Mapping parahippocampal systems for recognition and recency memory in the absence of the rat hippocampus
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The present study examined immediate-early gene expression in the perirhinal cortex of rats with hippocampal lesions. The goal was to test those models of recognition memory which assume that the perirhinal cortex can function independently of the hippocampus. The c-fos gene was targeted, as its expression in the perirhinal cortex is strongly associated with recognition memory. Four groups of rats were examined. Rats with hippocampal lesions and their surgical controls were given either a recognition memory task (novel vs. familiar objects) or a relative recency task (objects with differing degrees of familiarity). Perirhinal Fos expression in the hippocampal-lesioned groups correlated with both recognition and recency performance. The hippocampal lesions, however, had no apparent effect on overall levels of perirhinal or entorhinal cortex c-fos expression in response to novel objects, with only restricted effects being seen in the recency condition. Network analyses showed that whereas the patterns of parahippocampal interactions were differentially affected by novel or familiar objects, these correlated networks were not altered by hippocampal lesions. Additional analyses in control rats revealed two modes of correlated medial temporal activation. Novel stimuli recruited the pathway from the lateral entorhinal cortex (cortical layer II or III) to hippocampal field CA3, and thence to CA1. Familiar stimuli recruited the direct pathway from the lateral entorhinal cortex (principally layer III) to CA1. The present findings not only reveal the independence from the hippocampus of some perirhinal systems associated with recognition memory, but also show how novel stimuli engage hippocampal subfields in qualitatively different ways from familiar stimuli.
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The LEC-CA1 pathway is recruited for processing of exploration of familiar objects and object-recency, while the LEC-dentate gyrus-CA3 pathway is activated for processing of recognition of novel objects and object-recency.
“the LEC-CA1 pathway is recruited for the processing of exploration of familiar objects and of object-recency, while the pathway of LEC-dentate gyrus-CA3 is activated for the processing of recognition of novel objects and for object-recency”
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 Kinnavane et al., 2014
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Cites
Tabachnick, B. G., & Fidell, L. S. (1983) · Cited by 79,888 · see citing works
Baltosser, W. H., & Zar, J. H. (1996) · Ecology · doi:10.2307/2265725 · Cited by 35,166 · see citing works
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
Hu, L.-T., & Bentler, P. M. (1998) · Psychological Methods · doi:10.1037/1082-989x.3.4.424 · Cited by 12,298 · see citing works
The Nature of Recollection and Familiarity: A Review of 30 Years of Research
Yonelinas, A. P. (2002) · Journal of Memory and Language · doi:10.1006/jmla.2002.2864 · Cited by 3,840 · 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
The Medial Temporal Lobe and Recognition Memory
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
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
Self-citationBrain Maps: Structure of the Rat Brain
Swanson, L. W. (1992) · Medical Entomology and Zoology · Cited by 1,851 · see citing works
Brain maps: structure of the rat brain
Guillery, R. W. (1993) · Trends in Neurosciences · doi:10.1016/0166-2236(93)90187-q · Cited by 1,677 · 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
Self-citationNorman, K. A., & O'Reilly, R. C. (2003) · Psychological Review · doi:10.1037/0033-295x.110.4.611 · Cited by 1,312 · see citing works
Imaging recollection and familiarity in the medial temporal lobe: a three-component model
Diana, R. A., Yonelinas, A. P., & Ranganath, C. (2007) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2007.08.001 · Cited by 1,154 · see citing works
The anatomy of memory: an interactive overview of the parahippocampal–hippocampal network
van Strien, N. M., Cappaert, N. L. M., & Witter, M. P. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2614 · Cited by 1,041 · see citing works
Information Processing in Animals
(2014) · Psychology Press eBooks · doi:10.4324/9781315798820 · Cited by 902 · see citing works
Critical role of the hippocampus in memory for sequences of events
Fortin, N. J., Agster, K. L., & Eichenbaum, H. B. (2002) · Nature Neuroscience · doi:10.1038/nn834 · Cited by 881 · see citing works
Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat
Steward, O., & Scoville, S. A. (1976) · The Journal of Comparative Neurology · doi:10.1002/cne.901690306 · Cited by 837 · see citing works
When Is the Hippocampus Involved in Recognition Memory?
Barker, G. R. I., & Warburton, E. C. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6413-10.2011 · Cited by 818 · 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
Dissociating hippocampal subregions: A double dissociation between dentate gyrus and CA1
Gilbert, P. E., Kesner, R. P., & Lee, I. (2001) · Hippocampus · doi:10.1002/hipo.1077 · Cited by 641 · 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
Self-citationObject 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
Object recognition memory: Neurobiological mechanisms of encoding, consolidation and retrieval
Winters, B. D., Saksida, L. M., & Bussey, T. J. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.04.004 · Cited by 568 · see citing works
SOP: A Model of Automatic Memory Processing in Animal Behavior
Wagner, A. R. (2014) · doi:10.4324/9781315798820-6 · Cited by 516 · see citing works
Tests for Structural Equation Models
Bollen, K. A., & Long, J. S. (1992) · Sociological Methods & Research · doi:10.1177/0049124192021002001 · Cited by 468 · see citing works
Recollection-like memory retrieval in rats is dependent on the hippocampus
Fortin, N. J., Wright, S. P., & Eichenbaum, H. (2004) · Nature · doi:10.1038/nature02853 · Cited by 460 · see citing works
Different Contributions of the Hippocampus and Perirhinal Cortex to Recognition Memory
Wan, H., Aggleton, J. P., & Brown, M. W. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-03-01142.1999 · Cited by 449 · see citing works
Self-citationThe neural system that mediates familiarity memory
Montaldi, D., Spencer, T., Roberts, N., & Mayes, A. (2006) · Hippocampus · doi:10.1002/hipo.20178 · Cited by 435 · see citing works
Xiang, J. ‐., & Brown, M. W. (1998) · Neuropharmacology · doi:10.1016/s0028-3908(98)00030-6 · Cited by 425 · see citing works
Save, É., Poucet, B., Foreman, N., & Buhot, M.-C. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.3.447 · Cited by 383 · 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
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
Aggleton, J. P. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.09.005 · Cited by 319 · see citing works
Self-citationSparing of the familiarity component of recognition memory in a patient with hippocampal pathology.
Aggleton, J., Vann, S., Denby, C., Dix, S., Mayes, A., Roberts, N., & Yonelinas, A. (2005) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2005.01.019 · Cited by 317 · see citing works
Self-citationFurtak, S. C., Wei, S., Agster, K. L., & Burwell, R. D. (2007) · Hippocampus · doi:10.1002/hipo.20314 · Cited by 282 · 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
Borders and cytoarchitecture of the perirhinal and postrhinal cortices in the rat
Burwell, R. D. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1267 · Cited by 265 · see citing works
Forwood, S., Winters, B. D., & Bussey, T. J. (2004) · Hippocampus · doi:10.1002/hipo.20059 · Cited by 259 · see citing works
Hannesson, D. K., Howland, J. G., & Phillips, A. G. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5517-03.2004 · Cited by 231 · see citing works
The Hippocampus and Disambiguation of Overlapping Sequences
Agster, K. L., Fortin, N. J., & Eichenbaum, H. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-13-05760.2002 · Cited by 231 · see citing works
Cortical efferents of the perirhinal, postrhinal, and entorhinal cortices of the rat
Agster, K. L., & Burwell, R. D. (2009) · Hippocampus · doi:10.1002/hipo.20578 · Cited by 223 · see citing works
Information processing in animals: Memory mechanisms
Hall, G. (1983) · Biological Psychology · doi:10.1016/0301-0511(83)90021-2 · Cited by 223 · see citing works
The medial temporal lobe and the attributes of memory
Wixted, J. T., & Squire, L. R. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.03.005 · Cited by 222 · see citing works
What have ablation studies told us about the neural substrates of stimulus memory?
Murray, E. A. (1996) · Seminars in Neuroscience · doi:10.1006/smns.1996.0003 · Cited by 213 · see citing works
Zhu, X. O., Brown, M. W., McCabe, B. J., & Aggleton, J. P. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00320-i · Cited by 205 · see citing works
Self-citationZhu, X. O., Brown, M. W., & Aggleton, J. P. (1995) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1995.tb00679.x · Cited by 194 · see citing works
Self-citationVann, S., Tsivilis, D., Denby, C., Quamme, J., Yonelinas, A., Aggleton, J., Montaldi, D., & Mayes, A. (2009) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0812097106 · Cited by 184 · see citing works
Self-citationPoucet, B. (1989) · Behavioral Neuroscience · doi:10.1037//0735-7044.103.5.1009 · Cited by 168 · see citing works
Warburton, E. C., & Brown, M. W. (2009) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2009.12.022 · Cited by 166 · see citing works
Role of CA3 and CA1 subregions of the dorsal hippocampus on temporal processing of objects
Hoge, J., & Kesner, R. P. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.04.013 · Cited by 156 · see citing works
Cowell, R. A., Bussey, T. J., & Saksida, L. M. (2010) · Hippocampus · doi:10.1002/hipo.20865 · Cited by 151 · see citing works
Poucet, B. (1989) · Behavioral Neuroscience · doi:10.1037/0735-7044.103.5.1009 · Cited by 143 · see citing works
Recognition memory: Material, processes, and substrates
Brown, M. W., Warburton, E. C., & Aggleton, J. P. (2010) · Hippocampus · doi:10.1002/hipo.20858 · Cited by 138 · see citing works
Self-citationAlbasser, M. M., Poirier, G. L., & Aggleton, J. P. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.07042.x · Cited by 131 · see citing works
Self-citationFan, X., & Wang, L. (1998) · Educational and Psychological Measurement · doi:10.1177/0013164498058005001 · Cited by 122 · see citing works
Fornix microstructure correlates with recollection but not familiarity memory
Rudebeck, S. R., Scholz, J., Millington, R., Rohenkohl, G., Johansen-Berg, H., & Lee, A. C. H. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4707-09.2009 · Cited by 121 · see citing works
Ruth, R. E., Collier, T. J., & Routtenberg, A. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902700404 · Cited by 116 · see citing works
Mapping visual recognition memory through expression of the immediate early gene c-fos
Zhu, X.-O., McCabe, B. J., Aggleton, J. P., & Brown, M. W. (1996) · Neuroreport · doi:10.1097/00001756-199607290-00037 · Cited by 112 · see citing works
Self-citationSelective immunolesions of hippocampal cholinergic input fail to impair spatial working memory
McMahan, R. W., Sobel, T. J., & Baxter, M. G. (1997) · Hippocampus · doi:10.1002/(sici)1098-1063(1997)7:2 · Cited by 109 · see citing works
Benzodiazepine impairment of perirhinal cortical plasticity and recognition memory
Wan, H., Warburton, E. C., Zhu, X. O., Koder, T., Park, Y., Aggleton, J. P., Cho, K., Bashir, Z. I., & Brown, M. W. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03688.x · Cited by 81 · see citing works
Self-citationNew 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
Macrophage and microglia-like cells in the avian inner ear
Bhave, S. A., Oesterle, E. C., & Coltrera, M. D. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980824)398:2 · Cited by 77 · see citing works
Poirier, G. L., Amin, E., & Aggleton, J. P. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4607-07.2008 · Cited by 72 · see citing works
Self-citationIordanova, M., Burnett, D. J., Aggleton, J., Good, M., & Honey, R. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.07010.x · Cited by 69 · see citing works
Self-citationThe role of the dorsal CA1 and ventral CA1 in memory for the temporal order of a sequence of odors
Kesner, R. P., Hunsaker, M. R., & Ziegler, W. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.08.010 · Cited by 63 · see citing works
Ohara, S., Sato, S., Tsutsui, K., Witter, M. P., & Iijima, T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078928 · Cited by 59 · see citing works
Albasser, M. M., Amin, E., Lin, T.-C. E., Iordanova, M. D., & Aggleton, J. P. (2012) · Behavioral Neuroscience · doi:10.1037/a0029754 · Cited by 58 · see citing works
Self-citationInterfering with Fos expression in rat perirhinal cortex impairs recognition memory
Seoane, A., Tinsley, C. J., & Brown, M. W. (2012) · Hippocampus · doi:10.1002/hipo.22028 · Cited by 45 · see citing works
Albasser, M. M., Amin, E., Iordanova, M. D., Brown, M. W., Pearce, J. M. S., & Aggleton, J. P. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07755.x · Cited by 43 · see citing works
Self-citationContributions of area Te2 to rat recognition memoryPreprint
Ho, J. W., Narduzzo, K. E., Outram, A. R., Tinsley, C. J., Henley, J. M., Warburton, E. C., & Brown, M. W. (2011) · Learning & Memory · doi:10.1101/lm.2167511 · Cited by 42 · see citing works
Albasser, M. M., Amin, E., Iordanova, M. D., Brown, M. W., Pearce, J. M., & Aggleton, J. P. (2011) · Learning & Memory · doi:10.1101/lm.2132911 · Cited by 39 · see citing works
Self-citationAmin, E., Pearce, J. M., Brown, M. W., & Aggleton, J. P. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05131.x · Cited by 36 · see citing works
Self-citationProtzner, A. B., & McIntosh, A. R. (2006) · Human Brain Mapping · doi:10.1002/hbm.20233 · Cited by 36 · see citing works
Easton, A., & Eacott, M. J. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.10.019 · Cited by 31 · see citing works
Albasser, M. M., Dumont, J. R., Amin, E., Holmes, J. D., Horne, M. R., Pearce, J. M., & Aggleton, J. P. (2013) · Hippocampus · doi:10.1002/hipo.22154 · Cited by 24 · 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
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Barker, G. R. I., Banks, P. J., Scott, H., Ralph, G. S., Mitrophanous, K. A., Wong, L.-F., Bashir, Z. I., Uney, J. B., & Warburton, E. C. (2017) · Nature Neuroscience · doi:10.1038/nn.4472 · Cited by 124 · see citing works
- Authors
- Kinnavane, L., Amin, E., Horne, M., & Aggleton, J. P.
- Affiliations
- Cardiff University (GB)
- Corresponding author
- Kinnavane, L.
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2014-09-29
- Volume
- 40
- Issue
- 12
- Pages
- 3720-3734
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- PMC
- PMC4309468
- OpenAlex
- W2121438811
- Cited by
- 21
- References
- 75
- Citations by year
- 2023: 2 · 2022: 1 · 2021: 2 · 2020: 1 · 2019: 1 · 2018: 1 · 2017: 6 · 2016: 2 · 2015: 4 · 2014: 1
- FWCI
- 2.42
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- European Journal of Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- ORCA Online Research @Cardiff (Cardiff University) (acceptedVersion)
- Bristol Research (University of Bristol) (submittedVersion)
- Funders
- Wellcome Trust (WT 087955, WT 09520)
- 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
- recognition memory, perirhinal cortex, entorhinal cortex, hippocampal lesions, Fos expression, immediate early gene expression, novel object recognition, CA3, medial temporal lobe, network analysis, rats
- MeSH terms
- Animals, Hippocampus, Immunohistochemistry, Male, Models, Neurological, Neuropsychological Tests, Temporal Lobe, Proto-Oncogene Proteins c-fos, Recognition, Psychology, Rats
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