Abstract
The effects of an agonist (D-cycloserine) and an antagonist (dizocilpine) of N-methyl-D-aspartate (NMDA) receptors on the learning and extinction of a conditioned passive avoidance response were studied in mice with low, intermediate, and high levels of anxiety. In intermediate-anxiety mice, D-cycloserine (30 mg/kg) had no effect on learning but accelerated extinction, while dizocilpine (0.15 mg/kg) degraded acquisition of the reflex but delayed extinction. In high-anxiety mice, with good learning and no extinction, D-cycloserine had no effect, while dizocilpine decreased learning and facilitated retention of performance of the memory trace at the ongoing level in conditions promoting extinction. In low-anxiety mice, D-cycloserine degraded learning and accelerated extinction, while dizocilpine completely blocked learning and the retention of the passive avoidance response.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
A. S. Bazyan, I. S. Midzyanovskaya, G. D. Kuznetsova, K. Yu. Sarkisova, V. M. Getsova, N. V. Orlova, and A. A. Lushkin, “Possible mechanisms for the formation of the typological characteristics of behavior in WAG/Rij rats,” Zh. Vyssh. Nerv. Deyat., 51, No. 6, 709–716 (2001).
A. Yu. Bespalov and É. É. Zvartau, “Antagonists of ionotropic glutamate receptors as a study system in psychopharmacology,” Usp. Fiziol. Nauk., 30, No. 1, 39–53 (1999).
N. I. Dubrovina and L. V. Loskutova, Dopaminergic Mechanisms of Memory and Attention [in Russian], Siberian Division, Russian Academy of Medical Sciences, Novosibirsk (2003).
D. A. Zhukov and E. P. Vinogradova, “Different levels of anxiety in rats selected for the ability to acquire a conditioned passive avoidance reflex,” Zh. Vyssh. Nerv. Deyat., 44, No. 3, 591–596 (1994).
W. Adriani, A. Felici, F. Sargolini, F. Roullet, A. Usiello, A. Oliverio, and A. Mele, “N-methyl-D-aspartate and dopamine receptor involvement in the modulation of locomotor activity and memory processes,” Exptl. Brain Res., 123, No. 1–2, 52–59 (1998).
V. P. Bakshi, M. Tricklebank, H. C. Neijt, V. Lehmann-Masten, and M. H. Geyer, “Disruption of prepulse inhibition and increases in locomotor activity by competitive N-methyl-D-aspartate receptor antagonists in rats,” J. Pharmacol. Exptl. Ther., 288, No. 2, 643–652 (1999).
M. E. Bardgett, R. Boeckman, D. Krochmal, H. Fernando, R. Ahrens, and J. G. Csernansky, “NMDA receptor blockade and hippocampal neuronal loss impair fear conditioning and position habit reversal in C57B1/6 mice,” Brain Res. Bull., 60, No. 1–2, 131–142 (2003).
M. E. Bouton and E. W. Moody, “Memory processes in classical conditioning,” Neurosci. Biobehav. Rev., 28, No. 7, 663–674 (2004).
O. P. Dall’Igna, A. L. Da Silva, M. O. Dietrich, A. Hoffmann, R. V. de Oliveira, and D. R. Souza, “Chronic treatment with caffeine blunts the hyperlocomotor but not cognitive effects of the N-methyl-D-aspartate receptor antagonist MK-801 in mice,” Psychopharmacology, 166, No. 3, 258–263 (2003).
A. R. Delamater, “Experimental extinction in Pavlovian conditioning: behavioural and neuroscience perspectives,” Quart. J. Exptl. Psychol., B57, No. 2, 97–132 (2004).
E. De Leonibus, V. J. Costantini, C. Castellano, V. Ferretti, A. Oliverio, and A. Mele, “Distinct roles of the different ionotropic glutamate receptors within the nucleus accumbens in passive-avoidance learning and memory in mice,” Eur. J. Neurosci., 18, No. 8, 2365–2373 (2003).
E. Dere, B. Topic, M. A. De Souza Silva, H. Fink, T. Buddenberg, and J. P. Huston, “NMDA receptor antagonism via dextromethorphan and ifenprodil modulates graded anxiety test performance of C57BL/6 mice,” Behav. Pharmacol., 14, No. 3, 245–249 (2003).
N. B. Farber, “The NMDA receptor hypofunction model of psychosis,” Ann. N.Y. Acad. Sci., 1003, 119–130 (2003).
M. Fedosiewicz-Wasiluk, Z. Z. Holy, R. J. Wisniewska, and K. Wisniewski, “The influence of NMDA, a potent agonist of glutamate receptor, on behavioral activity of rats with experimental hyperammonemia evoked by liver failure,” Amino Acids, 28, No. 1, 111–117 (2005).
C. M. Fraser, M. J. Cooke, A. Fisher, I. D. Thompson, and T. W. Stone, “Interactions between ifenprodil and dizocilpine on mouse behaviour in models of anxiety and working memory,” Eur. J. Neuropsychopharmacol., 6, No. 4, 311–316 (1996).
K. A. Goosens and S. Maren, “NMDA receptors are essential for the acquisition, but not expression, of conditional fear and associative spike firing in the lateral amygdala,” Eur. J. Neurosci., 20, No. 2, 537–548 (2004).
Y. J. Ho, L. S. Hsu, C. F. Wang, W. Y. Hsu, T. J. Lai, C. C. Hsu, and Y. F. Tsai, “Behavioral effects of d-cycloserine in rats: The role of anxiety level,” Brain Res., 1043, No. 1–2, 179–185 (2005).
C. Land and D. C. Roccio, “D-cycloserine: effects on long-term retention of a conditioned response and on memory for contextual attributes,” Neurobiol. Learn. Mem., 72, No. 3, 158–168 (1999).
L. Ledgerwood, R. Richardson, and J. Cranney, “D-cycloserine facilitates extinction of learned fear: effects on reacquisition and generalized extinction,” Biol. Psychiatry, 57, No. 8 841–847 (2005).
H. J. Lee, J.-S. Choi, T. H. Brown, and J. J. Kim, “Amygdalar NMDA receptors are critical for the extinction of multiple conditioned fear responses,” J. Neurosci., 21, No. 11, 4116–4124 (2002).
K. M. Myers and M. Davis, “Behavioral and neural analysis of extinction,” Neuron, 36, No. 4, 567–584 (2002).
J. Podhorna and R. E. Brown, “Strain differences in activity and emotionality do not account for differences in learning and memory performance between C57BL/6 and DBA/2 mice,” Genes Brain Behav., 1, 96–110 (2002).
G. J. Quirk, “Memory for extinction of conditioned fear is long-lasting and persists following spontaneous recovery,” Learn. Mem., 9, No. 6, 402–407 (2002).
R. A. Rescorla, “Protection from extinction,” Learn. Behav., 31, No. 2, 124–132 (2003).
R. L. Ribeiro, R. Andreatini, C. Wolfman, H. Viola, J. H. Medina, and C. Da Cunha, “The ‘anxiety state’ and its relation with rat models of memory and habituation,” Neurobiol. Learn. Mem., 72, No. 2, 78–94 (1999).
R. Roesler, N. Schroder, M. R. Vianna, J. Quevedo, E. Bromberg, F. Kapczinski, and M. B. Ferreira, “Differential involvement of hippocampal and amygdalar NMDA receptors in contextual and aversive aspects of inhibitory avoidance memory in rats,” Brain Res., 975, No. 1–2, 207–213 (2003).
T. Tadano, S. Hozumi, F. Yamadera, A. Murata, F. Niijima, K. Tan-No, O. Nakagawasai, and K. Kisara, “Effects of NMDA receptor-related agonists on learning and memory impairment in olfactory bulbectomized mice,” Meth. Find. Exptl. Clin. Pharmacol., 26, No. 2, 93–97 (2004).
P. M. Wall and C. Messier, “Concurrent modulation of anxiety and memory,” Behav. Brain Res., 109, 229–241 (2000).
J. L. Wiley, A. F. Cristello, and R. L. Balster, “Effects of site-selective NMDA receptor antagonists in an elevated plus-maze model of anxiety in mice,” Eur. J. Pharmacol., 294, 101–107 (1995).
Author information
Authors and Affiliations
Additional information
__________
Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 92, No. 3, pp. 342–350, March, 2006.
Rights and permissions
About this article
Cite this article
Tomilenko, R.A., Dubrovina, N.I. Effects of activation and blockade of NMDA receptors on the extinction of a conditioned passive avoidance response in mice with different levels of anxiety. Neurosci Behav Physiol 37, 509–515 (2007). https://doi.org/10.1007/s11055-007-0044-1
Received:
Issue Date:
DOI: https://doi.org/10.1007/s11055-007-0044-1