Hippocampal and prefrontal contributions to memory retrieval: Examination of immediate early gene, NMDA receptor and environmental interactions.


Journal

The European journal of neuroscience
ISSN: 1460-9568
Titre abrégé: Eur J Neurosci
Pays: France
ID NLM: 8918110

Informations de publication

Date de publication:
08 2020
Historique:
received: 07 07 2019
accepted: 27 04 2020
pubmed: 5 5 2020
medline: 22 6 2021
entrez: 5 5 2020
Statut: ppublish

Résumé

Animals can use a range of strategies to recall important locations. These include simple stimulus-response strategies and more complex spatial (place) strategies, which are thought to have distinct neural substrates. The hippocampus-and NMDA receptor activation therein-is considered to be crucial for spatial, but not response strategies. The medial prefrontal cortex has also been implicated in memory retrieval; however, evidence concerning its specific role is equivocal. Both hippocampal and prefrontal regions have been associated with flexible behavioural responding (e.g. when task demands change). Here, we investigated the use of spatial and non-spatial strategies in the Morris water maze and their associated brain areas in rats using immediate early gene (IEG) imaging of Zif268 and c-Fos. Specifically, we charted the involvement of hippocampal and prefrontal subregions during retrieval of spatial and non-spatial memories. Behavioural flexibility was also examined using intact and partial cue configurations during recall. Results indicated that regions of both the hippocampus (area CA3) and prefrontal cortex (anterior cingulate cortex) were preferentially engaged in spatial memory recall compared to response learning. In addition, both spatial and non-spatial memories were dependent on NMDA receptor activation. MK801 impaired recall performance across all groups and reduced IEG activation across hippocampal and prefrontal regions. Finally, IEG results revealed divergent patterns of Zif268 and c-Fos activity and support the suggestion that Zif268 plays a functional role in the recall of long-term memories.

Identifiants

pubmed: 32365416
doi: 10.1111/ejn.14768
doi:

Substances chimiques

Early Growth Response Protein 1 0
Receptors, N-Methyl-D-Aspartate 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2982-2994

Subventions

Organisme : Maynooth University Doctoral Teaching scholarship

Informations de copyright

© 2020 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.

Références

Bannerman, D. M., Bus, T., Taylor, A., Sanderson, D. J., Schwarz, I., Jensen, V., & … Sprengel, R. (2012). Dissecting spatial knowledge from spatial choice by hippocampal NMDA receptor deletion. Nature Neuroscience, 15(8), 1153-1159. https://doi.org/10.1038/nn.3166
Bannerman, D. M., Good, M. A., Butcher, S. P., Ramsay, M., & Morris, R. G. (1995). Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature, 378(6553), 182-186.
Barry, D. N., & Commins, S. (2011). Imaging spatial learning in the brain using immediate early genes: Insights, opportunities and limitations. Reviews in the Neurosciences, 22(2), 131-142. https://doi.org/10.1515/rns.2011.019
Barry, D. N., & Commins, S. (2017). Temporal dynamics of immediate early gene expression during cellular consolidation of spatial memory. Behavioral Brain Research, 327, 44-53. https://doi.org/10.1016/j.bbr.2017.03.019
Barry, D. N., & Commins, S. (2019). A novel control condition for spatial learning in the Morris water maze. Journal of Neuroscience Methods, 318, 1-5. https://doi.org/10.1016/j.jneumeth.2019.02.015
Barry, D. N., Coogan, A. N., & Commins, S. (2016). The time course of systems consolidation of spatial memory from recent to remote retention: A comparison of the Immediate Early Genes Zif268, c-Fos and Arc. Neurobiology of Learning and Memory, 128, 46-55. https://doi.org/10.1016/j.nlm.2015.12.010
Broadbent, N. J., Squire, L. R., & Clark, R. E. (2006). Reversible hippocampal lesions disrupt water maze performance during both recent and remote memory tests. Learning & Memory, 13(2), 187-191. https://doi.org/10.1101/lm.134706
Cain, D. P., Saucier, D., Hall, J., Hargreaves, E. L., & Boon, F. (1996). Detailed behavioral analysis of water maze acquisition under APV or CNQX: Contribution of sensorimotor disturbances to drug-induced acquisition deficits. Behavioral Neuroscience, 110(1), 86-102.
Compton, D. M., Griffith, H. R., McDaniel, W. F., Foster, R. A., & Davis, B. K. (1997). The flexible use of multiple cue relationships in spatial navigation: A comparison of water maze performance following hippocampal, medial septal, prefrontal cortex, or posterior parietal cortex lesions. Neurobiology of Learning and Memory, 68(2), 117-132. https://doi.org/10.1006/nlme.1997.3793
Coogan, A. N., & Piggins, H. D. (2003). Circadian and photic regulation of phosphorylation of ERK1/2 and Elk-1 in the suprachiasmatic nuclei of the Syrian hamster. Journal of Neuroscience, 23(7), 3085-3093. https://doi.org/10.1523/JNEUROSCI.23-07-03085.2003
de Bruin, J. P., Moita, M. P., de Brabander, H. M., & Joosten, R. N. (2001). Place and response learning of rats in a Morris water maze: Differential effects of fimbria fornix and medial prefrontal cortex lesions. Neurobiology of Learning and Memory, 75(2), 164-178. https://doi.org/10.1006/nlme.2000.3962
de Bruin, J. P., Sanchez-Santed, F., Heinsbroek, R. P., Donker, A., & Postmes, P. (1994). A behavioural analysis of rats with damage to the medial prefrontal cortex using the Morris water maze: Evidence for behavioural flexibility, but not for impaired spatial navigation. Brain Research, 652(2), 323-333. https://doi.org/10.1016/0006-8993(94)90243-7
Devan, B. D., McDonald, R. J., & White, N. M. (1999). Effects of medial and lateral caudate-putamen lesions on place- and cue-guided behaviors in the water maze: Relation to thigmotaxis. Behavioral Brain Research, 100(1-2), 5-14. https://doi.org/10.1016/S0166-4328(98)00107-7
Farina, F. R., Burke, T., Coyle, D., Jeter, K., McGee, M., O'Connell, J., … Commins, S. (2015). Learning efficiency: The influence of cue salience during spatial navigation. Behav Processes, 116, 17-27. https://doi.org/10.1016/j.beproc.2015.04.010
Farina, F. R., & Commins, S. (2016). Differential expression of immediate early genes Zif268 and c-Fos in the hippocampus and prefrontal cortex following spatial learning and glutamate receptor antagonism. Behavioral Brain Research, 307, 194-198. https://doi.org/10.1016/j.bbr.2016.04.002
Fellini, L., Florian, C., Courtey, J., & Roullet, P. (2009). Pharmacological intervention of hippocampal CA3 NMDA receptors impairs acquisition and long-term memory retrieval of spatial pattern completion task. Learning & Memory, 16(6), 387-394. https://doi.org/10.1101/lm.1433209
Fleischmann, A., Hvalby, O., Jensen, V., Strekalova, T., Zacher, C., Layer, L. E., & … Gass, P. (2003). Impaired long-term memory and NR2A-type NMDA receptor-dependent synaptic plasticity in mice lacking c-Fos in the CNS. Journal of Neuroscience, 23(27), 9116-9122. https://doi.org/10.1523/JNEUROSCI.23-27-09116.2003
Guzowski, J. F. (2002). Insights into immediate-early gene function in hippocampal memory consolidation using antisense oligonucleotide and fluorescent imaging approaches. Hippocampus, 12(1), 86-104. https://doi.org/10.1002/hipo.10010
Guzowski, J. F., Setlow, B., Wagner, E. K., & McGaugh, J. L. (2001). Experience-dependent gene expression in the rat hippocampus after spatial learning: A comparison of the immediate-early genes Arc, c-fos, and zif268. Journal of Neuroscience, 21(14), 5089-5098.
Harvey, D. R., Brant, L., & Commins, S. (2009). Differences in cue-dependent spatial navigation may be revealed by in-depth swimming analysis. Behavioural Processes, 82(2), 190-197. https://doi.org/10.1016/j.beproc.2009.06.008
Jenkins, T. A., Amin, E., Harold, G. T., Pearce, J. M., & Aggleton, J. P. (2003). Distinct patterns of hippocampal formation activity associated with different spatial tasks: A Fos imaging study in rats. Experimental Brain Research, 151(4), 514-523. https://doi.org/10.1007/s00221-003-1499-0
Jo, Y. S., Park, E. H., Kim, I. H., Park, S. K., Kim, H., Kim, H. T., & Choi, J. S. (2007). The medial prefrontal cortex is involved in spatial memory retrieval under partial-cue conditions. Journal of Neuroscience, 27(49), 13567-13578. https://doi.org/10.1523/JNEUROSCI.3589-07.2007
Jones, M. W., Errington, M. L., French, P. J., Fine, A., Bliss, T. V., Garel, S., … Davis, S. (2001). A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nature Neuroscience, 4(3), 289-296. https://doi.org/10.1038/85138
Kealy, J., Diviney, M., Kehoe, E., McGonagle, V., O'Shea, A., Harvey, D., & Commins, S. (2008). The effects of overtraining in the Morris water maze on allocentric and egocentric learning strategies in rats. Behavioral Brain Research, 192(2), 259-263. https://doi.org/10.1016/j.bbr.2008.04.009
Kubik, S., Miyashita, T., & Guzowski, J. F. (2007). Using immediate-early genes to map hippocampal subregional functions. Learning & Memory, 14(11), 758-770. https://doi.org/10.1101/lm.698107
Lanahan, A., & Worley, P. (1998). Immediate-early genes and synaptic function. Neurobiology of Learning and Memory, 70(1-2), 37-43. https://doi.org/10.1006/nlme.1998.3836
Lee, I., & Kesner, R. P. (2002). Differential contribution of NMDA receptors in hippocampal subregions to spatial working memory. Nature Neuroscience, 5(2), 162-168. https://doi.org/10.1038/nn790
Li, H. B., Matsumoto, K., Yamamoto, M., & Watanabe, H. (1997). NMDA but not AMPA receptor antagonists impair the delay-interposed radial maze performance of rats. Pharmacology Biochemistry and Behavior, 58(1), 249-253. https://doi.org/10.1016/S0091-3057(97)00015-4
Liang, K. C., Hon, W., Tyan, Y. M., & Liao, W. L. (1994). Involvement of hippocampal NMDA and AMPA receptors in acquisition, formation and retrieval of spatial memory in the Morris water maze. Chinese Journal of Physiology, 37(4), 201-212.
Martin, S. J., Grimwood, P. D., & Morris, R. G. (2000). Synaptic plasticity and memory: An evaluation of the hypothesis. Annual Review of Neuroscience, 23, 649-711. https://doi.org/10.1146/annurev.neuro.23.1.649
McDonald, R. J., & White, N. M. (1994). Parallel information processing in the water maze: Evidence for independent memory systems involving dorsal striatum and hippocampus. Behavioral and Neural Biology, 61(3), 260-270. https://doi.org/10.1016/S0163-1047(05)80009-3
McLamb, R. L., Williams, L. R., Nanry, K. P., Wilson, W. A., & Tilson, H. A. (1990). MK-801 impedes the acquisition of a spatial memory task in rats. Pharmacology Biochemistry and Behavior, 37(1), 41-45. https://doi.org/10.1016/0091-3057(90)90038-J
Mei, B., Li, F., Gu, Y., Cui, Z., & Tsien, J. Z. (2011). NMDA receptors are not required for pattern completion during associative memory recall. PLoS ONE, 6(4), e19326. https://doi.org/10.1371/journal.pone.0019326
Morris, R. G., Anderson, E., Lynch, G. S., & Baudry, M. (1986). Selective impairment of learning and blockade of long-term potentiation by an N-methyl-d-aspartate receptor antagonist, AP5. Nature, 319, 774-776. https://doi.org/10.1038/319774a0
Morris, R. G. M., Garrud, P., Rawlins, J. N., & O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature, 297(5868), 681-683.
Morris, R. G., Steele, R. J., Bell, J. E., & Martin, S. J. (2013). N-methyl-d-aspartate receptors, learning and memory: Chronic intraventricular infusion of the NMDA receptor antagonist d-AP5 interacts directly with the neural mechanisms of spatial learning. European Journal of Neuroscience, 37(5), 700-717.
Nakazawa, K., Quirk, M. C., Chitwood, R. A., Watanabe, M., Yeckel, M. F., Sun, L. D., &…Tonegawa S. (2002). Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science, 297(5579), 211-218.
Niewoehner, B., Single, F. N., Hvalby, O., Jensen, V., Meyer zum Alten Borgloh, S., Seeburg, P. H., … Bannerman, D. M. (2007). Impaired spatial working memory but spared spatial reference memory following functional loss of NMDA receptors in the dentate gyrus. European Journal of Neuroscience, 25(3), 837-846. https://doi.org/10.1111/j.1460-9568.2007.05312.x
Packard, M. G., & McGaugh, J. L. (1992). Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: Further evidence for multiple memory systems. Behavioral Neuroscience, 106(3), 439-446. https://doi.org/10.1037/0735-7044.106.3.439
Paxinos, G., & Watson, C. (2007). The rat brain in stereotaxic coordinates. London, UK: Elsevier.
Piva, A., Gerace, E., Di Chio, M., Osanni, L., Padovani, L., Caffino, L., … Chiamulera, C. (2018). The metaplastic effects of NMDA receptors blockade on reactivation of instrumental memories in rats. Neurobiology of Learning and Memory, 154, 87-96.
Rice, J. P., Wallace, D. G., & Hamilton, D. A. (2015). Lesions of the hippocampus or dorsolateral striatum disrupt distinct aspects of spatial navigation strategies based on proximal and distal information in a cued variant of the Morris water task. Behavioural Brain Research, 289, 105-117. https://doi.org/10.1016/j.bbr.2015.04.026
Rodrigo, T. (2002). Navigational strategies and models. Psicológica: Revista De Metodología Y Psicología Experimental, 23(1), 3-32.
Save, E., & Poucet, B. (2000). Involvement of the hippocampus and associative parietal cortex in the use of proximal and distal landmarks for navigation. Behavioral Brain Research, 109(2), 195-206. https://doi.org/10.1016/S0166-4328(99)00173-4
Shapiro, M. L., & Caramanos, Z. (1990). NMDA antagonist MK-801 impairs acquisition but not performance of spatial working and reference memory. Psychobiology, 18(2), 231-243.
Shapiro, M. L., & O'Connor, C. (1992). N-methyl-D-aspartate receptor antagonist MK-801 and spatial memory representation: Working memory is impaired in an unfamiliar environment but not in a familiar environment. Behavioral Neuroscience, 106(4), 604-612.
Shires, K. L., & Aggleton, J. P. (2008). Mapping immediate-early gene activity in the rat after place learning in a water-maze: The importance of matched control conditions. European Journal of Neuroscience, 28(5), 982-996. https://doi.org/10.1111/j.1460-9568.2008.06402.x
Simon, N. I., Stevens, J. S., Curtis, N. J., & Ramus, S. J. (2011). Preserved object discrimination in the Morris water maze following lesions of the fornix in rats. Journal Behavioral and Neuroscience Research, 9(2), 109-119.
Sutherland, R. J., & Rodriguez, A. J. (1989). The role of the fornix/fimbria and some related subcortical structures in place learning and memory. Behavioral Brain Research, 32(3), 265-277. https://doi.org/10.1016/S0166-4328(89)80059-2
Teixeira, C. M., Pomedli, S. R., Maei, H. R., Kee, N., & Frankland, P. W. (2006). Involvement of the anterior cingulate cortex in the expression of remote spatial memory. Journal of Neuroscience, 26(29), 7555-7564.
Tsien, J. Z., Huerta, P. T., & Tonegawa, S. (1996). The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell, 87(7), 1327-1338. https://doi.org/10.1016/S0092-8674(00)81827-9
Van der Staay, F. J., Rutten, K., Erb, C., & Blokland, A. (2011). Effects of the cognition impairer MK-801 on learning and memory in mice and rats. Behavioral Brain Research, 220(1), 215-229. https://doi.org/10.1016/j.bbr.2011.01.052
Vorhees, C. V., & Williams, M. T. (2014). Assessing spatial learning and memory in rodents. ILAR Journal, 55(2), 310-332. https://doi.org/10.1093/ilar/ilu013
Whitlock, J. R., Sutherland, R. J., Witter, M. P., Moser, M. B., & Moser, E. I. (2008). Navigating from hippocampus to parietal cortex. Proceedings of the National Academy of Sciences United States of America, 105(39), 14755-14762. https://doi.org/10.1073/pnas.0804216105
Zangenehpour, S., & Chaudhuri, A. (2002). Differential induction and decay curves of c-fos and zif268 revealed through dual activity maps. Brain Research. Molecular Brain Research, 109(1-2), 221-225. https://doi.org/10.1016/S0169-328X(02)00556-9

Auteurs

Francesca R Farina (FR)

Department of Psychology, Maynooth University, Maynooth, Co. Kildare, Ireland.
Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin 2, Ireland.

Seán Commins (S)

Department of Psychology, Maynooth University, Maynooth, Co. Kildare, Ireland.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH