to exploratory behavior and demonstrate that inhibition of nitrergic transmission may make a contribution to this process.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. S. A. Saveliev, N. S. Repkina, and N. B. Saulskaya, “A sensitive method for assaying citrulline for the vital monitoring of nitric oxide production in the CNS,” Ros. Fiziol. Zh., 91, No. 5, 587–591 (2005).

    CAS  Google Scholar 

  2. N. B. Saulskaya, N. A. Solovieva, and S. A. Saveliev, “Release of glutamate into the nucleus accumbens on competitive presentation of defensive and food stimuli,” Zh. Vyssh. Nerv. Deyat., 55, No. 1, 71–77 (2005).

    CAS  Google Scholar 

  3. N. B. Saulskaya, N. V. Fofonova, P. V. Sudorgina, and A. S. Komarova, “Sound danger signals activate the NOergic system of the medial part of the nucleus accumbens,” Zh. Vyssh. Nerv. Deyat., 60, No. 1, 65–73 (2010).

    Google Scholar 

  4. B. A. Baldo and A. E. Kelley, “Discrete neurochemical coding of distinguishable motivational processes: insights from nucleus accumbens control of feeding,” Psychopharmacology, 191, No. 3, 439–459 (2007).

    Article  PubMed  CAS  Google Scholar 

  5. S. A. Cavigelli and M. K. McClintock, “Fear of novelty in infant rats predicts adult corticosterone dynamics and an early death,” Proc. Natl. Acad. Sci. USA, 100, No. 26, 16131–16136 (2003).

    Article  PubMed  CAS  Google Scholar 

  6. I. Ehrlich,Y. Humeau, F. Grenier, et al., “Amygdala inhibitory circuits and the control of fear memory,” Neuron, 62, No. 6, 757–771 (2009).

    Article  PubMed  CAS  Google Scholar 

  7. 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 

  8. 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,” Neurosci., 135, No. 1, 121–131 (2005).

    Article  CAS  Google Scholar 

  9. J. Garthwaite, “Concepts of neural nitric oxide-mediated transmission,” Eur. J. Neurosci., 27, No. 11, 2783–2802 (2008).

    Article  PubMed  Google Scholar 

  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. 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 

  12. J. E. LeDouxe, “Emotional circuits in the brain,” Annu. Rev. Neurosci., 23, 155–184 (2000).

    Article  Google Scholar 

  13. M. Legault and R. A. Wise, “Novelty-evoked elevations of nucleus accumbens dopamine: dependence on impulse flow from the ventral subiculum and glutamatergic neurotransmission in the ventral tegmental area,” Eur. J. Neurosci., 13, No. 4, 819–828 (2001).

    Article  PubMed  CAS  Google Scholar 

  14. J. E. Lisman and A. A. Grace, “The hippocampal-VTA loop: controlling the entry of information into long-term memory,” Neuron, 46, No. 5, 703–713 (2005).

    Article  PubMed  CAS  Google Scholar 

  15. S. Maren and G. J. Quirk, “Neuronal signaling of fear memory,” Nat. Neurosci. Rev., 5, No. 11, 844–852 (2004).

    Article  CAS  Google Scholar 

  16. G. E. Meredith, B. A. Baldo, M. E. Andrezjewski, and A. E. Kelley, “The structural basis for mapping behavior onto the striatum and its subdivisions,” Brain Struct. Funct., 213, No. 1–2, 17–27 (2008).

    Article  PubMed  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).

    Google Scholar 

  18. S. M. Nicola, “The nucleus accumbens as a part of a basal ganglia action selection circuit,” Psychopharmacology, 191, No. 3, 521–550 (2007).

    Article  PubMed  CAS  Google Scholar 

  19. P. Redgrave, T. J. Prescott, and K. Gurney, “The basal ganglia: a vertebrate solution to the selection problem,” Neurosci., 89, No. 4, 1009–1023 (1999).

    Article  CAS  Google Scholar 

  20. S. Reynolds and K. C. Berridge, “Glutamate motivational ensembles in the nucleus accumbens: rostrocaudal shell gradients of fear and feeding,” Eur. J. Neurosci., 17, No. 10, 2187–2200 (2003).

    Article  PubMed  Google Scholar 

  21. S. Reynolds and K. C. Berridge, “Emotional environments retune the valence of appetitive versus fearful functions in nucleus accumbens,” Nat. Neurosci., 11, No. 4, 324–425 (2008).

    Article  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. N. Saulskaya and C. A. Marsden, “Conditioned dopamine release: dependence upon N-methyl-D-aspartate receptors,” Neurosci., 67, No. 1, 57–63 (1995).

    Article  CAS  Google Scholar 

  25. N. Saulskaya and C. A. Marsden, “Extracellular glutamate in the nucleus accumbens during a conditioned emotional response in rats,” Brain Res., 698, No. 1, 114–120 (1995).

    Article  PubMed  CAS  Google Scholar 

  26. N. Saulskaya and N. A. Soloviova, “Tetrodotoxin-dependent glutamate release in the rat nucleus accumbens during concurrent presentation of appetitive and conditioned aversive stimuli,” J. Neurosci. Meth., 140, No. 1–2, 15–21 (2004).

    Article  CAS  Google Scholar 

  27. D. H. Zald, R. L. Cowan, P. Riccardi, et al., “Midbrain dopamine receptor availability is inversely associated with novelty-seeking traits in humans,” J. Neurosci., 28, No. 53, 14372–14378 (2008).

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. B. Saulskaya.

Additional information

Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 62, No. 4, pp. 475–484, July–August, 2012.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Saulskaya, N.B., Belozerov, Y.V. Danger Signals Inhibit Nitrergic Activation of the Nucleus Accumbens Induced by Exploratory Behavior. Neurosci Behav Physi 43, 1076–1083 (2013). https://doi.org/10.1007/s11055-013-9852-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11055-013-9852-7

Keywords

Navigation