Prolonged inactivation of the hippocampus reveals temporally graded retrograde amnesia for unreinforced spatial learning in rats
Abstract
We investigated whether systems consolidation of spatial memory could be detected in a non-navigational, spatial-learning test that takes advantage of rats' natural propensity to preferentially investigate an object that was displaced relative to spatial cues more than an object that remained stationary. Previous studies using navigational spatial-learning tests have generally failed to reveal temporally-graded retrograde amnesia, possibly because the hippocampus needs to be intact for the retrieval and/or processing of navigational information during the test. In the present study, the hippocampus of rats was kept inactivated, at two sites along its septo-temporal axis (dorsal and intermediate), for four consecutive days, beginning either 3h or 5 days after familiarization to two identical objects in an open field. Rats that had their hippocampus inactivated beginning 5 days but not 3h after familiarization showed evidence that they remembered the previous location of the displaced object. The results suggest that systems consolidation of spatial memories can be detected using a non-navigational test of spatial memory.
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Intra-hippocampal infusions of muscimol injected twice daily for 4 consecutive days, when injected 3 hours, but not 5 days, after the sample trial, impaired long-term OPP memory tested 2-4 days after the last infusion.
“Furthermore, when injected 3 hours, but not 5 days, after the sample trial, intra-hippocampal infusions of muscimol injected twice daily for 4 consecutive days, impaired long-term OPP memory which was tested 2–4 days after the last infusion of muscimol (Gaskin et al., 2011).”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Gaskin et al., 2011
Pre-test intra-hippocampus infusions of muscimol disrupted OPP memory tested 24 hours later in rats, supporting a critical role of the hippocampus in the retrieval of long-term OPP memory.
“Pre-test intra-hippocampus infusions of muscimol also disrupted OPP memory tested 24 hours later in rats (Gaskin et al., 2011), supporting a critical role of the hippocampus in the retrieval of long-term OPP memory.”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Gaskin et al., 2011
Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010 · see citing works
REMEMBERING: A STUDY IN EXPERIMENTAL AND SOCIAL PSYCHOLOGY
Bartlett, F. C., & Burt, C. (1933) · British Journal of Educational Psychology · doi:10.1111/j.2044-8279.1933.tb02913.x · Cited by 7,475 · see citing works
Developments of a water-maze procedure for studying spatial learning in the rat
Morris, R. (1984) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(84)90007-4 · Cited by 7,180 · see citing works
Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans.
Squire, L. R. (1992) · Psychological Review · doi:10.1037/0033-295x.99.2.195 · Cited by 5,376 · see citing works
(2005) · Choice Reviews Online · doi:10.5860/choice.43-0626 · Cited by 4,726 · see citing works
Modality-Specific Retrograde Amnesia of Fear
Kim, J. J., & Fanselow, M. S. (1992) · Science · doi:10.1126/science.1585183 · Cited by 2,483 · see citing works
Bartlett, F. C., & Kintsch, W. (1995) · Cambridge University Press eBooks · doi:10.1017/cbo9780511759185 · Cited by 2,408 · see citing works
Memory consolidation, retrograde amnesia and the hippocampal complex
Nadel, L., & Moscovitch, M. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80010-4 · Cited by 1,924 · see citing works
Protein synthesis and memory: A review.
Davis, H. P., & Squire, L. R. (1984) · Psychological Bulletin · doi:10.1037/0033-2909.96.3.518 · Cited by 1,505 · see citing works
Retrograde amnesia and memory consolidation: a neurobiological perspective
Squire, L. R., & Alvarez, P. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80023-9 · Cited by 1,412 · see citing works
Cognitive Neuroscience and the Study of Memory
Milner, B. A., Squire, L. R., & Kandel, E. R. (1998) · Neuron · doi:10.1016/s0896-6273(00)80987-3 · Cited by 1,300 · see citing works
Schemas and Memory Consolidation.
Tse, D., Langston, R. F., Kakeyama, M., Bethus, I., Spooner, P. A., Wood, E. R., Witter, M. P., & Morris, R. G. M. (2007) · Science · doi:10.1126/science.1135935 · Cited by 1,244 · see citing works
Memory consolidation and the medial temporal lobe: a simple network model.
Alvarez, P., & Squire, L. R. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.15.7041 · Cited by 1,054 · see citing works
Misanin, J. R., Miller, R. R., & Lewis, D. J. (1968) · Science · doi:10.1126/science.160.3827.554 · Cited by 872 · see citing works
The Primate Hippocampal Formation: Evidence for a Time-Limited Role in Memory Storage
Zola-Morgan, S. M., & Squire, L. R. (1990) · Science · doi:10.1126/science.2218534 · Cited by 863 · see citing works
Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats
Maren, S., Aharonov, G., & Fanselow, M. S. (1997) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00088-0 · Cited by 765 · see citing works
Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts
Mumby, D. G., Gaskin, S., Glenn, M. J., Schramek, T. E., & Lehmann, H. (2002) · Learning & Memory · doi:10.1101/lm.41302 · Cited by 714 · see citing works
Anagnostaras, S., Maren, S., & Fanselow, M. S. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-03-01106.1999 · Cited by 656 · see citing works
GABA and GABA Receptors in the Central Nervous System and Other Organs
Watanabe, M., Maemura, K., Kanbara, K., Tamayama, T., & Hayasaki, H. (2002) · International review of cytology · doi:10.1016/s0074-7696(02)13011-7 · Cited by 631 · see citing works
The labile nature of consolidation theory
Nader, K., Schafe, G. E., & LeDoux, J. E. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044580 · Cited by 613 · see citing works
Object recognition memory and the rodent hippocampus
Broadbent, N. J., Gaskin, S., Squire, L. R., & Clark, R. E. (2010) · Learning & Memory · doi:10.1101/lm.1650110 · Cited by 568 · see citing works
Reversible neural inactivation reveals hippocampal participation in several memory processes
Riedel, G., Micheau, J., Lam, A. G. M., Roloff, E. V. L., Martin, S. J., Bridge, H., de Hoz, L., Poeschel, B., McCulloch, J., & Morris, R. (1999) · Nature Neuroscience · doi:10.1038/13202 · Cited by 478 · see citing works
Martin, J. H. (1991) · Neuroscience Letters · doi:10.1016/0304-3940(91)90784-q · Cited by 459 · see citing works
Memory for places learned long ago is intact after hippocampal damage
Teng, E., & Squire, L. R. (1999) · Nature · doi:10.1038/23276 · Cited by 372 · see citing works
Anterograde and retrograde amnesia in rats with dorsal hippocampal or dorsomedial thalamic lesions
Winocur, G. (1990) · Behavioural Brain Research · doi:10.1016/0166-4328(90)90012-4 · Cited by 352 · see citing works
Navigation around London by a taxi driver with bilateral hippocampal lesions
Maguire, E. A., Nannery, R., & Spiers, H. J. (2006) · Brain · doi:10.1093/brain/awl286 · Cited by 335 · see citing works
Remote spatial memory in an amnesic person with extensive bilateral hippocampal lesions
Rosenbaum, R. S., Priselac, S., Köhler, S., Black, S. E., Gao, F., Nadel, L., & Moscovitch, M. (2000) · Nature Neuroscience · doi:10.1038/79867 · Cited by 293 · see citing works
Ennaceur, A., & Meliani, K. (1992) · Behavioural Brain Research · doi:10.1016/s0166-4328(05)80315-8 · Cited by 276 · see citing works
Maren, S., & Holt, W. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.1.97 · Cited by 272 · see citing works
Conjunctive representations, the hippocampus, and contextual fear conditioning
RUDY, J. W., & O'REILLY, R. C. (2001) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/cabn.1.1.66 · Cited by 247 · see citing works
Muscimol Inactivation of the Dorsal Hippocampus Impairs Contextual Retrieval of Fear Memory
Holt, W., & Maren, S. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-20-09054.1999 · Cited by 213 · see citing works
Hippocampus and remote spatial memory in rats
Clark, R. E., Broadbent, N., & Squire, L. R. (2004) · Hippocampus · doi:10.1002/hipo.20056 · Cited by 209 · see citing works
Clark, R. E., Broadbent, N., Zola, S. M., & Squire, L. R. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-11-04663.2002 · Cited by 196 · see citing works
Whishaw, I. Q., Hines, D. J., & Wallace, D. G. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00359-x · Cited by 192 · see citing works
Retrograde amnesia after hippocampal damage: Recent vs. remote memories in two tasks
Sutherland, R. J., Weisend, M. P., Mumby, D. G., Astur, R. S., Hanlon, F. M., Koerner, A., Thomas, M. J., Wu, Y., Moses, S. N., Cole, C., et al. (2001) · Hippocampus · doi:10.1002/1098-1063(2001)11:1 · Cited by 190 · see citing works
An allocentric spatial model for the hippocampal cognitive map
O'Keefe, J. M. (1991) · Hippocampus · doi:10.1002/hipo.450010303 · Cited by 162 · see citing works
Winocur, G., Moscovitch, M., Fogel, S., Rosenbaum, R. S., & Sekeres, M. (2005) · Nature Neuroscience · doi:10.1038/nn1401 · Cited by 161 · see citing works
Retrograde and anterograde object recognition in rats with hippocampal lesions
Gaskin, S., Tremblay, A., & Mumby, D. G. (2003) · Hippocampus · doi:10.1002/hipo.10154 · Cited by 160 · see citing works
Edeline, J., Hars, B., Hennevin, E., & Cotillon, N. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2001.4035 · Cited by 157 · see citing works
Mumby, D. G. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00097-2 · Cited by 145 · see citing works
Broadbent, N., Squire, L. R., & Clark, R. E. (2006) · Learning & Memory · doi:10.1101/lm.134706 · Cited by 138 · see citing works
Sutherland, R. J., O'Brien, J., & Lehmann, H. (2008) · Hippocampus · doi:10.1002/hipo.20431 · Cited by 137 · see citing works
Cho, Y. H., Béracochéa, D., & Jaffard, R. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-04-01759.1993 · Cited by 129 · see citing works
Lehmann, H., Lacanilao, S., & Sutherland, R. J. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05374.x · Cited by 129 · see citing works
Clark, R. E., Broadbent, N., & Squire, L. R. (2005) · Hippocampus · doi:10.1002/hipo.20076 · Cited by 119 · see citing works
The hippocampus, consolidation and on-line memory
Knowlton, B. J., & Fanselow, M. S. (1998) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(98)80154-2 · Cited by 102 · see citing works
Thinus‐Blanc, C., Save, É., Rossi‐Arnaud, C., Tozzi, A., & Ammassari‐Teule, M. (1996) · Behavioural Brain Research · doi:10.1016/0166-4328(96)00016-2 · Cited by 97 · see citing works
Memory and cerebral protein synthesis in mice as affected by graded amounts of puromycin
Flexner, L. B., Flexner, J. B., & Stellar, E. (1965) · Experimental Neurology · doi:10.1016/0014-4886(65)90114-7 · Cited by 90 · see citing works
To consolidate or not to consolidate: what are the questions?
Dudai, Y., & Morris, R. (2000) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198524823.003.0011 · Cited by 87 · see citing works
Making context memories independent of the hippocampusPreprint
Lehmann, H., Sparks, F. T., Spanswick, S. C., Hadikin, C., McDonald, R. J., & Sutherland, R. J. (2009) · Learning & Memory · doi:10.1101/lm.1385409 · Cited by 86 · see citing works
Wiig, K. A., Cooper, L. N., & Bear, M. F. (1996) · Learning & Memory · doi:10.1101/lm.3.4.313 · Cited by 72 · see citing works
GABA and Muscimol as Reversible Inactivation Tools in Learning and Memory
Majchrzak, M. J., & Scala, G. D. (2000) · Neural Plasticity · doi:10.1155/np.2000.19 · Cited by 66 · see citing works
Mumby, D. G., & Glenn, M. J. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00217-5 · Cited by 62 · see citing works
Effect of hippocampal isolation on retention.
Uretsky, E., & McCleary, R. A. (1969) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0027647 · Cited by 54 · see citing works
Spatial Location Learning in Mice with Ibotenate Lesions of Entorhinal Cortex or Subiculum
Cho, Y. H., & Jaffard, R. (1995) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1995.0011 · Cited by 52 · see citing works
Kubie, J. L., Sutherland, R. J., & Muller, R. U. (1999) · Psychobiology · doi:10.3758/bf03332125 · Cited by 50 · see citing works
Winocur, G., Moscovitch, M., Rosenbaum, R. S., & Sekeres, M. (2010) · Hippocampus · doi:10.1002/hipo.20721 · Cited by 49 · see citing works
Ramos, J. M. J. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00388.x · Cited by 47 · see citing works
Mao, J.-B., & Robinson, J. K. (1998) · Brain Research · doi:10.1016/s0006-8993(97)01324-3 · Cited by 40 · see citing works
McDonald, R. J., Yim, T. T.-L., Lehmann, H., Sparks, F. T., Zelinski, E. L., Sutherland, R. J., & Hong, N. S. (2010) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2010.06.001 · Cited by 35 · see citing works
Jersalinsky, D., Quillfeldt, J. A., Walz, R., da Silva, R. C., Silva, M. B. E., Bianchin, M. M., Schmitz, P. K., Zanatta, M. S., Ruschel, A. C., Paczko, N., et al. (1994) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(05)80066-4 · Cited by 33 · see citing works
Dorsal hippocampus function in learning and expressing a spatial discriminationPreprint
White, N. M., & Gaskin, S. (2006) · Learning & Memory · doi:10.1101/lm.138806 · Cited by 28 · see citing works
Gaskin, S., & White, N. M. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.09.012 · Cited by 25 · see citing works
Patterns of retrograde amnesia for recent and remote incidental spatial learning in rats
Gaskin, S., Tardif, M., & Mumby, D. G. (2009) · Hippocampus · doi:10.1002/hipo.20583 · Cited by 19 · see citing works
Broadbent, N., Squire, L. R., & Clark, R. E. (2009) · Hippocampus · doi:10.1002/hipo.20722 · Cited by 19 · see citing works
Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways.
Lavenex (2000) · Pure Amsterdam UMC · doi:10.1002/1098-1063(2000)10:4 · Cited by 1 · see citing works
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Chao, O. Y., de Souza Silva, M. A., Yang, Y.-M., & Huston, J. P. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.04.007 · Cited by 158 · see citing works
Transcranial slow oscillation stimulation during sleep enhances memory consolidation in rats
Binder, S., Berg, K., Gasca, F., Lafon, B., Parra, L. C., Born, J., & Marshall, L. (2014) · Brain Stimulation · doi:10.1016/j.brs.2014.03.001 · Cited by 74 · see citing works
c-Fos expression correlates with performance on novel object and novel place recognition tests
Mendez, M., Arias, N., Uceda, S., & Arias, J. L. (2015) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2015.07.004 · Cited by 54 · see citing works
Callaghan, C. K., & Kelly, A. M. (2012) · Hippocampus · doi:10.1002/hipo.22033 · Cited by 53 · see citing works
Beeman, C. L., Bauer, P. S., Pierson, J. L., & Quinn, J. J. (2013) · Learning & Memory · doi:10.1101/lm.031161.113 · Cited by 46 · see citing works
Pierson, J. L., Pullins, S. E., & Quinn, J. J. (2015) · Hippocampus · doi:10.1002/hipo.22413 · Cited by 24 · see citing works
Wartman, B. C., Gervais, N. J., Smith, C., Comba, R., Mumby, D. G., & Holahan, M. R. (2012) · Brain Research · doi:10.1016/j.brainres.2012.08.012 · Cited by 13 · see citing works
Ramos, J. M. J. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.08.036 · Cited by 5 · see citing works
Scott, G. A., Saucier, D. M., & Lehmann, H. (2016) · Journal of Behavioral and Brain Science · doi:10.4236/jbbs.2016.64019 · Cited by 4 · see citing works
Coria-Lucero, C. D., Ledezma, C., Castro, A., Delgado, S. M., Anzulovich, A. C., & Navigatore-Fonzo, L. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.01.014 · Cited by 4 · see citing works
Tanninen, S. E. (2012) · TSpace (University of Toronto)
- Authors
- Gaskin, S., Tardif, M., & Mumby, D. G.
- Affiliations
- Concordia University (CA)
- Corresponding author
- Gaskin, Stéphane
- Venue
- Neurobiology of Learning and Memory
- Publisher
- Elsevier BV
- Published
- 2011-09
- Volume
- 96
- Issue
- 2
- Pages
- 288-296
- ISSN
- 1074-7427 (ISSN-L)
- OpenAlex
- W2163339613
- Cited by
- 11
- References
- 69
- Citations by year
- 2021: 1 · 2020: 1 · 2016: 1 · 2015: 2 · 2014: 1 · 2013: 1 · 2012: 4
- FWCI
- 0.97
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neurobiology of Learning and Memory (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Natural Sciences and Engineering Research Council of Canada
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Keywords
- hippocampal inactivation, retrograde amnesia, systems consolidation, spatial memory, object displacement, rats
- MeSH terms
- Amnesia, Retrograde, Animals, Hippocampus, Male, Reinforcement, Psychology, Retention, Psychology, Space Perception, Maze Learning, Rats, Long-Evans, Rats
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