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Effects of Administration of an Agonist and an Antagonist of GABAA Receptors into the Amygdala in Rabbits on the Respiratory and Cardiac Components of Conditioned Reflex Fear

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The role of the GABAergic system of the amygdala in the autonomic and behavioral manifestations of conditioned reflex fear was studied in groups of “active” and “passive” rabbits selected on the basis of testing in an open field and a dark-light chamber. The animals were trained to a conditioned reflex by combining light (4 sec) and electrocutaneous stimulation of the hindlimbs (1 sec, 10 Hz). The extent of conditioned reflex fear was assessed in terms of changes in heart rate and respiratory movements in response to the conditioned and unconditioned stimuli as compared with rates prior to training. After training, a GABA receptor agonist (muscimol, 0.1 μg/1 μl) or antagonist bicuculline metabromide, 0.5 μg/1 μl) was applied locally into the right or left basal nucleus of the amygdala via a cannula. Administration of muscimol into the amygdala induced more extensive autonomic changes in passive rabbits than in active, eliminating the reduction in the rate of respiratory movements in response to the conditioned stimulus typical of freezing, as well as weakening or altering responses to electrocutaneous stimulation, as judged by heart and respiratory rates. Activation of the left amygdala with bicuculline increased the probability of active motor reactions in active rabbits, while activation of the right amygdala, conversely, increased the probability of freezing. These results provide evidence of the nonequivalence of the GABAergic system of the amygdala in animals with active and passive behavioral strategies.

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References

  1. T. Buresh, M. Petran’, and I. Zakhar, Electrophysiological Study Methods, IL, Moscow (1962).

    Google Scholar 

  2. D. A. Zhukov, Psychogenic Stress. Behavioral and Endocrine Correlates of the Genetic Determinants of Stress Reactivity in Uncontrollable Situations, St. Petersburg Center for Scientific and Technical Information (SPbTsNTI), St. Petersburg (1997).

    Google Scholar 

  3. I. V. Pavlova and M. R. Rysakova, “Network activity of ‘interneurons’ and large cells in the amygdala in active and passive rabbits,” Ros. Fiziol. Zh., 97, No. 12, 1297–1308 (2011).

    CAS  Google Scholar 

  4. I. V. Pavlova and M. R. Rysakova, “Characteristics of the manifestations of conditioned reflex fear inactive and passive rabbits,” Ros. Fiziol. Zh., 99, No. 11, 1308–1317 (2013).

    Google Scholar 

  5. M. R. Rysakova and I. V. Pavlova, “Interaction of neurons in the basal and central nuclei of the amygdala in rabbits and active and passive behavioral strategies in emotionally negative situations,” Zh. Vyssh. Nerv. Deyat., 61, No. 2, 190–203 (2011).

    CAS  Google Scholar 

  6. M. R. Rysakova and I. V. Pavlova, “Effects of intra-amygdalar administration of GABAA receptor agonists and antagonists on the behavior of active and passive rabbits in emotionally negative situations,” Zh. Vyssh. Nerv. Deyat., 62, No. 3, 332–345 (2012).

    CAS  Google Scholar 

  7. I. D. Fedorchenko, M. A. Merkulova, and A. M. Inyushkin, “Amygdalofugal modulation of the inspiratory inhibitory Hering-Breuer reflex,” Byull. Eksperim. Biol. Med., 133, No. 4, 371–373 (2002).

    Google Scholar 

  8. C. Applegate, R. C. Frysinger, B. S. Kapp, and M. Gallagher, “Multiple unit activity recorded from amygdale central nucleus during Pavlovian heart rate conditioning in rabbit,” Brain Res., 238, No. 2, 457–462 (1982).

    Article  CAS  PubMed  Google Scholar 

  9. D. J. Berlau and J. L. McGaugh, “Enhancement of extinction memory consolidation: the role of the noradrenergic and GABAergic systems within the basolateral amygdale,” Neurobiol. Learn. Mem., 86, No. 2, 123–132 (2006).

    Article  CAS  PubMed  Google Scholar 

  10. H. T. Blair, G. E. Schafe, E. R. Bauer, et al., “Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning,” Learn. Mem., 8, No. 5, 229–242 (2001).

    Article  CAS  PubMed  Google Scholar 

  11. H. T. Blair, P. Sotres-Bayon, M. A. Moita, and J. E. LeDoux, “The lateral amygdale processes the value of conditioned and unconditioned aversive stimuli,” Neuroscience, 133, No. 2, 561–569 (2005).

    Article  CAS  PubMed  Google Scholar 

  12. C. H. Bueno, H. J. Zangrossi, and M. B. Viana, “The inactivation of the basolateral nucleus of the rat amygdale has an anxiolytic effect in the elevated T-maze and light/dark transition tests,” Braz. J. Med. Biol. Res., 38, No. 11, 1697–1701 (2005).

    Article  CAS  PubMed  Google Scholar 

  13. L. B. Burhans and B. G. Schreurs, “Inactivation of the central nucleus of the amygdale blocks classical conditioning but not conditioning-specific reflex modification of rabbits hart rate,” Neurobiol. Learn. Mem., 100, 88–97 (2013).

    Article  PubMed  Google Scholar 

  14. K. A. Goosens and S. Maren, “Pretraining NMDA receptor blockade in the basolateral complex, but not the central nucleus, of the amygdala prevents savings of conditional fear,” Behav. Neurosci., 117, No. 4, 738–750 (2003).

    Article  CAS  PubMed  Google Scholar 

  15. J. E. LeDoux, “The amygdale,” Curr. Biol., 17, No. 20, 868–874 (2007).

    Article  Google Scholar 

  16. M. Lehner, A. Wislowska-Stanek, E. Taracha, et al., “The effects of midazolam and D-cycloserine on the release of glutamate and GABA in the basolateral amygdale of low and high anxiety rats during extinction trial of a conditioned fear test,” Neurobiol. Learn. Mem., 94, No. 4, 468–480 (2010).

    Article  CAS  PubMed  Google Scholar 

  17. C. R. Leite-Panissi and L. Menescal-de-Oliveira, “Central nucleus of the amygdala and the control of tonic immobility in guinea pigs,” Brain Res. Bull., 58, No. 1, 13–189 (2002).

    Article  CAS  PubMed  Google Scholar 

  18. H. A. Moghaddam, A. Roohbakhsh, R. Rostami, et al., “GABA and histamine interaction in the basolateral amygdala of rats in the plus-maze test of anxiety-like behaviors,” Pharmacology, 82, No. 1, 59–66 (2008).

    Article  Google Scholar 

  19. J. Muller, K. R. Corodima, Z. Fridel, and J. E. LeDoux, “Functional inactivation of the lateral and basal nuclei of the amygdale by muscimol infusion prevents fear conditioning to an explicit conditioned stimulus and to contextual stimuli,” Behav. Neurosci., 111, No. 4, 683–691 (1997).

    Article  CAS  PubMed  Google Scholar 

  20. H. C. Pape, “GABAergic neurons: gate masters of the amygdale, mastered by dopamine,” Neuron, 48, No. 6, 1025–1037 (2005).

    Article  Google Scholar 

  21. J. R. Pascoe and B. S. Kapp, “Electrophysiological characteristics of amygdaloid central nucleus during Pavlovian fear conditioning in the rabbit,” Behav. Brain Res., 16, No. 2–3, 117–133 (1985).

    Article  CAS  PubMed  Google Scholar 

  22. K. Rea, M. Roche, and D. R. Finn, “Modulation of conditioned fear, fear-conditioned analgesia, and brain regional c-Fos expression following administration of muscimol into the rat basolateral amygdale,” J. Pain, 12, No. 6, 712–721 (2011).

    Article  CAS  PubMed  Google Scholar 

  23. S. Royer and D. Pare, “Bidirectional synaptic plasticity in intercalated amygdale neurons and the extinction of conditioned fear responses,” Neuroscience, 115, No. 2, 455–462 (2002).

    Article  CAS  PubMed  Google Scholar 

  24. N. Salome, S. Ngampramuan, and E. Nalivaiko, “Intra-amygdala injection of GABAA agonist, muscimol, reduces tachycardia and modifies cardiac sympathovagal balance during restraint stress in rats,” Neuroscience, 148, No. 2, 335–341 (2007).

    Article  CAS  PubMed  Google Scholar 

  25. R. O. Tasan, A. Bukovac, Y. N. Peterschmitt, et al., “Altered GABA transmission in a mouse model of increased trait anxiety,” Neuroscience, 183, No. 1, 71–80 (2011).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. V. M. Van Nobelen and L. Kokkinidis, “Amygdaloid GABA, not glutamate neurotransmission or mRNA transcription, controls footshock-associated fear arousal in the acoustic startle paradigm,” Neuroscience, 137, No. 2, 707–716 (2006).

    Article  PubMed  Google Scholar 

  27. T. A. Berner, R. M. Pilowsky, and A. K. Godchild, “Retrograde projections to a discrete apneic site in the midline medulla oblongata in the rat,” Brain Res., 1208, 128–136 (2008).

    Article  Google Scholar 

  28. A. E. Wilensky, G. E. Schafe, M. R. Kristensen, and J. E. LeDoux, “Rethinking fear circuit: the central nucleus of the amygdale is required for the acquisition, consolidation, and expression of Pavlovian fear conditioning,” J. Neurosci., 26, No. 48, 12,387–12,396 (2006).

    Article  CAS  Google Scholar 

  29. S. Yoshida, T. Matsubara, A. Uemura, et al., “Role of medial amygdale in controlling hemodynamics via GABA(A) receptor in anesthetized rats,” Circ. J., 66, No. 2, 197–203 (2002).

    Article  CAS  PubMed  Google Scholar 

  30. Y. H. Yu and W. W. Blessing, “Neurons in amygdala mediate ear pinna vasoconstriction elicited by unconditioned salient stimuli in conscious rabbits,” Auton. Neurosci., 87, No. 2–3, 236–242 (2001).

    Article  CAS  PubMed  Google Scholar 

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Correspondence to I. V. Pavlova.

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Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 63, No. 6, pp. 730–743, November–December, 2013.

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Pavlova, I.V., Rysakova, M.P. Effects of Administration of an Agonist and an Antagonist of GABAA Receptors into the Amygdala in Rabbits on the Respiratory and Cardiac Components of Conditioned Reflex Fear. Neurosci Behav Physi 45, 188–198 (2015). https://doi.org/10.1007/s11055-015-0057-0

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  • DOI: https://doi.org/10.1007/s11055-015-0057-0

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