Spatial memory, recognition memory, and the hippocampus
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There is wide agreement that spatial memory is dependent on the integrity of the hippocampus, but the importance of the hippocampus for nonspatial tasks, including tasks of object recognition memory is not as clear. We examined the relationship between hippocampal lesion size and both spatial memory and object recognition memory in rats. Spatial memory was impaired after bilateral dorsal hippocampal lesions that encompassed 30-50% total volume, and as lesion size increased from 50% to approximately 100% of total hippocampal volume, performance was similarly impaired. In contrast, object recognition was intact after dorsal hippocampal lesions that damaged 50-75% of total hippocampal volume and was impaired only after larger lesions that encompassed 75-100% of hippocampal volume. Last, ventral hippocampal lesions that encompassed approximately 50% of total hippocampal volume impaired spatial memory but did not affect object recognition memory. These findings show that the hippocampus is important for both spatial memory and recognition memory. However, spatial memory performance requires more hippocampal tissue than does recognition memory.
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Some studies showed that rats with hippocampal lesions had impaired NOP (across delays from 10 minutes to 24 hours) memory.
“Some studies showed that rats with hippocampal lesions had impaired NOP (across delays from 10 minutes to 24 hours) memory (Ainge et al., 2006; Broadbent et al., 2010; Broadbent et al., 2004; Clark et al., 2000), whereas the majority of the studies employing hippocampal lesions in rats failed to report an influence in the NOP test (Albasser et al., 2012; Albasser et al., 2010; Barker and Warburton”
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 Broadbent et al., 2004
Severe, but not partial, lesions of the hippocampus influenced NOP memory.
“Lesion extent of the hippocampus has been discussed, in that severe, but not partial, lesions influenced NOP memory (Broadbent et al., 2004).”
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 Broadbent et al., 2004
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Cites
(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010 · 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
Self-citationSquire, L. R., Stark, C. E. L., & Clark, R. E. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144130 · Cited by 2,680 · see citing works
Self-citationRecognition memory: What are the roles of the perirhinal cortex and hippocampus?
Brown, M. W., & Aggleton, J. P. (2001) · Nature reviews. Neuroscience · doi:10.1038/35049064 · Cited by 1,555 · see citing works
From Conditioning to Conscious Recollection
Eichenbaum, H., & Cohen, N. J. (2004) · doi:10.1093/acprof:oso/9780195178043.001.0001 · Cited by 1,026 · see citing works
Moser, E., Moser, M. ‐., & Andersen, P. N. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-09-03916.1993 · Cited by 916 · see citing works
Spatial learning with a minislab in the dorsal hippocampus.
Moser, M., Moser, E. I., Forrest, E., Andersen, P. N., & Morris, R. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.21.9697 · Cited by 902 · see citing works
Impaired Recognition Memory in Rats after Damage to the Hippocampus
Clark, R. E., Zola, S. M., & Squire, L. R. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-23-08853.2000 · Cited by 740 · see citing works
Self-citationHippocampal 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
Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry
Brun, V. H., Otnæss, M. K., Molden, S., Steffenach, H.-A., Witter, M. P., Moser, M.-B., & Moser, E. I. (2002) · Science · doi:10.1126/science.1071089 · Cited by 606 · see citing works
Winters, B. D., Forwood, S., Cowell, R. A., Saksida, L. M., & Bussey, T. J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1346-04.2004 · Cited by 588 · see citing works
Impaired Recognition Memory in Monkeys after Damage Limited to the Hippocampal Region
Zola, S. M., Squire, L. R., Teng, E., Stefanacci, L., Buffalo, E. A., & Clark, R. E. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-01-00451.2000 · Cited by 477 · see citing works
Self-citationRecognition memory and the human hippocampus.
Manns, J., Hopkins, R., Reed, J. M., Kitchener, E. G., & Squire, L. (2003) · Neuron · doi:10.1016/s0896-6273(02)01147-9 · Cited by 472 · see citing works
Self-citationMurray, E. A., & Mishkin, M. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-16-06568.1998 · Cited by 434 · see citing works
Bannerman, D. M., Yee, B. K., Good, M. A., Heupel, M. J., Iversen, S. D., & Rawlins, J. N. P. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.6.1170 · Cited by 397 · see citing works
Perspectives on object-recognition memory following hippocampal damage: lessons from studies in rats
Mumby, D. G. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00367-9 · Cited by 356 · see citing works
Effects of Stress and Hippocampal NMDA Receptor Antagonism on Recognition Memory in RatsPreprint
Baker, K. B., & Kim, J. J. (2002) · Learning & Memory · doi:10.1101/lm.46102 · Cited by 292 · see citing works
Holdstock, J. S., Mayes, A. R., Roberts, N., Cezayirli, E., Isaac, C. L., O'REILLY, R. C., & Norman, K. (2002) · Hippocampus · doi:10.1002/hipo.10011 · Cited by 280 · see citing works
Pothuizen, H. H. J., Zhang, W., Jongen‐Rêlo, A. L., Feldon, J., & Yee, B. K. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2004.03170.x · Cited by 274 · see citing works
Entorhinal cortex of the rat: Organization of intrinsic connections
Dolorfo, C. L., & Amaral, D. G. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980817)398:1 · Cited by 268 · see citing works
Lee, I., & Kesner, R. P. (2004) · Hippocampus · doi:10.1002/hipo.10167 · Cited by 253 · see citing works
Nemanic, S., Alvarado, M. C., & Bachevalier, J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3763-03.2004 · Cited by 217 · 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
Handelmann, G. E., & Olton, D. S. (1981) · Brain Research · doi:10.1016/0006-8993(81)90183-9 · Cited by 181 · see citing works
SUZUKI, W. A., & Eichenbaum, H. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06726.x · Cited by 175 · 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
Rats with lesions of the hippocampus are impaired on the delayed nonmatching‐to‐sample task†
Clark, R. E., West, A. N., Zola, S. M., & Squire, L. R. (2001) · Hippocampus · doi:10.1002/hipo.1035 · Cited by 135 · see citing works
Self-citationde Hoz, L., Knox, J., & Morris, R. (2003) · Hippocampus · doi:10.1002/hipo.10079 · Cited by 135 · see citing works
Steffenach, H.-A., Sloviter, R. S., Moser, E. I., & Moser, M. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.042700999 · Cited by 129 · see citing works
Duva, C. A., Floresco, S., Wunderlich, G. R., Lao, T. L., Pinel, J. P. J., & Phillips, A. G. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.6.1184 · Cited by 111 · see citing works
Visual memory task for rats reveals an essential role for hippocampus and perirhinal cortex
Prusky, G. T., Douglas, R. M., Nelson, L., Shabanpoor, A., & Sutherland, R. J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308528101 · Cited by 108 · see citing works
Duva, C. A., Floresco, S., Wunderlich, G. R., et al. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.6.1184 · Cited by 96 · see citing works
Zola, S. M., & Squire, L. R. (2001) · Hippocampus · doi:10.1002/hipo.1027 · Cited by 90 · see citing works
Self-citationDifferential involvement of amygdala and hippocampus in responding to novel objects and contexts.
Moses, S. N., Sutherland, R., & McDonald, R. (2002) · Brain Research Bulletin · doi:10.1016/s0361-9230(02)00820-1 · Cited by 53 · see citing works
Effects of hippocampal lesions on patterned motor learning in the rat
Gould, T. J., Rowe, W. B., Heman, K. L., Mesches, M. H., Young, D. A., Rose, G. M., & Bickford, P. C. (2002) · Brain Research Bulletin · doi:10.1016/s0361-9230(02)00832-8 · Cited by 48 · 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
Episodic memory, semantic memory, and amnesia
Squire, L. R., & Zola, S. M. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1998)8:3
Flagged first, then by citations
Research works printed but not linked: 37
- [1]Squire, L. R. (1992) Psychol. Rev. 99, 195-231. [DOI] [PubMed] [Google Scholar]
- [3]Suzuki, W. A. & Eichenbaum, H. (2000) Ann. N.Y. Acad. Sci. 911, 175-191. [DOI] [PubMed] [Google Scholar]
- [4]Squire, L. R., Stark, C. E. L. & Clark, R. E. (2004) Annu. Rev. Neurosci. 27, 279-306. [DOI] [PubMed] [Google Scholar]
- [5]Fujimichi, R., Naya, Y. & Miyashita, Y. in Cognitive Neurosciences III, ed. Gazzaniga, M. S. (MIT Press, Cambridge, MA), in press.
- [6]Lavenex, P. & Amaral, D. G. (2000) Hippocampus 10, 420-430. [DOI] [PubMed] [Google Scholar]
- [8]Tulving, E. & Markowitsch, H. J. (1998) Hippocampus 8, 198-204. [DOI] [PubMed] [Google Scholar]
- [9]Brown, M. W. & Aggleton, J. P. (2001) Nat. Rev. Neurosci. 2, 51-61. [DOI] [PubMed] [Google Scholar]
- [10]Manns, J. R., Hopkins, R. O., Reed, J. M., Kitchener, E. G. & Squire, L. R. (2003) Neuron 37, 171-180. [DOI] [PubMed] [Google Scholar]
- [11]Beason-Held, L. L., Rosene, D. L., Killiany, R. J. & Moss, M. B. (1999) Hippocampus 9, 562-574. [DOI] [PubMed] [Google Scholar]
- [12]Zola, S. M., Squire, L. R., Teng, E., Stefanacci, L., Buffalo, E. A. & Clark, R. E. (2000) J. Neurosci. 20, 451-463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [13]Nemanic, S., Alvarado, M. C. & Bachevalier, J. (2004) J. Neurosci. 24, 2013-2026. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [14]Clark, R. E., Zola, S. M. & Squire, L. R. (2000) J. Neurosci. 20, 8853-8860. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [15]Clark, R. E., West, A. N., Zola, S. M. & Squire, L. R. (2001) Hippocampus 11, 176-186. [DOI] [PubMed] [Google Scholar]
- [16]Gould, T. J., Rowe, W. B., Heman, K. L., Mesches, M. H., Young, D. A., Rose, G. M. & Bickford, P. C. (2002) Brain Res. Bull. 58, 581-586. [DOI] [PubMed] [Google Scholar]
- [17]Prusky, G., Douglas, R., Nelson, L., Shabanpoor, A. & Sutherland, R. (2004) Proc. Natl. Acad. Sci. USA 101, 5064-5068. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [18]Holdstock, J. S., Mayes, A. R., Roberts, N., Cezayirli, E., Isaac, C. L., O'Reilly, R. C. & Norman, K. A. (2002) Hippocampus 12, 341-351. [DOI] [PubMed] [Google Scholar]
- [19]Murray, E. A. & Mishkin, M. (1998) J. Neurosci. 18, 6568-6582. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [20]Mumby, D. G. (2001) Behav. Brain Res. 127, 159-181. [DOI] [PubMed] [Google Scholar]
- [21]Winters, B. D., Forwood, S. E., Cowell, R. A., Saksida, L. M. & Bussey, T. J. (2004) J. Neurosci. 24, 5901-5908. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [22]Moser, E., Moser, M.-B. & Andersen, P. (1993) J. Neurosci. 13, 3916-3925. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [23]Moser, M.-B., Moser, E., Forrest, E., Andersen, P. & Morris, R. G. M. (1995) Proc. Natl. Acad. Sci. USA 92, 9697-9701. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [24]Duva, C. A., Floresco, S. B., Wunderlich, G. R., Lao, T. L., Pinel, J. P. J. & Phillips, A. G. (1997) Behav. Neurosci. 111, 1184-1196. [DOI] [PubMed] [Google Scholar]
- [25]Baxter, M. G. & Murray, E. A. (2001) Hippocampus 11, 61-71. [DOI] [PubMed] [Google Scholar]
- [26]Zola, S. & Squire, L. R. (2001) Hippocampus 11, 92-98. [DOI] [PubMed] [Google Scholar]
- [27]Bannerman, D. M., Yee, B. K., Good, M. A., Heupel, M. J., Iversen, S. D. & Rawlins, J. N. (1999) Behav. Neurosci. 11, 1170-1188. [DOI] [PubMed] [Google Scholar]
- [28]Prusky, G., Douglas, R., Nelson, L., Shabanpoor, A. & Sutherland, R. (2004) Proc. Natl. Acad. Sci. USA 101, 5064-5068. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [29]Pothuizen, H. H., Zhang, W. N., Jongen-Relo, A. L., Feldon, J. & Yee, B. K. (2004) Eur. J. Neurosci. 19, 705-712. [DOI] [PubMed] [Google Scholar]
- [30]de Hoz, L., Knox, J. & Morris, R. G. M. (2003) Hippocampus 13, 587-603. [DOI] [PubMed] [Google Scholar]
- [31]Dolorfo, C. L. & Amaral, D. G. (1998) J. Comp. Neurol. 398, 25-48. [PubMed] [Google Scholar]
- [32]Handelmann, G. E. & Olton, D. S. (1981) Brain Res. 217, 41-58. [DOI] [PubMed] [Google Scholar]
- [33]Brun, V. H., Otnass, M. K., Mollen, S., Steffenach, H.-A., Witter, M. P., Moser, M.-B. & Moser, E. I. (2002) Science 296, 2243-2246. [DOI] [PubMed] [Google Scholar]
- [34]Steffenach, H.-A., Sloviter, R. S., Moser, E. I. & Moser, M.-B. (2002) Proc. Natl. Acad. Sci. USA 99, 3194-3198. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [35]Lee, I. & Kesner, R. P. (2004) Hippocampus 14, 66-76. [DOI] [PubMed] [Google Scholar]
- [36]Moses, S. N., Sutherland, R. J. & MacDonald, R. J. (2002) Brain Res. Bull. 58, 517-527. [DOI] [PubMed] [Google Scholar]
- [37]Mumby, D. G., Gaskin, S., Glenn, M. J., Schramek, T. E. & Lehmann, H. (2002) Learn. Mem. 9, 49-57. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [38]Gaskin, S., Tremblay, A. & Mumby, D. G. (2003) Hippocampus 13, 962-969. [DOI] [PubMed] [Google Scholar]
- [39]Baker, K. B. & Kim, J. J. (2002) Learn. Mem. 9, 58-65. [DOI] [PMC free article] [PubMed] [Google Scholar]
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Eichenbaum, H., Yonelinas, A. P., & Ranganath, C. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.30.051606.094328 · Cited by 2,580 · see citing works
Recognition memory and the medial temporal lobe: a new perspective
Squire, L. R., Wixted, J. T., & Clark, R. E. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2154 · Cited by 1,028 · see citing works
Self-citationA novel pathway regulates memory and plasticity via SIRT1 and miR-134
Gao, J., Wang, W.-Y., Mao, Y.-W., Gräff, J., Guan, J.-S., Pan, L., Mak, G., Kim, D., Su, S. C., & Tsai, L.-H. (2010) · Nature · doi:10.1038/nature09271 · Cited by 975 · see citing works
Arc/Arg3.1 Is Essential for the Consolidation of Synaptic Plasticity and Memories
Plath, N., Ohana, O., Dammermann, B., Errington, M. L., Schmitz, D., Gross, C., Mao, X., Engelsberg, A., Mahlke, C., Welzl, H., et al. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.024 · Cited by 827 · see citing works
The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents
Dere, E., Huston, J. P., & Silva, M. A. D. S. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.01.005 · Cited by 669 · see citing works
Jessberger, S., Clark, R. E., Broadbent, N. J., Clemenson, G. D., Consiglio, A., Lie, D. C., Squire, L. R., & Gage, F. H. (2009) · Learning & Memory · doi:10.1101/lm.1172609 · Cited by 654 · see citing works
Self-citationObject recognition memory: Neurobiological mechanisms of encoding, consolidation and retrieval
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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
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Wang, S., & Morris, R. (2009) · Annual Review of Psychology · doi:10.1146/annurev.psych.093008.100523 · Cited by 536 · see citing works
Bruel‐Jungerman, E., Laroche, S., & Rampon, C. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03875.x · Cited by 505 · see citing works
Roozendaal, B., Okuda, S., van der Zee, E. A., & McGaugh, J. L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601874103 · Cited by 499 · see citing works
Mechanisms of late-onset cognitive decline after early-life stress
Brunson, K. L., Kramár, E., Lin, B., Chen, Y., Colgin, L. L., Yanagihara, T. K., Lynch, G., & Baram, T. Z. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2281-05.2005 · Cited by 479 · see citing works
Visual Perception and Memory: A New View of Medial Temporal Lobe Function in Primates and Rodents
Murray, E. A., Bussey, T. J., & Saksida, L. M. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.113046 · Cited by 436 · see citing works
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O'Doherty, A., Ruf, S., Mulligan, C., Hildreth, V., Errington, M. L., Cooke, S., Sesay, A., Modino, S., Vanes, L., Hernandez, D., et al. (2005) · Science · doi:10.1126/science.1114535 · Cited by 434 · see citing works
Ivy, A. S., Rex, C. S., Chen, Y., Dubé, C., Maras, P. M., Grigoriadis, D. E., Gall, C. M., Lynch, G., & Baram, T. Z. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1784-10.2010 · Cited by 402 · see citing works
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Zhang, G., & Stackman, R. W. (2015) · Frontiers in Pharmacology · doi:10.3389/fphar.2015.00225 · Cited by 386 · see citing works
Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling
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Quinn, H. R., Matsumoto, I., Callaghan, P. D., Long, L. E., Arnold, J. C., Gunasekaran, N., Thompson, M. R., Dawson, B., Mallet, P. E., Kashem, M. A., et al. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301475 · Cited by 293 · see citing works
Moseley, A. E., Williams, M. T., Schaefer, T. L., Bohanan, C. S., Neumann, J. C., Behbehani, M. M., Vorhees, C. V., & Lingrel, J. B. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4464-06.2007 · Cited by 288 · see citing works
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Shi, H., Yu, Y., Lin, D., Zheng, P., Zhang, P., Hu, M., Wang, Q., Pan, W., Yang, X., Hu, T., et al. (2020) · Microbiome · doi:10.1186/s40168-020-00920-y · Cited by 264 · see citing works
Dinel, A., André, C., Aubert, A., Ferreira, G., Layé, S., & Castanon, N. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024325 · Cited by 264 · see citing works
Simmons, D. A., Rex, C. S., Palmer, L. C., Pandyarajan, V., Fedulov, V., Gall, C. M., & LYNCH, G. S. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811228106 · Cited by 261 · see citing works
Wallace, M. E., Luine, V. N., Arellanos, A., & Frankfurt, M. (2006) · Brain Research · doi:10.1016/j.brainres.2006.07.064 · Cited by 255 · see citing works
Langston, R. F., & Wood, E. R. (2009) · Hippocampus · doi:10.1002/hipo.20714 · Cited by 244 · see citing works
Barrett, R. M., & Wood, M. A. (2008) · Learning & Memory · doi:10.1101/lm.917508 · Cited by 239 · see citing works
Escribano, L., Simón, A.-M., Gimeno, E., Cuadrado-Tejedor, M., López de Maturana, R., García-Osta, A., Ricobaraza, A., Pérez-Mediavilla, A., Del Río, J., & Frechilla, D. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.32 · Cited by 235 · see citing works
Hippocampal-dependent learning requires a functional circadian system
Ruby, N. F., Hwang, C. E., Wessells, C., Fernandez, F., Zhang, P., Sapolsky, R., & Heller, H. C. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808259105 · Cited by 234 · see citing works
Interactions between estradiol, BDNF and dendritic spines in promoting memory
Luine, V. N., & Frankfurt, M. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.10.019 · Cited by 234 · see citing works
Exposure to polystyrene microplastics impairs hippocampus-dependent learning and memory in mice
Lee, C., Hsu, L., Wu, I.-L., Wang, Y., Chen, W.-C., Liu, Y., Yang, L.-T., Tan, C.-L., Luo, Y.-H., Wang, C.-C., et al. (2022) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2022.128431 · Cited by 226 · see citing works
Transgenic miR132 Alters Neuronal Spine Density and Impairs Novel Object Recognition Memory
Hansen, K. F., Sakamoto, K., Wayman, G. A., Impey, S., & Obrietan, K. H. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015497 · Cited by 225 · see citing works
Spatial memory: Theoretical basis and comparative review on experimental methods in rodents
Paul, C.-M., Giòrdano, M., & Santamaria, A. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.05.022 · Cited by 223 · see citing works
Ali, T., & Kim, M. O. (2015) · Journal of Pineal Research · doi:10.1111/jpi.12238 · Cited by 222 · see citing works
Post-training reversible inactivation of the hippocampus enhances novel object recognition memory
Oliveira, A. M. M., Hawk, J. D., Abel, T., & Havekes, R. (2010) · Learning & Memory · doi:10.1101/lm.1625310 · Cited by 222 · see citing works
The Human Hippocampus: Cognitive Maps or Relational Memory?
Kumaran, D., & Maguire, E. A. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1103-05.2005 · Cited by 218 · see citing works
Hippocampal neuroplasticity induced by early-life stress: Functional and molecular aspects
Fenoglio, K. A., Brunson, K. L., & Baram, T. (2006) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2006.02.001 · Cited by 215 · see citing works
Bagot, R. C., van Hasselt, F. N., Champagne, D. L., Meaney, M. J., Krugers, H. J., & Joëls, M. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.03.004 · Cited by 216 · see citing works
Pascual, M., Baliño, P., Alfonso-Loeches, S., Aragón, C. M. G., & Guerri, C. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2011.02.012 · Cited by 213 · see citing works
Balderas, I., Rodriguez-Ortiz, C. J., Salgado-Tonda, P., Chavez-Hurtado, J., McGaugh, J. L., & Bermudez-Rattoni, F. (2008) · Learning & Memory · doi:10.1101/lm.1028008 · Cited by 213 · see citing works
Eichenbaum, H., & Lipton, P. A. (2008) · Hippocampus · doi:10.1002/hipo.20500 · Cited by 209 · see citing works
Haettig, J., Stefanko, D. P., Multani, M. L., Figueroa, D. X., McQuown, S. C., & Wood, M. A. (2011) · Learning & Memory · doi:10.1101/lm.1986911 · Cited by 211 · 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
Self-citationHales, J. B., Schlesiger, M. I., Leutgeb, J. K., Squire, L. R., Leutgeb, S., & Clark, R. E. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.10.009 · Cited by 204 · see citing works
Self-citationHernandez, C. M., Kayed, R., Zheng, H., Sweatt, J. D., & Dineley, K. T. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5038-09.2010 · Cited by 204 · see citing works
“The time spent exploring a novel object versus a familiar object is a measure of attention and nonspatial declarative memory (Broadbent et al., 2004).”
BackgroundVanillic acid attenuates Aβ1-42-induced oxidative stress and cognitive impairment in mice
Amin, F. U., Shah, S. A., & Kim, M. O. (2017) · Scientific Reports · doi:10.1038/srep40753 · Cited by 205 · see citing works
Protein Phosphatase 1 Regulates the Histone Code for Long-Term Memory
Koshibu, K., Gräff, J., Beullens, M., Heitz, F. D., Berchtold, D., Russig, H. D., Farinelli, M., Bollen, M., & Mansuy, I. M. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3610-09.2009 · Cited by 202 · see citing works
Steullet, P., Cabungcal, J.-H., Kulak, A., Kraftsik, R., Chen, Y., Dalton, T. P., Cuenod, M., & Do, K. Q. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.3857-09.2010 · Cited by 202 · see citing works
The case for episodic memory in animals
Dere, E., KARTTEKE, E., Huston, J. P., & DESOUZASILVA, M. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.09.005 · Cited by 202 · see citing works
Muhammad, T., Ali, T., Ikram, M. A., Khan, A., Alam, S. I., & Kim, M. O. (2018) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-018-9824-3 · Cited by 201 · see citing works
Behavioral and anatomical abnormalities in Mecp2 mutant mice: A model for Rett syndrome
Stearns, N. A., Schaevitz, L. R., Bowling, H. L., Nag, N., Berger, U. V., & Berger-Sweeney, J. E. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.02.009 · Cited by 199 · see citing works
Focal Lesions of Human Hippocampal CA1 Neurons in Transient Global Amnesia Impair Place Memory
Bartsch, T., Schönfeld, R., Müller, F. U., Alfke, K., Leplow, B., Aldenhoff, J. B., Deuschl, G., & Koch, J. M. (2010) · Science · doi:10.1126/science.1188160 · Cited by 194 · see citing works
From Rapid Place Learning to Behavioral Performance: A Key Role for the Intermediate Hippocampus
Bast, T., Wilson, I. A., Witter, M. P., & Morris, R. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000089 · Cited by 189 · see citing works
Kanoski, S. E., & Davidson, T. L. (2010) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/a0017228 · Cited by 185 · see citing works
Andonegui, G., Zelinski, E. L., Schubert, C. L., Knight, D., Craig, L. A., Winston, B. W., Spanswick, S. C., Petri, B., Jenne, C. N., Sutherland, J., et al. (2018) · JCI Insight · doi:10.1172/jci.insight.99364 · Cited by 177 · see citing works
Pattern Separation Deficits May Contribute to Age-Associated Recognition Impairments
Burke, S., Wallace, J. L., Nematollahi, S., Uprety, A., & Barnes, C. A. (2010) · Behavioral Neuroscience · doi:10.1037/a0020893 · Cited by 174 · see citing works
Dong, S., Zeng, Q., Mitchell, E. S., Xiu, J., Duan, Y., Li, C., Tiwari, J. K., Hu, Y., Cao, X., & Zhao, Z. Y. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031211 · Cited by 179 · see citing works
Bouter, Y., Dietrich, K., Wittnam, J. L., Rezaei-Ghaleh, N., Pillot, T., Papot-Couturier, S., Lefebvre, T., Sprenger, F., Wirths, O., Zweckstetter, M., et al. (2013) · Acta Neuropathologica · doi:10.1007/s00401-013-1129-2 · Cited by 175 · see citing works
Stress and adolescent hippocampal neurogenesis: diet and exercise as cognitive modulators
Hueston, C. M., Cryan, J. F., & Nolan, Y. M. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.48 · Cited by 171 · see citing works
Tordera, R. M., Totterdell, S., Wojcik, S. M., Brose, N., Elizalde, N., Lasheras, B., & del Rı́o, J. A. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05259.x · Cited by 169 · see citing works
Cognitive-vestibular interactions: A review of patient difficulties and possible mechanisms
Hanes, D. A., & McCollum, G. (2006) · Journal of Vestibular Research · doi:10.3233/ves-2006-16301 · Cited by 169 · see citing works
Exercise enhances hippocampal‐dependent learning in the rat: Evidence for a BDNF‐related mechanism
Griffin, É. W., Bechara, R. G., Birch, A. M., & Kelly, A. M. (2009) · Hippocampus · doi:10.1002/hipo.20631 · Cited by 168 · see citing works
Inagaki, T., Gautreaux, C., & Luine, V. N. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.05.013 · Cited by 164 · see citing works
Thanopoulou, K., Fragkouli, A., Stylianopoulou, F., & Georgopoulos, S. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005888107 · Cited by 161 · see citing works
Phan, A., Lancaster, K. E., Armstrong, J. N., MacLusky, N. J., & Choleris, E. (2011) · Endocrinology · doi:10.1210/en.2010-1273 · Cited by 160 · see citing works
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
Bast, T. (2007) · Reviews in the Neurosciences · doi:10.1515/revneuro.2007.18.3-4.253 · Cited by 149 · see citing works
Meyer‐Lindenberg, A. (2005) · Journal of Clinical Investigation · doi:10.1172/jci24892 · Cited by 153 · see citing works
Neuronal circuitry for recognition memory of object and place in rodent models
Chao, O. Y.-H., Nikolaus, S., Yang, Y., & Huston, J. P. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104855 · Cited by 157 · see citing works
Jacome, L. F., Gautreaux, C., Inagaki, T., Mohan, G., Alves, S. E., Lubbers, L. S., & Luine, V. N. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.08.016 · Cited by 150 · see citing works
Vasopressin 1b Receptor Knock-Out Impairs Memory for Temporal Order
DeVito, L. M., Konigsberg, R., Lykken, C., Sauvage, M., Young, W. S., & Eichenbaum, H. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5488-08.2009 · Cited by 147 · see citing works
Vuong, B., Odero, G., Rozbacher, S., Stevenson, M., Kereliuk, S. M., Pereira, T. J., Dolinsky, V. W., & Kauppinen, T. M. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0859-9 · Cited by 147 · see citing works
Hippocampal adult neurogenesis: Its regulation and potential role in spatial learning and memory
Lieberwirth, C., Pan, Y., Liu, Y., Zhang, Z., & Wang, Z. (2016) · Brain Research · doi:10.1016/j.brainres.2016.05.015 · Cited by 144 · see citing works
Szyndler, J., Piechal, A., Blecharz-Klin, K., Skórzewska, A., Maciejak, P., Walkowiak, J., Turzyńska, D., Bidziński, A., Płaźnik, A., & Widy-Tyszkiewicz, E. (2006) · PubMed · Cited by 147 · see citing works
Ahn, H. J., Hernandez, C. M., Levenson, J. M., Lubin, F. D., Liou, H.-C., & Sweatt, J. D. (2008) · Learning & Memory · doi:10.1101/lm.866408 · Cited by 144 · see citing works
Ali, T., Yoon, G. H., Shah, S. A., Lee, H. Y., & Kim, M. O. (2015) · Scientific Reports · doi:10.1038/srep11708 · Cited by 146 · see citing works
Low Doses of 17β-Estradiol Rapidly Improve Learning and Increase Hippocampal Dendritic Spines
Phan, A., Gabor, C., Favaro, K. J., Kaschack, S., Armstrong, J. N., MacLusky, N. J., & Choleris, E. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.82 · Cited by 146 · see citing works
NLRP3 inflammasome in ischemic stroke: As possible therapeutic target
Alishahi, M., Farzaneh, M., Ghaedrahmati, F., Nejabatdoust, A., Sarkaki, A., & Khoshnam, S. E. (2019) · International Journal of Stroke · doi:10.1177/1747493019841242 · Cited by 142 · see citing works
Jenrow, K. A., Brown, S. L., Lapanowski, K., Naei, H., Kolozsvary, A. J. J., & Kim, J. H. (2013) · Radiation Research · doi:10.1667/rr3026.1 · Cited by 141 · see citing works
Ainge, J. A., Heron-Maxwell, C., Theofilas, P., Wright, P., de Hoz, L., & Wood, E. R. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.09.005 · Cited by 140 · see citing works
Object memory and perception in the medial temporal lobe: an alternative approach
Bussey, T. J., & Saksida, L. M. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.10.014 · Cited by 136 · see citing works
Behavioral Tagging: A Translation of the Synaptic Tagging and Capture Hypothesis
Moncada, D., Ballarini, F., & Viola, H. (2015) · Neural Plasticity · doi:10.1155/2015/650780 · Cited by 134 · see citing works
Regulation of object recognition and object placement by ovarian sex steroid hormones
Tuscher, J. J., Fortress, A. M., Kim, J., & Frick, K. M. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.08.001 · Cited by 134 · see citing works
Meck, W. H. (2008) · Frontiers in Integrative Neuroscience · doi:10.3389/neuro.07.007.2007 · Cited by 133 · see citing works
Object familiarization and novel-object preference in rats
Gaskin, S., Tardif, M., Cole, E., Piterkin, P., Kayello, L., & Mumby, D. G. (2010) · Behavioural Processes · doi:10.1016/j.beproc.2009.10.003 · Cited by 133 · see citing works
Lukas, M., & Neumann, I. D. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.08.016 · Cited by 133 · see citing works
Positive reward prediction errors during decision-making strengthen memory encoding
Jang, A. I., Nassar, M. R., Dillon, D. G., & Frank, M. J. (2019) · Nature Human Behaviour · doi:10.1038/s41562-019-0597-3 · Cited by 129 · see citing works
Oral supplementation of 2′-fucosyllactose during lactation improves memory and learning in rats
Oliveros, E., Ramirez, M., Vázquez, E., Barranco, A., Gruart, A., Delgado-Garcia, J. M., Buck, R. H., Rueda, R., & Martín, M. J. (2016) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2015.12.014 · Cited by 131 · see citing works
Expression of HIV-Tat protein is associated with learning and memory deficits in the mouse
Carey, A. N., Sypek, E. I., Singh, H. D., Kaufman, M. J., & McLaughlin, J. P. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.12.019 · Cited by 130 · see citing works
Global Cerebral Ischemia: Synaptic and Cognitive Dysfunction
Neumann, J. T., Cohan, C. H., Dave, K. R., Wright, C. B., & Pérez‐Pinzón, M. A. (2012) · Current Drug Targets · doi:10.2174/138945013804806514 · Cited by 135 · see citing works
Riga, D., Kramvis, I., Koskinen, M. K., van Bokhoven, P., van der Harst, J. E., Heistek, T. S., Jaap Timmerman, A., van Nierop, P., van der Schors, R. C., Pieneman, A. W., et al. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aai8753 · Cited by 128 · see citing works
Bröker‐Lai, J., Kollewe, A., Schindeldecker, B., Pohle, J., Nguyễn, V., Mathar, I., Guzman, R. E., Schwarz, Y. N., Lai, A., Weißgerber, P., et al. (2017) · The EMBO Journal · doi:10.15252/embj.201696369 · Cited by 126 · see citing works
Qiu, S., Palavicini, J. P., Wang, J., Gonzalez, N. S., He, S., Dustin, E., Zou, C., Ding, L., Bhattacharjee, A., Skike, C. E. V., et al. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00488-7 · Cited by 126 · see citing works
Neuroprotection by Acetyl-L-Carnitine after Traumatic Injury to the Immature Rat Brain
Scafidi, S., Racz, J. L., Hazelton, J. L., McKenna, M. C., & Fiskum, G. M. (2010) · Developmental Neuroscience · doi:10.1159/000323178 · Cited by 125 · see citing works
- Authors
- Broadbent, N. J., Squire, L. R., & Clark, R. E.
- Affiliations
- University of California San Diego (US)
- Corresponding author
- Clark, Robert E.
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2004-09-27
- Volume
- 101
- Issue
- 40
- Pages
- 14515-14520
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC521976
- OpenAlex
- W2038813826
- Cited by
- 985
- References
- 37
- Citations by year
- 2026: 25 · 2025: 26 · 2024: 35 · 2023: 40 · 2022: 59 · 2021: 51 · 2020: 55 · 2019: 53 · 2018: 56 · 2017: 57 · 2016: 51 · 2015: 51 · 2014: 52 · 2013: 48 · 2012: 63
- FWCI
- 14.60
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- U.S. Department of Veterans Affairs
- James S. McDonnell Foundation
- National Alliance for Research on Schizophrenia and Depression
- National Institute on Aging (P50AG005131, P50-AG05131)
- National Institute of Mental Health (P50 AG05131, AG05131)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
- Keywords
- spatial memory, recognition memory, hippocampus, hippocampal lesions, lesion size, dorsal hippocampus, ventral hippocampus, object recognition, rats
- MeSH terms
- Animals, Hippocampus, Male, Memory, Spatial Behavior, Rats, Long-Evans, Recognition, Psychology, Rats
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