GluN2B-containing NMDA receptors and AMPA receptors in medial prefrontal cortex are necessary for odor span in rats

Frontiers in Behavioral Neuroscience

Volumn 7, Issue DEC, 2013, Pages

  Davies, Don A ^a   Greba, Quentin ^a   Howland, John G ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

CNQX; CPP; Glutamate; Odor span task; Ro 25 6981; Working memory

Indexed keywords

AMPA RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DECISION MAKING; LATENT PERIOD; MALE; MEDIAL PREFRONTAL CORTEX; NONHUMAN; ODOR SPAN CAPACITY; OLFACTORY DISCRIMINATION; PREFRONTAL CORTEX; PROTEIN FUNCTION; RAT; REWARD; SPICE; TASK PERFORMANCE; WORKING MEMORY;

EID: 84889644212     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2013.00183     Document Type: Article

References (54)

1. April, L. B., Bruce, K., and Galizio, M. (2013). The magic number 70 (plus or minus 20): variables determining performance in the rodent odor span task. Learn. Motiv. 44, 143-158. doi: 10.1016/j.lmot.2013.03.001
2. Aujla, H., and Beninger, R. J. (2001). Hippocampal-prefrontocortical circuits: PKA inhibition in the prefrontal cortex impairs delayed nonmatching in the radial maze in rats. Behav. Neurosci. 115, 1204-1211. doi: 10.1037/0735-7044.115.6.1204
3. Aura, J., and Riekkinen, P., Jr. (1999). Blockade of NMDA receptors located at the dorsomedial prefrontal cortex impairs spatial working memory in rats. Neuroreport 10, 243-248. doi: 10.1097/00001756-199902050-00008
4. Baddeley, A. (2003). Working memory: looking back and looking forward. Nat. Rev. Neurosci. 4, 829-839. doi: 10.1038/nrn1201
5. Barch, D. M., and Smith, E. (2008). The cognitive neuroscience of working memory: relevance to CNTRICS and schizophrenia. Biol. Psychiatry 64, 11-17. doi: 10.1016/j.biopsych.2008.03.003
6. Barch, D. M., Berman, M. G., Engle, R., Jones, J. H., Jonides, J., Macdonald, A., III, et al. (2009). CNTRICS final task selection: working memory. Schizophr. Bull. 35, 136-152. doi: 10.1093/schbul/sbn153
7. Caetano, M. S., Horst, N. K., Harenberg, L., Liu, B., Arnsten, A. F., and Laubach, M. (2012). Lost in transition: aging-related changes in executive control by the medial prefrontal cortex. J. Neurosci. 32, 3765-3777. doi: 10.1523/jneurosci.6011-11.2012
8. Cazakoff, B. N., and Howland, J. G. (2011). AMPA receptor endocytosis in rat perirhinal cortex underlies retrieval of object memory. Learn. Mem. 18, 688-692. doi: 10.1101/lm.2312711
9. Chey, J., Lee, J., Kim, Y. S., Kwon, S. M., and Shin, Y. M. (2002). Spatial working memory span, delayed response and executive function in schizophrenia. Psychiatry Res. 110, 259-271. doi: 10.1016/s0165-1781(02)00105-1
10. Cui, Y., Jin, J., Zhang, X., Xu, H., Yang, L., Du, D., et al. (2011). Forebrain NR2B overexpression facilitating the prefrontal cortex long-term potentiation and enhancing working memory function in mice. PLoS One 6:e20312. doi: 10.1371/journal.pone.0020312
11. Davies, D. A., Molder, J. J., Greba, Q., and Howland, J. G. (2013). Inactivation of medial prefrontal cortex or acute stress impairs odor span in rats. Learn. Mem. 20, 665-669. doi: 10.1101/lm.032243.113
12. D'Esposito, M. (2007). From cognitive to neural models of working memory. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362, 761-772. doi: 10.1098/rstb.2007.2086
13. Devilbiss, D. M., Jenison, R. L., and Berridge, C. W. (2012). Stress-induced impairment of a working memory task: role of spiking rate and spiking history predicted discharge. PLoS Comput. Biol. 8:e1002681. doi: 10.1371/journal.pcbi.1002681
14. Doyle, K. M., Feerick, S., Kirkby, D. L., Eddleston, A., and Higgins, G. A. (1998). Comparison of various N-methyl-D-aspartate receptor antagonists in a model of short-term memory and on overt behaviour. Behav. Pharmacol. 9, 671-681. doi: 10.1097/00008877-199812000-00003
15. Dudchenko, P. A. (2004). An overview of the tasks used to test working memory in rodents. Neurosci. Biobehav. Rev. 28, 699-709. doi: 10.1016/j.neubiorev.2004.09.002
16. Dudchenko, P. A., Talpos, J., Young, J., and Baxter, M. G. (2012). Animal models of working memory: a review of tasks that might be used in screening drug treatments for the memory impairments found in schizophrenia. Neurosci. Biobehav. Rev. doi: 10.1016/j.neubiorev.2012.03.003. [Epub ahead of print].
17. Dudchenko, P. A., Wood, E. R., and Eichenbaum, H. (2000). Neurotoxic hippocam-pal lesions have no effect on odor span and little effect on odor recognition memory but produce significant impairments on spatial span, recognition and alternation. J. Neurosci. 20, 2964-2977.
18. Fischer, G., Mutel, V., Trube, G., Malherbe, P., Kew, J. N., Mohacsi, E., et al. (1997). Ro 25-6981, a highly potent and selective blocker of N-methyl-D-aspartate receptors containing the NR2B subunit. Characterization in vitro. J. Pharmacol. Exp. Ther. 283, 1285-1292.
19. Floresco, S. B., Seamans, J. K., and Phillips, A. G. (1997). Selective roles for hippocampal, prefrontal cortical and ventral striatal circuits in radial-arm maze tasks with or without a delay. J. Neurosci. 17, 1880-1890.
20. Galizio, M., Deal, M., Hawkey, A., and April, B. (2013). Working memory in the odor span task: effects of chlordiazepoxide, dizocilpine (MK801), morphine and scopolamine. Psychopharmacology (Berl) 225, 397-406. doi: 10.1007/s00213-012-2825-7
21. Gilmartin, M. R., and Helmstetter, F. J. (2010). Trace and contextual fear conditioning require neural activity and NMDA receptor-dependent transmission in the medial prefrontal cortex. Learn. Mem. 17, 289-296. doi: 10.1101/lm.1597410
22. Gilmartin, M. R., Kwapis, J. L., and Helmstetter, F. J. (2013). NR2A-and NR2B-containing NMDA receptors in the prelimbic medial prefrontal cortex differentially mediate trace, delay and contextual fear conditioning. Learn. Mem. 20, 290-294. doi: 10.1101/lm.030510.113
23. Gold, J. M., Hahn, B., Zhang, W. W., Robinson, B. M., Kappenman, E. S., Beck, V. M., et al. (2010). Reduced capacity but spared precision and maintenance of working memory representations in schizophrenia. Arch. Gen. Psychiatry 67, 570-577. doi: 10.1001/archgenpsychiatry.2010.65
24. Goldman-Rakic, P. S. (1996). Regional and cellular fractionation of working memory. Proc. Natl. Acad. Sci. U S A 93, 13473-13480. doi: 10.1073/pnas.93.24.13473
25. Ho, J. W., Narduzzo, K. E., Outram, A., Tinsley, C. J., Henley, J. M., Warburton, E. C., et al. (2011). Contributions of area Te2 to rat recognition memory. Learn. Mem. 18, 493-501. doi: 10.1101/lm.2167511
26. Homayoun, H., and Moghaddam, B. (2007). NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons. J. Neurosci. 27, 11496-11500. doi: 10.1523/jneurosci.2213-07.2007
27. Honore, T., Davies, S. N., Drejer, J., Fletcher, E. J., Jacobsen, P., Lodge, D., et al. (1988). Quinoxalinediones: potent competitive non-NMDA glutamate receptor antagonists. Science 241, 701-703. doi: 10.1126/science.2899909
28. Howland, J. G., and Cazakoff, B. N. (2010). Effects of acute stress and GluN2B-containing NMDA receptor antagonism on object and object-place recognition memory. Neurobiol. Learn. Mem. 93, 261-267. doi: 10.1016/j.nlm.2009.10.006
29. Howland, J. G., and Wang, Y. T. (2008). Synaptic plasticity in learning and memory: stress effects in the hippocampus. Prog. Brain Res. 169, 145-158. doi: 10.1016/s0079-6123(07)00008-8
30. Huntley, J. D., and Howard, R. J. (2010). Working memory in early Alzheimer's disease: a neuropsychological review. Int. J. Geriatr. Psychiatry 25, 121-132. doi: 10.1002/gps.2314
31. Jackson, M. E., Homayoun, H., and Moghaddam, B. (2004). NMDA receptor hypofunction produces concomitant firing rate potentiation and burst activity reduction in the prefrontal cortex. Proc. Natl. Acad. Sci. U S A 101, 8467-8472. doi: 10.1073/pnas.0308455101
32. Kocsis, B. (2012). Differential role of NR2A and NR2B subunits in N-methyl-D-aspartate receptor antagonist-induced aberrant cortical gamma oscillations. Biol. Psychiatry 71, 987-995. doi: 10.1016/j.biopsych.2011.10.002
33. Kolb, B. (1991). Animal models for human PFC-related disorders. Prog. Brain Res. 85, 501-519. doi: 10.1016/S0079-6123(08)62697-7
34. Lehmann, J., Schneider, J., McPherson, S., Murphy, D. E., Bernard, P., Tsai, C., et al. (1987). CPP, a selective N-methyl-D-aspartate (NMDA)-type receptor antagonist: characterization in vitro and in vivo. J. Pharmacol. Exp. Ther. 240, 737-746.
35. Li, H. B., Matsumoto, K., Yamamoto, M., and Watanabe, H. (1997). NMDA but not AMPA receptor antagonists impair the delay-interposed radial maze performance of rats. Pharmacol. Biochem. Behav. 58, 249-253. doi: 10.1016/s0091-3057(97)00015-4
36. Li, N., Lee, B., Liu, R. J., Banasr, M., Dwyer, J. M., Iwata, M., et al. (2010). mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science 329, 959-964. doi: 10.1126/science.1190287
37. Liu, L., Wong, T. P., Pozza, M. F., Lingenhoehl, K., Wang, Y., Sheng, M., et al. (2004). Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304, 1021-1024. doi: 10.1126/science.1096615
38. MacQueen, D. A., Bullard, L., and Galizio, M. (2011). Effects of dizocilpine (MK801) on olfactory span in rats. Neurobiol. Learn. Mem. 95, 57-63. doi: 10.1016/j.nlm.2010.11.004
39. Moghaddam, B., and Adams, B. W. (1998). Reversal of phencyclidine effects by a group II metabotropic glutamate receptor agonist in rats. Science 281, 1349-1352. doi: 10.1126/science.281.5381.1349
40. Murphy, E. R., Fernando, A. B., Urcelay, G. P., Robinson, E. S., Mar, A. C., Theobald, D. E., et al. (2012). Impulsive behaviour induced by both NMDA receptor antagonism and GABAA receptor activation in rat ventromedial prefrontal cortex. Psychopharmacology (Berl) 219, 401-410. doi: 10.1007/s00213-011-2572-1
41. Paxinos, G., and Watson, C. (1997). The Rat Brain in Stereotaxic Coordinates. Amsterdam: Elsevier.
42. Romanides, A. J., Duffy, P., and Kalivas, P. W. (1999). Glutamatergic and dopamin-ergic afferents to the prefrontal cortex regulate spatial working memory in rats. Neuroscience 92, 97-106. doi: 10.1016/s0306-4522(98)00747-7
43. Rushforth, S. L., Allison, C., Wonnacott, S., and Shoaib, M. (2010). Subtype-selective nicotinic agonists enhance olfactory working memory in normal rats: a novel use of the odour span task. Neurosci. Lett. 471, 114-118. doi: 10.1016/j.neulet.2010.01.022
44. Rushforth, S. L., Steckler, T., and Shoaib, M. (2011). Nicotine improves working memory span capacity in rats following sub-chronic ketamine exposure. Neu-ropsychopharmacology 36, 2774-2781. doi: 10.1038/npp.2011.224
45. Seamans, J. K., Floresco, S. B., and Phillips, A. G. (1995). Functional differences between the prelimbic and anterior cingulate regions of the rat prefrontal cortex. Behav. Neurosci. 109, 1063-1073. doi: 10.1037/0735-7044.109.6.1063
46. Smith, J. W., Gastambide, F., Gilmour, G., Dix, S., Foss, J., Lloyd, K., et al. (2011). A comparison of the effects of ketamine and phencyclidine with other antagonists of the NMDA receptor in rodent assays of attention and working memory. Psychopharmacology (Berl) 217, 255-269. doi: 10.1007/s00213-011-2277-5
47. Turchi, J., and Sarter, M. (2000). Cortical cholinergic inputs mediate processing capacity: effects of 192 IgG-saporin-induced lesions on olfactory span performance. Eur. J. Neurosci. 12, 4505-4514. doi: 10.1111/j.1460-9568.2000.01347.x
48. Wang, M., Yang, Y., Wang, C. J., Gamo, N. J., Jin, L. E., Mazer, J. A., et al. (2013). NMDA receptors subserve persistent neuronal firing during working memory in dorsolateral prefrontal cortex. Neuron 77, 736-749. doi: 10.1016/j.neuron.2012.12.032
49. Whitlock, J. R., Heynen, A. J., Shuler, M. G., and Bear, M. F. (2006). Learning induces long-term potentiation in the hippocampus. Science 313, 1093-1097. doi: 10.1126/science.1128134
50. Winters, B. D., and Reid, J. M. (2010). A distributed cortical representation underlies crossmodal object recognition in rats. J. Neurosci. 30, 6253-6261. doi: 10.1523/jneurosci.6073-09.2010
51. Wong, T. P., Howland, J. G., Robillard, J. M., Ge, Y., Yu, W., Titterness, A. K., et al. (2007). Hippocampal long-term depression mediates acute stress-induced spatial memory retrieval impairment. Proc. Natl. Acad. Sci. U S A 104, 11471-11476. doi: 10.1073/pnas.0702308104
52. Yang, C. H., Huang, C. C., and Hsu, K. S. (2005). Behavioral stress enhances hippocampal CA1 long-term depression through the blockade of the glutamate uptake. J. Neurosci. 25, 4288-4293. doi: 10.1523/jneurosci.0406-05.2005
53. Young, J. W., Kerr, L. E., Kelly, J. S., Marston, H. M., Spratt, C., Finlayson, K., et al. (2007). The odour span task: a novel paradigm for assessing working memory in mice. Neuropharmacology 52, 634-645. doi: 10.1016/j.neuropharm.2006.09.006
54. Zhang, X. H., Wu, L. J., Gong, B., Ren, M., Li, B. M., and Zhuo, M. (2008). Inductionand conditioning-protocol dependent involvement of NR2B-containing NMDA receptors in synaptic potentiation and contextual fear memory in the hippocampal CA1 region of rats. Mol. Brain 1:9. doi: 10.1186/1756-6606-1-9