Spatial and stimulus-type tuning in the LEC, MEC, POR, PrC, CA1, and CA3 during spontaneous item recognition memory: Spatial and Stimulus-Type Tunings in Recognition Memory
Abstract
According to the "two streams" hypothesis, the lateral entorhinal (LEC) and the perirhinal (PrC) cortices process information related to items (a "what" stream), the postrhinal (POR) and the medial entorhinal cortices (MEC) process spatial information (a "where" stream), and both types of information are integrated in the hippocampus (HIP). However, within the framework of memory function, only the HIP is reliably shown to preferentially process spatial information, and the PrC items' features. In contrast, the role of the LEC and MEC in memory is virtually unexplored, and conflicting results emerge for the POR. Moreover, the specific contribution of the hippocampal subfields CA1 and CA3 to spatial and non-spatial memory is not thoroughly understood. To investigate which of these areas is specifically tuned to spatial demands or stimulus identity (odor or object), we assessed the pattern of activation of these areas during recognition memory by detecting the immediate-early gene Arc, commonly used as a marker of neuronal activation. We report that all MTL areas were recruited during the spatial and the non-spatial tasks. However, the LEC, MEC, POR, and CA1 were activated to a comparable level in spatial and non-spatial tasks, while the PrC was tuned to stimulus-type, not spatial demands, and CA3 to spatial demands but not stimulus-type. Results are discussed within the frame of a recent model suggesting that the MTL could be segregated in terms of memory processes, such as recollection and familiarity, rather than information content.
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The LEC preferentially processes object-associated information, e.g., the past and current locations of objects, and the context of the objects.
“Behavioral, imaging and electrophysiological recording data suggest that LEC preferentially processes object-associated information, e.g., the past and current locations of objects (Beer et al., 2013; Deshmukh and Knierim, 2011; Tsao et al., 2013; Van Cauter et al., 2013), and the context of the objects (Wilson et al., 2013b; Wilson et al., 2013c).”
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 Beer et al., 2013
Both CA1 and CA3 areas (more CA1 than CA3) were recruited in the NOP test.
“Both CA1 and CA3 areas (more CA1 than CA3) were recruited in the NOP test (Beer et al., 2013).”
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 Beer et al., 2013
Higher c-fos expression induced by the OPP, but not NOP, test was found in the hippocampal CA1 and CA3 subregions, while Arc mRNA imaging data showed higher involvement of CA3 in OPP than NOP.
“Higher c-fos expression induced by the OPP, but not NOP, test was found in the hippocampal CA1 and CA3 subregions (Mendez et al., 2015), while Arc mRNA imaging data showed higher involvement of CA3 in OPP than NOP (Beer et al., 2013).”
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 Beer et al., 2013
CA1 area was required in both object and location conditions, while CA3 was more recruited for OPP than NOP.
“CA1 area was required in both object and location conditions, while CA3 was more recruited for OPP than NOP (Beer et al., 2013).”
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 Beer et al., 2013
Imaging data show the CA1 to be activated during both spatial and nonspatial processing, while CA3 activation codes primarily information about place.
“Imaging data also show the CA1 to be activated during both spatial and nonspatial processing, while CA3 activation codes primarily information about place (Beer et al., 2013; Beer et al., 2014).”
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 Beer et al., 2013
Cites
The mouse brain in stereotaxic coordinates
Konsman, J. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(03)00088-x · Cited by 16,796 · see citing works
The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat
O'Keefe, J., & Dostrovsky, J. (1971) · Brain Research · doi:10.1016/0006-8993(71)90358-1 · Cited by 6,151 · see citing works
Microstructure of a spatial map in the entorhinal cortex
Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., & Moser, E. I. (2005) · Nature · doi:10.1038/nature03721 · Cited by 4,068 · see citing works
Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures?
Fanselow, M. S., & Dong, H.-W. (2010) · Neuron · doi:10.1016/j.neuron.2009.11.031 · Cited by 3,358 · 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
Object vision and spatial vision: Two cortical pathways
Mishkin, M., Ungerleider, L. G., & Macko, K. A. (1983) · Trends in Neurosciences · doi:10.1016/0166-2236(83)90190-x · Cited by 2,947 · 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
(1995) · Choice Reviews Online · doi:10.5860/choice.32-5931 · Cited by 2,337 · see citing works
Swanson, L. W., & Cowan, W. M. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901720104 · Cited by 1,571 · 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
Two cortical systems for memory-guided behaviour
Ranganath, C., & Ritchey, M. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3338 · Cited by 1,377 · see citing works
Hippocampal ‘time cells’ bridge the gap in memory for discontiguous events
MacDonald, C. J., Lepage, K. Q., Eden, U. T., & Eichenbaum, H. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.012 · Cited by 1,193 · see citing works
Requirement for Hippocampal CA3 NMDA Receptors in Associative Memory Recall
Nakazawa, K., Quirk, M. C., Chitwood, R. A., Watanabe, M., Yeckel, M. F., Sun, L. D., Kato, A., Carr, C. A., Johnston, D., Wilson, M. A., et al. (2002) · Science · doi:10.1126/science.1071795 · Cited by 1,090 · 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
Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles
Guzowski, J. F., McNaughton, B. L., Barnes, C. A., & Worley, P. F. (1999) · Nature Neuroscience · doi:10.1038/16046 · Cited by 1,032 · see citing works
Multiple routes to memory: distinct medial temporal lobe processes build item and source memories
Davachi, L., Mitchell, J. P., & Wagner, A. D. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0337195100 · Cited by 899 · see citing works
West, M. J. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01362-9 · Cited by 814 · see citing works
Separating the brain regions involved in recollection and familiarity in recognition memory
Yonelinas, A. P., Otten, L. J., Shaw, K. N., & Rugg, M. D. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.5295-04.2005 · Cited by 813 · see citing works
Mishkin, M., & Ungerleider, L. G. (1982) · Behavioural Brain Research · doi:10.1016/0166-4328(82)90081-x · Cited by 810 · see citing works
Dissociable correlates of recollection and familiarity within the medial temporal lobes
Ranganath, C., Yonelinas, A. P., Cohen, M. X., Dy, C. J., Tom, S. M., & D’Esposito, M. (2004) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2003.07.006 · Cited by 689 · 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
Cortical analysis of visual context.
Bar, M., & Aminoff, E. (2003) · Neuron · doi:10.1016/s0896-6273(03)00167-3 · Cited by 630 · see citing works
NMDA receptors, place cells and hippocampal spatial memory
Nakazawa, K., McHugh, T. J., Wilson, M. A., & Tonegawa, S. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1385 · Cited by 619 · see citing works
Yonelinas, A. (1997) · Memory & Cognition · doi:10.3758/bf03211318 · Cited by 523 · see citing works
The Parahippocampal Region: Corticocortical Connectivity
Burwell, R. D. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06717.x · Cited by 513 · see citing works
Hippocampal CA3 NMDA Receptors Are Crucial for Memory Acquisition of One-Time Experience
Nakazawa, K., Sun, L. D., Quirk, M. C., Rondi‐Reig, L., Wilson, M. A., & Tonegawa, S. (2003) · Neuron · doi:10.1016/s0896-6273(03)00165-x · Cited by 506 · see citing works
Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning
Nakashiba, T., Young, J. Z., McHugh, T. J., Buhl, D. L., & Tonegawa, S. (2008) · Science · doi:10.1126/science.1151120 · Cited by 492 · see citing works
Vazdarjanova, A., & Guzowski, J. F. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0350-04.2004 · Cited by 465 · see citing works
Representation of Non-Spatial and Spatial Information in the Lateral Entorhinal Cortex
Deshmukh, S. S., & Knierim, J. J. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00069 · Cited by 449 · 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
The 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
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
Mapping behaviorally relevant neural circuits with immediate-early gene expression
Guzowski, J. F., Timlin, J. A., Roysam, B., McNaughton, B. L., Worley, P. F., & Barnes, C. A. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.08.018 · Cited by 404 · see citing works
Bowles, B., Crupi, C., Mirsattari, S., Pigott, S. E., Parrent, A., Pruessner, J., Yonelinas, A., & Köhler, S. (2007) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0705273104 · Cited by 367 · see citing works
Morris, R., & Frey, U. (1997) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1997.0136 · Cited by 366 · see citing works
Impaired Spatial Representation in CA1 after Lesion of Direct Input from Entorhinal Cortex
Brun, V. H., Leutgeb, S., Wu, H., Schwarcz, R. M., Witter, M. P., Moser, E. I., & Moser, M. (2008) · Neuron · doi:10.1016/j.neuron.2007.11.034 · Cited by 364 · see citing works
Memory Representation within the Parahippocampal Region
Young, B. J., Otto, T., Fox, G. D., & Eichenbaum, H. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-13-05183.1997 · Cited by 363 · see citing works
Ensemble Dynamics of Hippocampal Regions CA3 and CA1
Guzowski, J. F., Knierim, J. J., & Moser, E. I. (2004) · Neuron · doi:10.1016/j.neuron.2004.11.003 · Cited by 354 · 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
Otto, T., & Eichenbaum, H. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.5.762 · Cited by 343 · see citing works
The Parahippocampal Cortex Mediates Spatial and Nonspatial Associations
Aminoff, E., Gronau, N., & Bar, M. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl078 · Cited by 341 · see citing works
Behavioral functions of the CA3 subregion of the hippocampusPreprint
Kesner, R. P. (2007) · Learning & Memory · doi:10.1101/lm.688207 · Cited by 337 · see citing works
Formation of Temporal Memory Requires NMDA Receptors within CA1 Pyramidal Neurons
Huerta, P. T., Sun, L. D., Wilson, M. A., & Tonegawa, S. (2000) · Neuron · doi:10.1016/s0896-6273(00)80909-5 · Cited by 335 · see citing works
Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex
Brun, V. H., Solstad, T., Kjelstrup, K. B., Fyhn, M., Witter, M. P., Moser, E. I., & Moser, M. (2008) · Hippocampus · doi:10.1002/hipo.20504 · Cited by 315 · see citing works
Vazdarjanova, A. I., McNaughton, B. L., Barnes, C. A., Worley, P. F., & Guzowski, J. F. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-23-10067.2002 · Cited by 307 · see citing works
Perirhinal Cortex Supports Encoding and Familiarity-Based Recognition of Novel Associations
Haskins, A., Yonelinas, A. P., Quamme, J. R., & Ranganath, C. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.035 · Cited by 281 · see citing works
Considering the evolution of regeneration in the central nervous system
Tanaka, E. M., & Ferretti, P. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2707 · Cited by 264 · see citing works
Using immediate-early genes to map hippocampal subregional functionsPreprint
Kubík, Š., Miyashita, T., & Guzowski, J. F. (2007) · Learning & Memory · doi:10.1101/lm.698107 · Cited by 257 · see citing works
Bar, M., Aminoff, E., & Schacter, D. L. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0987-08.2008 · Cited by 246 · see citing works
Gateways of Ventral and Dorsal Streams in Mouse Visual Cortex
Wang, Q., Gao, E., & Burkhalter, A. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3488-10.2011 · Cited by 232 · 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
Moser, E. I., & Moser, M. (2008) · Hippocampus · doi:10.1002/hipo.20483 · Cited by 220 · see citing works
Apolipoprotein E receptors: linking brain development and alzheimer's disease
Herz, J., & Beffert, U. (2000) · Nature reviews. Neuroscience · doi:10.1038/35036221 · Cited by 218 · see citing works
Norman, G., & Eacott, M. J. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.2.557 · Cited by 217 · 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
Distinct roles of medial and lateral entorhinal cortex in spatial cognition
Van Cauter, T., Camon, J., Alvernhe, A., Elduayen, C., Sargolini, F., & Save, E. (2013) · Cerebral Cortex · doi:10.1093/cercor/bhs033 · Cited by 196 · see citing works
Zhu, 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
The rhinal cortices: a wall of inhibition between the neocortex and the hippocampus
DECURTIS, M., & Paré, D. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.08.005 · Cited by 185 · 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
Recognition memory: opposite effects of hippocampal damage on recollection and familiarity
Sauvage, M. M., Fortin, N. J., Owens, C. B., Yonelinas, A. P., & Eichenbaum, H. (2007) · Nature Neuroscience · doi:10.1038/nn2016 · Cited by 174 · see citing works
Self-citationPihlajamäki, M., Tanila, H., Könönen, M., Hänninen, T., Hämäläinen, A., Soininen, H., & Aronen, H. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03282.x · Cited by 156 · see citing works
Gilbert, P. E., & Kesner, R. P. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.6.1385 · Cited by 146 · see citing works
Eacott, M. J., & Gaffan, E. A. (2005) · The Quarterly Journal of Experimental Psychology Section B · doi:10.1080/02724990444000203 · Cited by 145 · see citing works
Distinct roles for dorsal CA3 and CA1 in memory for sequential nonspatial events
Farovik, A., Dupont, L. M., & Eichenbaum, H. (2010) · Learning & Memory · doi:10.1101/lm.1616209 · Cited by 140 · see citing works
The Role of CA1 in the Acquisition of an Object-Trace-Odor Paired Associate Task.
Kesner, R. P., Hunsaker, M. R., & Gilbert, P. E. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.3.781 · Cited by 121 · see citing works
Positional firing properties of postrhinal cortex neurons
Burwell, R. D., & Hafeman, D. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00160-x · Cited by 119 · see citing works
Hippocampal Representational Organization and Spatial Context
Mizumori, S. J. Y., Ragozzino, K. E., Cooper, B. G., & Leutgeb, S. (1999) · Hippocampus · doi:10.1002/(sici)1098-1063(1999)9:4 · Cited by 106 · see citing works
Nakamura, N. H., Flasbeck, V., Maingret, N., Kitsukawa, T., & Sauvage, M. M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4480-12.2013 · Cited by 103 · see citing works
Self-citationThe temporal attributes of episodic memory
Kesner, R. P., & Hunsaker, M. R. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.12.029 · Cited by 102 · see citing works
Kesner, R. P., Hunsaker, M. R., & Warthen, M. W. (2008) · Behavioral Neuroscience · doi:10.1037/a0013592 · Cited by 100 · see citing works
Single Neuron Activity and Theta Modulation in Postrhinal Cortex during Visual Object Discrimination
Furtak, S. C., Ahmed, O. J., & Burwell, R. D. (2012) · Neuron · doi:10.1016/j.neuron.2012.10.039 · Cited by 92 · see citing works
Kajiwara, R., Takashima, I., Mimura, Y., Witter, M. P., & Iijima, T. (2003) · Journal of Neurophysiology · doi:10.1152/jn.01033.2002 · Cited by 91 · see citing works
CA3 NMDA receptors are required for the rapid formation of a salient contextual representation
McHugh, T. J., & Tonegawa, S. (2009) · Hippocampus · doi:10.1002/hipo.20684 · Cited by 63 · see citing works
NMDA signaling in CA1 mediates selectively the spatial component of episodic memory
Place, R., Lykken, C., Beer, Z., Suh, J., McHugh, T. J., Tonegawa, S., Eichenbaum, H., & Sauvage, M. M. (2012) · Learning & Memory · doi:10.1101/lm.025254.111 · Cited by 46 · see citing works
Self-citationAmygdala lesions selectively impair familiarity in recognition memory
Farovik, A., Place, R., Miller, D. R., & Eichenbaum, H. (2011) · Nature Neuroscience · doi:10.1038/nn.2919 · Cited by 46 · see citing works
Gaffan, E. A., Healey, A. N., & Eacott, M. J. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.5.992 · Cited by 45 · see citing works
Mapping memory function in the medial temporal lobe with the immediate-early gene Arc
Sauvage, M. M., Nakamura, N. H., & Beer, Z. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.04.048 · Cited by 41 · see citing works
Self-citationBeaudin, S. A., Singh, T., Agster, K. L., & Burwell, R. D. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs038 · Cited by 39 · see citing works
The Caudal Medial Entorhinal Cortex: a Selective Role in Recollection-Based Recognition Memory
Sauvage, M. M., Beer, Z., Ekovich, M., Ho, L., & Eichenbaum, H. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4301-10.2010 · Cited by 38 · see citing works
Self-citationEffect of cholinergic drugs on the brainstem auditory evoked responses (far-field) in rats
Bhargava, V. K., Salamy, A., & McKean, C. M. (1978) · Neuroscience · doi:10.1016/0306-4522(78)90034-9 · Cited by 25 · see citing works
Sauvage, M. M. (2010) · Consciousness and Cognition · doi:10.1016/j.concog.2010.06.023 · Cited by 18 · see citing works
Self-citationGlutamate-induced fastigial pressor response in the dog
Dormer, K. J., Foreman, R. D., & STONE, H. L. (1977) · Neuroscience · doi:10.1016/0306-4522(77)90053-7 · Cited by 17 · see citing works
Role of dCA3 efferents via the fimbria in the acquisition of a delay nonmatch to place task
Hunsaker, M. R., Allan, K. D., & Kesner, R. P. (2007) · Hippocampus · doi:10.1002/hipo.20288 · Cited by 16 · 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
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
Chao, O. Y.-H., Huston, J. P., Li, J., Wang, A., & Silva, M. A. D. S. (2015) · Hippocampus · doi:10.1002/hipo.22547 · Cited by 110 · see citing works
Stackman, 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
Self-citationSave, É., & Sargolini, F. (2017) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2017.00081 · Cited by 53 · see citing works
In search of a recognition memory engram
Brown, M. W., & Banks, P. J. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.09.016 · Cited by 56 · see citing works
McKenzie, S., Keene, C. S., Farovik, A., Bladon, J. H., Place, R., Komorowski, R. W., & Eichenbaum, H. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.12.008 · Cited by 53 · see citing works
Dietz, B. E., & Manahan‐Vaughan, D. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.02.026 · Cited by 53 · see citing works
Beer, Z., Vavra, P., Atucha, E., Rentzing, K., Heinze, H.-J., & Sauvage, M. M. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2006100 · Cited by 44 · see citing works
Self-citationRodo, C., Sargolini, F., & Save, E. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.12.009 · Cited by 42 · see citing works
Mapping memory function in the medial temporal lobe with the immediate-early gene Arc
Sauvage, M. M., Nakamura, N. H., & Beer, Z. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.04.048 · Cited by 41 · see citing works
Self-citationde Souza Silva, M. A., Huston, J. P., Wang, A.-L., Petri, D., & Chao, O. Y.-H. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhv112 · Cited by 41 · see citing works
Chao, O. Y., Nikolaus, S., Lira Brandão, M., Huston, J. P., & de Souza Silva, M. A. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.03.019 · Cited by 38 · see citing works
Lateral Entorhinal Cortex Lesions Impair Local Spatial Frameworks
Kuruvilla, M. V., & Ainge, J. A. (2017) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2017.00030 · Cited by 39 · see citing works
Lux, V., Atucha, E., Kitsukawa, T., & Sauvage, M. M. (2016) · eLife · doi:10.7554/elife.11862 · Cited by 34 · see citing works
Self-citationNeural circuits for goal-directed navigation across species
Basu, J., & Nagel, K. I. (2024) · Trends in Neurosciences · doi:10.1016/j.tins.2024.09.005 · Cited by 33 · see citing works
Single-cell memory trace imaging with immediate-early genes
Sauvage, M. M., Kitsukawa, T., & Atucha, E. (2019) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2019.108368 · Cited by 32 · see citing works
Self-citationUpdate on temporal lobe‐dependent information processing, in health and disease
Chauvière, L. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14594 · Cited by 25 · see citing works
Atucha, E., Ku, S.-P., Lippert, M., & Sauvage, M. M. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113317 · Cited by 24 · see citing works
Self-citationLux, V., Masseck, O. A., Herlitze, S., & Sauvage, M. M. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv282 · Cited by 23 · see citing works
Self-citationQi, X., Du, Z. J., Zhu, L., Liu, X., Xu, H., Zhou, Z., Zhong, C., Li, S., Wang, L., & Zhang, Z. (2019) · Neuroscience Bulletin · doi:10.1007/s12264-018-0325-4 · Cited by 19 · see citing works
Scott, H., Smith, A. E., Barker, G. R., Uney, J. B., & Warburton, E. C. (2017) · Neuroepigenetics · doi:10.1016/j.nepig.2017.02.001 · Cited by 18 · see citing works
Lateral entorhinal cortex lesions impair both egocentric and allocentric object–place associations
Kuruvilla, M. V., Wilson, D. I. G., & Ainge, J. A. (2020) · Brain and Neuroscience Advances · doi:10.1177/2398212820939463 · Cited by 18 · see citing works
Atucha, E., Karew, A., Kitsukawa, T., & Sauvage, M. M. (2017) · Hippocampus · doi:10.1002/hipo.22754 · Cited by 17 · see citing works
Self-citationProbing the nature of episodic memory in rodents
Huston, J. P., & Chao, O. Y.-H. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104930 · Cited by 16 · see citing works
The anatomy and function of the postrhinal cortex.
Estela-Pro, V. J., & Burwell, R. D. (2021) · Behavioral Neuroscience · doi:10.1037/bne0000500 · Cited by 14 · see citing works
Hallmarks of healthy cognitive aging: Inter-individual differences in aging trajectories
Abrous, D. N., Blin, N., Boraxbekk, C., Catheline, G., Fitzsimons, C. P., Hilscher, M. M., Lemoine, M., Lopes, L. V., Maass, A., Nilsson, M., et al. (2026) · Ageing Research Reviews · doi:10.1016/j.arr.2026.103102 · Cited by 18 · see citing works
Self-citationHippocampal ensemble dynamics and memory performance are modulated by respiration during encoding
Nakamura, N. H., Furue, H., Kobayashi, K., & Oku, Y. (2023) · Nature Communications · doi:10.1038/s41467-023-40139-7 · Cited by 13 · see citing works
Immediate-Early Gene Expression in Neural Circuits Related to Object Recognition Memory
Barbosa, F. F., & Silva, R. H. (2018) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-812012-5.00018-5 · Cited by 11 · see citing works
Poitreau, J., Buttet, M., Manrique, C., Poucet, B., Sargolini, F., & Save, E. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113448 · Cited by 10 · see citing works
Oulé, M., Atucha, E., Wells, T. M., Macharadze, T., Sauvage, M. M., Kreutz, M. R., & Lopez‐Rojas, J. (2021) · iScience · doi:10.1016/j.isci.2021.102876 · Cited by 10 · see citing works
Self-citationRecognition memory-induced gene expression in the perirhinal cortex: A transcriptomic analysis
Scott, H., Rogers, M. F., Scott, H. L., Campbell, C., Warburton, E. C., & Uney, J. B. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.04.007 · Cited by 9 · see citing works
Hippocampal Arc protein expression and conditioned fear.
Hudgins, C. D., & Otto, T. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.04.004 · Cited by 7 · see citing works
How do mammals convert dynamic odor information into neural maps for landscape navigation?
Sunil, A., Pedroncini, O., Schaefer, A. T., & Ackels, T. (2024) · PLoS Biology · doi:10.1371/journal.pbio.3002908 · Cited by 7 · see citing works
Hoang, T., & Manahan‐Vaughan, D. (2023) · Brain Structure and Function · doi:10.1007/s00429-023-02694-z · Cited by 4 · see citing works
Remembering the gist of an event over a lifetime depends on the hippocampusPreprint
Atucha, E., Ku, S.-P., Lippert, M., & Sauvage, M. M. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.04.14.439803 · Cited by 4 · see citing works
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Pedroncini, O., Federman, N., & Marín‐Burgin, A. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2414038121 · Cited by 3 · see citing works
Chao, O. Y.-H., Huston, J. P., & Silva, M. A. D. S. (2018) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-812012-5.00014-8 · Cited by 3 · see citing works
Miller, T. D., Kennard, C., Gowland, P. A., Antoniades, C. A., & Rosenthal, C. R. (2024) · Cognitive Neuroscience · doi:10.1080/17588928.2024.2315818 · Cited by 2 · see citing works
The entorhinal spatial map integrates visual identity information of landmarks
Wang, G., Shahid, F., Malone, T. J., Tyan, J., Cekada, K., Chen, L., & Gu, Y. Z. (2026) · Nature Communications · doi:10.1038/s41467-026-72453-1 · Cited by 3 · see citing works
Evidence for grid-cell-like activity in the time domain
Peters‐Founshtein, G., Dafni‐Merom, A., Monsa, R., & Arzy, S. (2024) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2024.108878 · Cited by 2 · see citing works
Perirhinal Cortex: Neural Representations ☆
Brown, M. W., Eldridge, M. A. G., & Banks, P. J. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21078-x · Cited by 1 · see citing works
Heimer‐McGinn, V., Trettel, S. G., Kent, B. W., Singh, M. A., & Burwell, R. D. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.23.497405 · Cited by 1 · see citing works
Evidence for grid-cell-related activity in the time domainPreprint
Peters‐Founshtein, G., Dafni‐Merom, A., Monsa, R., & Arzy, S. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.14.476894
Arai, S., Sypniewski, K. A., & Pavlides, C. (2024) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2024.108015
Targeting diaschisis to alleviate memory deficits after experimental stroke
Adenauer, L., Contini, G., Reichelt, K., Pires, N., Beck, H., & Opitz, T. (2026) · Neurobiology of Disease · doi:10.1016/j.nbd.2026.107401
Aberrant increased GABAergic neuronal activity in postrhinal cortex impairs spatial memory
Zhang, J., Liu, M., Wang, D., Shi, M., Ye, X., Ahmadzai, S., & Qi, X. (2026) · Behavioural Brain Research · doi:10.1016/j.bbr.2026.116277
- Authors
- Beer, Z., Chwiesko, C., Kitsukawa, T., & Sauvage, M. M.
- Affiliations
- Ruhr University Bochum (DE)
- The University of Osaka (JP)
- Corresponding author
- Sauvage, Magdalena M.
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2013-09-18
- Volume
- 23
- Issue
- 12
- Pages
- 1425-1438
- ISSN
- 1050-9631 (ISSN-L)
- OpenAlex
- W1606464716
- Cited by
- 49
- References
- 84
- Citations by year
- 2026: 4 · 2024: 6 · 2023: 3 · 2022: 4 · 2021: 4 · 2020: 2 · 2019: 4 · 2018: 3 · 2017: 7 · 2016: 5 · 2015: 4 · 2014: 2 · 2013: 1
- FWCI
- 2.18
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministerio de Economía y Competitividad
- 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
- recognition memory, spatial memory, lateral entorhinal cortex, medial entorhinal cortex, perirhinal cortex, postrhinal cortex, hippocampal CA1, hippocampal CA3, medial temporal lobe
- MeSH terms
- Analysis of Variance, Animals, Cytoskeletal Proteins, Gene Expression Regulation, Male, Mice, Inbred C57BL, Nerve Tissue Proteins, Neural Pathways, Space Perception, Signal Transduction, Entorhinal Cortex, Recognition, Psychology, Mice
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