Retrograde and anterograde object recognition in rats with hippocampal lesions
Abstract
Retrograde and anterograde object-recognition memory was assessed in rats with cytotoxic lesions of the hippocampal formation (HPC), using a paradigm based on the natural tendency of rats to spend more time exploring novel objects than familiar objects. The rats were allowed to explore a sample object for 5 min/day on 5 consecutive days, either 5 weeks or 1 week before surgery. After surgery, retrograde recognition was assessed by comparing the amount of time spent exploring the sample versus a novel object in a free-choice situation. Control rats spent more time exploring the novel object than the sample objects from both presurgery time periods, whereas rats with HPC lesions did not discriminate between the novel objects and sample objects from either presurgery time period. Despite their deficits on the retrograde recognition test, the rats with HPC lesions performed like control rats on anterograde recognition tests, displaying a strong exploratory preference for novel objects over sample objects, with retention delays of either 15 min or 24 h. The findings suggest that extrahippocampal circuitry is capable of supporting object recognition, but only if the HPC does not participate in encoding the original encounter with the object.
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Long-term NOP impairment was consistently found when the hippocampus was damaged after the learning session.
“Nevertheless, long-term NOP impairment was consistently found when the hippocampus was damaged after the learning session (Broadbent et al., 2010; Gaskin et al., 2003; Haijima and Ichitani, 2012).”
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., 2003
Animals with hippocampus lesion, after being submitted to repeated exposure of the sample trial in the NOP test, exhibited impaired recognition memory when tested within 5, but not 8, weeks after the lesions.
“In studies investigating retrograde memory, animals with hippocampus lesion, after being submitted to repeated exposure of the sample trial in the NOP test, exhibited impaired recognition memory when tested within 5, but not 8, weeks after the lesions (Broadbent et al., 2010; Gaskin et al., 2003; Haijima and Ichitani, 2012).”
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., 2003
Cites
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
McClelland, J. L., McNaughton, B. L., & O'Reilly, R. C. (1995) · Psychological Review · doi:10.1037/0033-295x.102.3.419 · Cited by 5,256 · see citing works
A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data
Ennaceur, A., & Delacour, J. (1988) · Behavioural Brain Research · doi:10.1016/0166-4328(88)90157-x · Cited by 3,223 · 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
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
Episodic memory, amnesia, and the hippocampal–anterior thalamic axis
Aggleton, J. P., & Brown, M. W. (1999) · Behavioral and Brain Sciences · doi:10.1017/s0140525x99002034 · Cited by 1,879 · see citing works
A cortical–hippocampal system for declarative memory
Eichenbaum, H. (2000) · Nature reviews. Neuroscience · doi:10.1038/35036213 · Cited by 1,725 · see citing works
Recognition 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
Meunier, M., Bachevalier, J., Mishkin, M., & Murray, E. A. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-12-05418.1993 · Cited by 900 · 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
Zola-Morgan, S. M., Squire, L., Amaral, D., & Suzuki, W. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-12-04355.1989 · Cited by 766 · 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
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
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
Ennaceur, A., Neave, N., & Aggleton, J. P. (1997) · Experimental Brain Research · doi:10.1007/pl00005603 · Cited by 670 · see citing works
Dix, S. L., & Aggleton, J. P. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00079-5 · Cited by 598 · see citing works
Phillips, R. G., & LeDoux, J. E. (1994) · Learning & Memory · doi:10.1101/lm.1.1.34 · Cited by 528 · 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
Murray, E. A., & Mishkin, M. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-16-06568.1998 · Cited by 434 · see citing works
Rhinal cortex lesions and object recognition in rats.
Mumby, D. G., & Pinel, J. P. J. (1994) · Behavioral Neuroscience · doi:10.1037//0735-7044.108.1.11 · Cited by 412 · see citing works
Self-citationDamage limited to the hippocampal region produces long-lasting memory impairment in monkeys
Alvarez, P., Zola-Morgan, S. M., & Squire, L. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-05-03796.1995 · Cited by 376 · see citing works
Context and conditioning: A place for space
Nadel, L., & Willner, J. (1980) · Physiological Psychology · doi:10.3758/bf03332853 · Cited by 373 · 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
Self-citationAnterograde 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
Ennaceur, A., Neave, N., & Aggleton, J. P. (1996) · Behavioural Brain Research · doi:10.1016/0166-4328(96)00006-x · Cited by 351 · see citing works
Rhinal cortex lesions and object recognition in rats.
Mumby, D. G., & Pinel, J. P. J. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.1.11 · Cited by 348 · see citing works
Self-citationAmnesia and recognition memory: A re-analysis of psychometric data
Aggleton, J. P., & Shaw, C. (1996) · Neuropsychologia · doi:10.1016/0028-3932(95)00150-6 · Cited by 323 · see citing works
Gaffan, D., & Murray, E. A. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.1.30 · Cited by 265 · see citing works
Conditioning and contextual retrieval in hippocampal rats.
Good, M. A., & Honey, R. C. (1991) · Behavioral Neuroscience · doi:10.1037//0735-7044.105.4.499 · Cited by 246 · see citing works
Gaffan, D., & Murray, E. A. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.1.30 · Cited by 217 · see citing works
Conditioning and contextual retrieval in hippocampal rats.
Good, M. A., & Honey, R. C. (1991) · Behavioral Neuroscience · doi:10.1037/0735-7044.105.4.499 · Cited by 202 · 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
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
Self-citationAggleton, J. P., Keen, S., Warburton, E. C., & Bussey, T. J. (1997) · Brain Research Bulletin · doi:10.1016/s0361-9230(97)00007-5 · Cited by 168 · see citing works
Mumby, D. G. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00097-2 · Cited by 145 · see citing works
Self-citationWarburton, E. C., & Aggleton, J. P. (1998) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00047-3 · Cited by 127 · see citing works
Spontaneous recognition of object configurations in rats: effects of fornix lesions
Ennaceur, A., & Aggleton, J. P. (1994) · Experimental Brain Research · doi:10.1007/bf00227281 · Cited by 121 · see citing works
Mumby, D. G., Glenn, M. J., Nesbitt, C., & Kyriazis, D. A. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00444-2 · Cited by 120 · see citing works
Self-citationWiig, K. A., & Bilkey, D. K. (1995) · Behavioral Neuroscience · doi:10.1037//0735-7044.109.4.620 · Cited by 91 · see citing works
Wiig, K. A., & Bilkey, D. K. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.4.620 · Cited by 71 · see citing works
Spatial organization of episodic memory
Gaffan, D. (1991) · Hippocampus · doi:10.1002/hipo.450010311 · Cited by 62 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Squire, 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
The organization of recent and remote memories
Frankland, P. W., & Bontempi, B. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1607 · Cited by 2,138 · see citing works
Spatial memory, recognition memory, and the hippocampus
Broadbent, N. J., Squire, L. R., & Clark, R. E. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406344101 · Cited by 985 · 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
Self-citationWinocur, G., Moscovitch, M., & Bontempi, B. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.04.016 · Cited by 486 · see citing works
On the delay-dependent involvement of the hippocampus in object recognition memory
HAMMOND, R. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.03.005 · Cited by 476 · see citing works
The rodent hippocampus is essential for nonspatial object memory
Cohen, S. J., Munchow, A. H., Rios, L. M., Zhang, G., Ásgeirsdóttir, H. N., & Stackman, R. W. (2013) · Current Biology · doi:10.1016/j.cub.2013.07.002 · Cited by 325 · see citing works
Rossato, J. I., Bevilaqua, L. R. M., Myskiw, J. C., Medina, J. H., Izquierdo, I., & Cammarota, M. (2007) · Learning & Memory · doi:10.1101/lm.422607 · Cited by 282 · 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
Time-dependent involvement of the dorsal hippocampus in trace fear conditioning in mice
Misane, I., Tovote, P., Meyer, M., Spiess, J., Ögren, S. O., & Stiedl, O. (2005) · Hippocampus · doi:10.1002/hipo.20067 · Cited by 183 · 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
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 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
Self-citationDo hippocampal pyramidal cells respond to nonspatial stimuli?
O’Keefe, J., & Krupic, J. (2021) · Physiological Reviews · doi:10.1152/physrev.00014.2020 · Cited by 93 · see citing works
Lenck-Santini, P.-P., Rivard, B., Muller, R. U., & Poucet, B. (2005) · Hippocampus · doi:10.1002/hipo.20060 · Cited by 81 · see citing works
Hardt, O., Migues, P. V., Hastings, M., Wong, J., & Nader, K. (2010) · Hippocampus · doi:10.1002/hipo.20708 · Cited by 79 · see citing works
New behavioral protocols to extend our knowledge of rodent object recognition memory
Albasser, M. M., Chapman, R. J., Amin, E., Iordanova, M. D., Vann, S. D., & Aggleton, J. P. (2010) · Learning & Memory · doi:10.1101/lm.1879610 · Cited by 79 · see citing works
Jobim, P. F. C., Pedroso, T. R., Werenicz, A., Christoff, R. R., Maurmann, N., Reolon, G. K., Schröder, N., & Roesler, R. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.12.004 · Cited by 68 · see citing works
A limited role for the hippocampus in the modulation of novel-object preference by contextual cues
Piterkin, P., Cole, E., Cossette, M.-P., Gaskin, S., & Mumby, D. G. (2008) · Learning & Memory · doi:10.1101/lm.1035508 · Cited by 65 · see citing works
Self-citationStackman, R. W., Cohen, S. J., Lora, J. C., & Rios, L. M. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.06.016 · Cited by 66 · see citing works
Beer, Z., Chwiesko, C., & Sauvage, M. M. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.03.001 · Cited by 59 · see citing works
Nicotinic receptor activation in perirhinal cortex and hippocampus enhances object memory in rats
Melichercik, A. M., Elliott, K. S., Bianchi, C., Ernst, S. M., & Winters, B. D. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.01.008 · Cited by 54 · 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
Recent and remote retrograde memory deficit in rats with medial entorhinal cortex lesions
Hales, J. B., Vincze, J. L., Reitz, N. T., Ocampo, A. C., Leutgeb, S., & Clark, R. E. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.07.013 · Cited by 33 · see citing works
Iwamura, E., Yamada, K., & Ichitani, Y. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.03.048 · Cited by 20 · see citing works
Gaskin, S., Tardif, M., & Mumby, D. G. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.06.001 · Cited by 11 · see citing works
Hales, J. B., Ocampo, A. C., Broadbent, N. J., & Clark, R. E. (2015) · Neural Plasticity · doi:10.1155/2015/847136 · Cited by 7 · see citing works
- Authors
- Gaskin, S., Tremblay, A., & Mumby, D. G.
- Affiliations
- Concordia University (CA)
- Corresponding author
- Mumby, Dave G.
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2003-01
- Volume
- 13
- Issue
- 8
- Pages
- 962-969
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- OpenAlex
- W2155791928
- Cited by
- 160
- References
- 42
- Citations by year
- 2026: 3 · 2025: 2 · 2023: 4 · 2022: 4 · 2021: 4 · 2020: 7 · 2019: 4 · 2018: 6 · 2017: 2 · 2016: 6 · 2015: 11 · 2014: 9 · 2013: 15 · 2012: 10
- FWCI
- 3.43
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- object recognition memory, retrograde amnesia, anterograde amnesia, hippocampal lesions, hippocampal formation, novel object recognition, memory encoding, rats
- MeSH terms
- Amnesia, Retrograde, Animals, Denervation, Disease Models, Animal, Hippocampus, Male, Memory, Neural Pathways, Pattern Recognition, Visual, Reaction Time, Time Factors, Rats, Long-Evans, Amnesia, Anterograde, Recognition, Psychology, Rats
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