Vital intracerebral microdialysis experiments in Sprague–Dawley rats with high-performance liquid chromatography (HPLC) showed that presentation during exploratory behavior of a tone previously combined with pain stimulation decreased exploratory activity and inhibited the exploratory behavior-induced increase in the extracellular citrulline (a co-product of NO synthesis) level in the medial sector of the nucleus accumbens. Administration of the GABAA receptor antagonist bicuculline (20 μM) into the medial sector of the nucleus accumbens firstly produced partial recovery of the increase in the extracellular citrulline level in this structure induced by exploratory behavior and suppressed by a tone previously combined with pain stimulation and, secondly, prevented inhibition of exploratory behavior by this danger sound signal. The data obtained here provide the first evidence that inhibition of exploratory behavior by danger signals and the exploration-associated activation of the nitrergic system of the medial sector of the nucleus accumbens are mediated by GABAA receptor mechanisms.
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S. A. Savel’ev, N. S. Repkina, and N. B. Saul’skaya, “A sensitive method for assay of citrulline for vital monitoring of nitric oxide production in the CNS,” Ros. Fiziol. Zh., 91, No. 5, 587–591 (2005).
N. B. Saul’skaya and Ya. V. Belozerov, “Extracellular citrulline levels in the nucleus accumbens during feeding behavior,” Ros. Fiziol. Zh., 97, No. 6, 566–572 (2011).
N. B. Saul’skaya and Ya. V. Belozerov, “Danger signals inhibit nitrergic activation of the nucleus accumbens induced by exploratory behavior,” Zh. Vyssh. Nerv. Deyat., 62, No. 4, 475–484 (2012).
N. B. Saul’skaya, N. A. Solov’eva, and S. A. Savel’ev, “Glutamate release in the nucleus accumbens (n. accumbens) in competitive presentation of defensive and feeding stimuli,” Zh. Vyssh. Nerv. Deyat., 55, No. 1, 71–77 (2005).
N. B. Saul’skaya and P. V. Sudorgina, “A mediolateral gradient of nitrergic activation of the nucleus accumbens during exploratory behavior,” Ros. Fiziol. Zh., 98, No. 4, 461–468 (2012).
N. B. Saul’skaya, N. V. Fofonova, and P. V. Sudorgina, “Activation of the NO-ergic system of the nucleus accumbens on presentation of contextual danger signals,” Ros. Fiziol. Zh., 95, No. 8, 793–800 (2009).
N. B. Saul’skaya, N. V. Fofonova, P. V. Sudorgina, and A. S. Komarova, “Danger sound signals activated the NO-ergic system of the medial sector of the nucleus accumbens,” Zh. Vyssh. Nerv. Deyat., 60, No. 1, 65–73 (2010).
I. Afanas’ev, B. Ferger, and K. Kuschinsky, “The associative type of sensitization to d-amphetamine is expressed as an NO-dependent dramatic increase in extracellular dopamine in the nucleus accumbens,” Naunyn Schmiedeberg Arch. Pharmacol., 362, No. 3, 232–237 (2000).
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).
S. D. Floresco, Y. Zhang, and T. Enomato, “Neural circuits subserving behavioral flexibility and their relevance to schizophrenia,” Behav. Brain Res., 204, No. 2, 396–409 (2009).
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.
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).
S. K. Hong, I. S. Jung, S. A. Bang, and S. E. Kim, “Effect of nitric oxide synthase inhibitor and NMDA receptor antagonist on the development of nicotine sensitization of the nucleus accumbens dopamine release: an in vivo microdialysis study,” Neurosci. Lett., 409, No. 3, 220–223 (2006).
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).
S. Ikemoto, “Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex,” Brain Res. Rev., 56, No. 1, 27–78 (2007).
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).
A. E. Kelley, “Neural integrative activities of the nucleus accumbens subregions in relation to learning and motivation,” Psychobiology, 27, No. 2, 198–213 (1999).
A. V. Kravitz, L. D. Tye, and A. C. Kreitzer, “Distinct roles for direct and indirect pathway striatal neurons in reinforcement,” Nat. Neurosci., 15, No. 6, 816–818 (2012).
J. E. LeDoux, “Emotional circuits in the brain,” Annu. Rev. Neurosci., 23, 155–184 (2000).
G. F. Meredith and S. Totterdell, “Microcircuits in the nucleus accumbens’ shell and core involved in cognition and reward,” Psychobiology, 27, No. 2, 165–186 (1999).
S. M. Nicola, “The nucleus accumbens as a part of a basal ganglia action selection circuit,” Psychopharmacology, 191, No. 3, 521–550 (2007).
C. A. Orsini and M. Maren, “Neural and cellular mechanisms of fear and extinction memory formation,” Neurosci. Biobehav. Rev., 36, No. 7, 1773–1803 (2012).
P. Redgrave, T. J. Prescott, and K. Gurney, “The basal ganglia: a vertebrate solution to the selection problem,” Neuroscience, 89, No. 4, 1009–1023 (1999).
S. Reynolds and K. C. Berridge, “Fear and feeding in the nucleus accumbens shell: rostrocaudal segregation of GABA-elicited defensive behavior versus eating behavior,” J. Neurosci., 21, No. 9, 3261–3270 (2001).
S. Reynolds and K. C. Berridge, “Positive and negative motivation in nucleus accumbens shell: bivalent rostrocaudal gradients for GABA-elicited eating, taste “liking”/“disliking” reactions, place preference/avoidance, and fear,” J. Neurosci., 22, No. 16, 7308–7320 (2002).
S. Reynolds and K. C. Berridge, “Emotional environments retune the valence of appetitive versus fearful functions in nucleus accumbens,” Nat. Neurosci., 11, No. 4, 423–425 (2008).
H. Sahrei, F. Zarei, A. Eidi, et al., “The role of nitric oxide within the nucleus accumbens on the acquisition and expression of morphine-induced place preference in morphine sensitized rats,” Eur. J. Pharmacol., 556, No. 1–3, 99–106 (2007).
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).
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).
N. B. 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).
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Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 63, No. 6, pp. 744–752, November–December, 2013.
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Saul’skaya, N.B., Terekhova, E.A. GABA-Nitrergic Interactions in the Nucleus Accumbens during Inhibition of Exploratory Behavior by Danger Signals. Neurosci Behav Physi 45, 199–205 (2015). https://doi.org/10.1007/s11055-015-0058-z
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DOI: https://doi.org/10.1007/s11055-015-0058-z