Object-place-context learning impairment correlates with spatial learning impairment in aged Long-Evans rats.
Morris water maze
aging
context
entorhinal cortex
hippocampus
memory
object recognition
Journal
Hippocampus
ISSN: 1098-1063
Titre abrégé: Hippocampus
Pays: United States
ID NLM: 9108167
Informations de publication
Date de publication:
11 Dec 2023
11 Dec 2023
Historique:
revised:
28
09
2023
received:
08
02
2023
accepted:
18
11
2023
medline:
11
12
2023
pubmed:
11
12
2023
entrez:
11
12
2023
Statut:
aheadofprint
Résumé
The hippocampal formation is vulnerable to the process of normal aging. In humans, the extent of this age-related deterioration varies among individuals. Long-Evans rats replicate these individual differences as they age, and therefore they serve as a valuable model system to study aging in the absence of neurodegenerative diseases. In the Morris water maze, aged memory-unimpaired (AU) rats navigate to remembered goal locations as effectively as young rats and demonstrate minimal alterations in physiological markers of synaptic plasticity, whereas aged memory-impaired (AI) rats show impairments in both spatial navigation skills and cellular and molecular markers of plasticity. The present study investigates whether another cognitive domain is affected similarly to navigation in aged Long-Evans rats. We tested the ability of young, AU, and AI animals to recognize novel object-place-context (OPC) configurations and found that performance on the novel OPC recognition paradigm was significantly correlated with performance on the Morris water maze. In the first OPC test, young and AU rats, but not AI rats, successfully recognized and preferentially explored objects in novel OPC configurations. In a second test with new OPC configurations, all age groups showed similar OPC associative recognition memory. The results demonstrated similarities in the behavioral expression of associative, episodic-like memory between young and AU rats and revealed age-related, individual differences in functional decline in both navigation and episodic-like memory abilities.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIA NIH HHS
ID : P01 AG009973
Pays : United States
Informations de copyright
© 2023 Wiley Periodicals LLC.
Références
Bergado, J. A., Almaguer, W., Rojas, Y., Capdevila, V., & Frey, J. U. (2011). Spatial and emotional memory in aged rats: A behavioral-statistical analysis. Neuroscience, 172, 256-269.
Bitzenhofer, S. H., Westeinde, E. A., Zhang, H. X. B., & Isaacson, J. S. (2022). Rapid odor processing by layer 2 subcircuits in lateral entorhinal cortex. eLife, 11, e75065.
Bota, M., Sporns, O., & Swanson, L. W. (2015). Architecture of the cerebral cortical association connectome underlying cognition. Proceedings of the National Academy of Sciences, 112(16), E2093-E2101.
Braak, H., & Braak, E. V. A. (1995). Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiology of Aging, 16(3), 271-278.
Branch, A., Monasterio, A., Blair, G., Knierim, J. J., Gallagher, M., & Haberman, R. P. (2019). Aged rats with preserved memory dynamically recruit hippocampal inhibition in a local/global cue mismatch environment. Neurobiology of Aging, 76, 151-161.
Burke, S. N., Wallace, J. L., Nematollahi, S., Uprety, A. R., & Barnes, C. A. (2010). Pattern separation deficits may contribute to age-associated recognition impairments. Behavioral Neuroscience, 124(5), 559-573.
Cavoy, A., & Delacour, J. (1993). Spatial but not object recognition is impaired by aging in rats. Physiology & Behavior, 53(3), 527-530.
Chao, O. Y., Huston, J. P., Li, J. S., Wang, A. L., & de Souza Silva, M. A. (2016). The medial prefrontal cortex-lateral entorhinal cortex circuit is essential for episodic-like memory and associative object-recognition. Hippocampus, 26(5), 633-645.
Deshmukh, S. S., & Knierim, J. J. (2011). Representation of non-spatial and spatial information in the lateral entorhinal cortex. Frontiers in Behavioral Neuroscience, 5, 69.
Doan, T. P., Lagartos-Donate, M. J., Nilssen, E. S., Ohara, S., & Witter, M. P. (2019). Convergent projections from perirhinal and postrhinal cortices suggest a multisensory nature of lateral, but not medial, entorhinal cortex. Cell Reports, 29(3), 617-627.
Eacott, M. J., & Norman, G. (2004). Integrated memory for object, place, and context in rats: A possible model of episodic-like memory? Journal of Neuroscience, 24(8), 1948-1953.
Ennaceur, A., & Delacour, J. (1988). A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behavioural Brain Research, 31(1), 47-59.
Foster, T. C. (1999). Involvement of hippocampal synaptic plasticity in age-related memory decline. Brain Research Reviews, 30(3), 236-249.
Fouquet, M., Desgranges, B., La Joie, R., Rivière, D., Mangin, J. F., Landeau, B., Mezenge, F., Pelerin, A., de La Sayette, V., Viader, F., Baron, J., Eustache, F., & Chételat, G. (2012). Role of hippocampal CA1 atrophy in memory encoding deficits in amnestic mild cognitive impairment. NeuroImage, 59(4), 3309-3315.
Gage, F. H., Dunnett, S. B., & Björklund, A. (1984). Spatial learning and motor deficits in aged rats. Neurobiology of Aging, 5(1), 43-48.
Gallagher, M., Burwell, R., & Burchinal, M. (1993). Severity of spatial learning impairment in aging: Development of a learning index for performance in the Morris water maze. Behavioral Neuroscience, 107(4), 618-626.
Gallagher, M., & Rapp, P. R. (1997). The use of animal models to study the effects of aging on cognition. Annual Review of Psychology, 48(1), 339-370.
Gámiz, F., & Gallo, M. (2012). Spontaneous object recognition memory in aged rats: Complexity versus similarity. Learning & Memory, 19(10), 444-448.
Gómez-Isla, T., Price, J. L., McKeel, D. W., Jr., Morris, J. C., Growdon, J. H., & Hyman, B. T. (1996). Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. Journal of Neuroscience, 16(14), 4491-4500.
Hafting, T., Fyhn, M., Molden, S., Moser, M. B., & Moser, E. I. (2005). Microstructure of a spatial map in the entorhinal cortex. Nature, 436(7052), 801-806.
Hirni, D. I., Kivisaari, S. L., Krumm, S., Monsch, A. U., Berres, M., Oeksuez, F., Reinhardt, J., Ulmer, S., Kressig, R. W., Stippich, C., & Taylor, K. I. (2016). Neuropsychological markers of medial perirhinal and entorhinal cortex functioning are impaired twelve years preceding diagnosis of Alzheimer's dementia. Journal of Alzheimer's Disease, 52(2), 573-580.
Høydal, Ø. A., Skytøen, E. R., Andersson, S. O., Moser, M. B., & Moser, E. I. (2019). Object-vector coding in the medial entorhinal cortex. Nature, 568(7752), 400-404.
Hyman, B. T., Van Hoesen, G. W., Damasio, A. R., & Barnes, C. L. (1984). Alzheimer's disease: Cell-specific pathology isolates the hippocampal formation. Science, 225(4667), 1168-1170.
Jack, C. R., Petersen, R. C., Xu, Y. C., Waring, S. C., O'Brien, P. C., Tangalos, E. G., Smith, G. E., Ivnik, R. J., & Kokmen, E. (1997). Medial temporal atrophy on MRI in normal aging and very mild Alzheimer's disease. Neurology, 49(3), 786-794.
Knierim, J. J. (2015). The hippocampus. Current Biology, 25(23), R1116-R1121.
Kordower, J. H., Chu, Y., Stebbins, G. T., DeKosky, S. T., Cochran, E. J., Bennett, D., & Mufson, E. J. (2001). Loss and atrophy of layer II entorhinal cortex neurons in elderly people with mild cognitive impairment. Annals of Neurology: Official Journal of the American Neurological Association and the Child Neurology Society, 49(2), 202-213.
Kropff, E., Carmichael, J. E., Moser, M. B., & Moser, E. I. (2015). Speed cells in the medial entorhinal cortex. Nature, 523(7561), 419-424.
Langston, R. F., & Wood, E. R. (2010). Associative recognition and the hippocampus: Differential effects of hippocampal lesions on object-place, object-context and object-place-context memory. Hippocampus, 20(10), 1139-1153.
Lee, I. A., & Preacher, K. J. (2013). Calculation for the test of the difference between two dependent correlations with one variable in common [computer software]. Available from http://quantpsy.org.
Lee, H., Wang, Z., Tillekeratne, A., Lukish, N., Puliyadi, V., Zeger, S., Gallagher, M., & Knierim, J. J. (2022). Loss of functional heterogeneity along the CA3 transverse axis in aging. Current Biology, 32, 2681-2693.e4.
Lee, H., Wang, Z., Zeger, S. L., Gallagher, M., & Knierim, J. J. (2021). Heterogeneity of age-related neural hyperactivity along the CA3 transverse axis. Journal of Neuroscience, 41(4), 663-673.
Leitner, F. C., Melzer, S., Lütcke, H., Pinna, R., Seeburg, P. H., Helmchen, F., & Monyer, H. (2016). Spatially segregated feedforward and feedback neurons support differential odor processing in the lateral entorhinal cortex. Nature Neuroscience, 19(7), 935-944.
Lukaszewska, I., & Radulska, I. (1994). Object recognition is not impaired in old rats. Acta Neurobiologiae Experimentalis, 54, 143-150.
Mathis, A., Mamidanna, P., Cury, K. M., Abe, T., Murthy, V. N., Mathis, M. W., & Bethge, M. (2018). DeepLabCut: Markerless pose estimation of user-defined body parts with deep learning. Nature Neuroscience, 21(9), 1281-1289.
Morris, R. (1984). Developments of a water-maze procedure for studying spatial learning in the rat. Journal of Neuroscience Methods, 11(1), 47-60.
Mueller, S. G., & Weiner, M. W. (2009). Selective effect of age, apo e4, and Alzheimer's disease on hippocampal subfields. Hippocampus, 19(6), 558-564.
Ohara, S., Gianatti, M., Itou, K., Berndtsson, C. H., Doan, T. P., Kitanishi, T., Mizuseki, K., Iijima, T., Tsutsui, K. I., & Witter, M. P. (2019). Entorhinal layer II calbindin-expressing neurons originate widespread telencephalic and intrinsic projections. Frontiers in Systems Neuroscience, 13, 54.
O'Keefe, J., & Nadel, L. (1978). The hippocampus as a cognitive map. Oxford University Press.
Olsen, R. K., Yeung, L. K., Noly-Gandon, A., D'Angelo, M. C., Kacollja, A., Smith, V. M., Ryan, J. D., & Barense, M. D. (2017). Human anterolateral entorhinal cortex volumes are associated with cognitive decline in aging prior to clinical diagnosis. Neurobiology of Aging, 57, 195-205.
Pereira, I. T., Gallagher, M., & Rapp, P. R. (2015). Head west or left, east or right: Interactions between memory systems in neurocognitive aging. Neurobiology of Aging, 36(11), 3067-3078.
Rapp, P. R., & Amaral, D. G. (1992). Individual differences in the cognitive and neurobiological consequences of normal aging. Trends in Neurosciences, 15(9), 340-345.
Ray, S., Naumann, R., Burgalossi, A., Tang, Q., Schmidt, H., & Brecht, M. (2014). Grid-layout and theta-modulation of layer 2 pyramidal neurons in medial entorhinal cortex. Science, 343(6173), 891-896.
Redish, A. D., & Touretzky, D. S. (1998). The role of the hippocampus in solving the Morris water maze. Neural Computation, 10(1), 73-111.
Robitsek, R. J., Fortin, N. J., Koh, M. T., Gallagher, M., & Eichenbaum, H. (2008). Cognitive aging: A common decline of episodic recollection and spatial memory in rats. Journal of Neuroscience, 28(36), 8945-8954.
Rosenzweig, E. S., Redish, A. D., McNaughton, B. L., & Barnes, C. A. (2003). Hippocampal map realignment and spatial learning. Nature Neuroscience, 6(6), 609-615.
Sargolini, F., Fyhn, M., Hafting, T., McNaughton, B. L., Witter, M. P., Moser, M. B., & Moser, E. I. (2006). Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science, 312(5774), 758-762.
Scoville, W. B., & Milner, B. (1957). Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery, and Psychiatry, 20(1), 11-21.
Solstad, T., Boccara, C. N., Kropff, E., Moser, M. B., & Moser, E. I. (2008). Representation of geometric borders in the entorhinal cortex. Science, 322(5909), 1865-1868.
Stranahan, A. M., Haberman, R. P., & Gallagher, M. (2011). Cognitive decline is associated with reduced reelin expression in the entorhinal cortex of aged rats. Cerebral Cortex, 21(2), 392-400.
Stranahan, A. M., Salas-Vega, S., Jiam, N. T., & Gallagher, M. (2011). Interference with reelin signaling in the lateral entorhinal cortex impairs spatial memory. Neurobiology of Learning and Memory, 96(2), 150-155.
Teng, E., & Squire, L. R. (1999). Memory for places learned long ago is intact after hippocampal damage. Nature, 400(6745), 675-677.
Tolman, E. C. (1948). Cognitive maps in rats and men. Psychological Review, 55(4), 189-208.
Tsao, A., Moser, M. B., & Moser, E. I. (2013). Traces of experience in the lateral entorhinal cortex. Current Biology, 23(5), 399-405.
Tsao, A., Sugar, J., Lu, L., Wang, C., Knierim, J. J., Moser, M. B., & Moser, E. I. (2018). Integrating time from experience in the lateral entorhinal cortex. Nature, 561(7721), 57-62.
Tse, D., Langston, R. F., Kakeyama, M., Bethus, I., Spooner, P. A., Wood, E. R., Menno, P. W., & Morris, R. G. (2007). Schemas and memory consolidation. Science, 316(5821), 76-82.
Vandrey, B., Garden, D. L., Ambrozova, V., McClure, C., Nolan, M. F., & Ainge, J. A. (2020). Fan cells in layer 2 of the lateral entorhinal cortex are critical for episodic-like memory. Current Biology, 30(1), 169-175.
Varga, C., Lee, S. Y., & Soltesz, I. (2010). Target-selective GABAergic control of entorhinal cortex output. Nature Neuroscience, 13(7), 822-824.
Wang, C., Chen, X., Lee, H., Deshmukh, S. S., Yoganarasimha, D., Savelli, F., & Knierim, J. J. (2018). Egocentric coding of external items in the lateral entorhinal cortex. Science, 362(6417), 945-949.
Wilson, I. A., Gallagher, M., Eichenbaum, H., & Tanila, H. (2006). Neurocognitive aging: Prior memories hinder new hippocampal encoding. Trends in Neurosciences, 29(12), 662-670.
Wilson, I. A., Ikonen, S., Gureviciene, I., McMahan, R. W., Gallagher, M., Eichenbaum, H., & Tanila, H. (2004). Cognitive aging and the hippocampus: How old rats represent new environments. Journal of Neuroscience, 24(15), 3870-3878.
Wilson, I. A., Ikonen, S., McMahan, R. W., Gallagher, M., Eichenbaum, H., & Tanila, H. (2003). Place cell rigidity correlates with impaired spatial learning in aged rats. Neurobiology of Aging, 24(2), 297-305.
Wilson, D. I., Langston, R. F., Schlesiger, M. I., Wagner, M., Watanabe, S., & Ainge, J. A. (2013). Lateral entorhinal cortex is critical for novel object-context recognition. Hippocampus, 23(5), 352-366.
Wilson, D. I., Watanabe, S., Milner, H., & Ainge, J. A. (2013). Lateral entorhinal cortex is necessary for associative but not nonassociative recognition memory. Hippocampus, 23(12), 1280-1290.
Yassa, M. A., Lacy, J. W., Stark, S. M., Albert, M. S., Gallagher, M., & Stark, C. E. (2011). Pattern separation deficits associated with increased hippocampal CA3 and dentate gyrus activity in nondemented older adults. Hippocampus, 21(9), 968-979.
Yassa, M. A., Mattfeld, A. T., Stark, S. M., & Stark, C. E. (2011). Age-related memory deficits linked to circuit-specific disruptions in the hippocampus. Proceedings of the National Academy of Sciences, 108(21), 8873-8878.