Pattern separation deficits associated with increased hippocampal CA3 and dentate gyrus activity in nondemented older adults
Open accessAbstract
There is widespread evidence that memory deteriorates with aging, however the exact mechanisms that underlie these changes are not well understood. Given the growing size of the aging population, there is an imperative to study age‐related neurocognitive changes in order to better parse healthy from pathological aging. Using a behavioral paradigm that taxes pattern separation (the ability to differentiate novel yet similar information from previously learned information and thus avoid interference), we investigated age‐related neural changes in the human hippocampus using high‐resolution (1.5 mm isotropic) blood‐oxygenation level‐dependent fMRI. Recent evidence from animal studies suggests that hyperactivity in the CA3 region of the hippocampus may underlie behavioral deficits in pattern separation in aged rats. Here, we report evidence that is consistent with findings from the animal studies. We found a behavioral impairment in pattern separation in a sample of healthy older adults compared with young controls. We also found a related increase in CA3/dentate gyrus activity levels during an fMRI contrast that stresses pattern separation abilities. In a detailed analysis of behavior, we also found that the pattern of impairment was consistent with the predictions of the animal model, where larger changes in the input (greater dissimilarity) were required in order for elderly adults to successfully encode new information as distinct from previously learned information. These findings are also consistent with recent fMRI and behavioral reports in healthy aging, and further suggest that a specific functional deficit in the CA3/dentate network contributes to memory difficulties with aging. © 2010 Wiley‐Liss, Inc.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Greater hippocampal activation during encoding tasks is associated with worse task performance in MCI and AD patients.
“Greater hippocampal activation during encoding tasks is associated with worse task performance [176] in MCI and AD patients [172, 177]”
From Apolipoprotein E4, inhibitory network dysfunction, and Alzheimer’s disease (2019) · cites this paper as [176]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages
Cox, R. W. (1996) · Computers and Biomedical Research · doi:10.1006/cbmr.1996.0014 · Cited by 10,913 · 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
Regional Brain Changes in Aging Healthy Adults: General Trends, Individual Differences and Modifiers
Raz, N., Lindenberger, U., Rodrigue, K. M., Kennedy, K. M., Head, D., Williamson, A., Dahle, C., Gerstorf, D., & Acker, J. D. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi044 · Cited by 2,875 · see citing works
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
Self-citationTHE AMYGDALA MODULATES THE CONSOLIDATION OF MEMORIES OF EMOTIONALLY AROUSING EXPERIENCES
McGaugh, J. L. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144157 · Cited by 2,296 · see citing works
Insights into the ageing mind: a view from cognitive neuroscience
Hedden, T., & Gabrieli, J. D. E. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1323 · Cited by 2,223 · see citing works
The role of acetylcholine in learning and memory
Hasselmo, M. E. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.09.002 · Cited by 1,693 · see citing works
Pattern Separation in the Dentate Gyrus and CA3 of the Hippocampus
Leutgeb, J. K., Leutgeb, S., Moser, M.-B., & Moser, E. I. (2007) · Science · doi:10.1126/science.1135801 · Cited by 1,601 · cited 1× · see citing works
“Although both regions are thought to play a role in pattern separation, recent evidence from rodent studies suggests that the mechanisms are different (Leutgeb et al., 2007) and that the dentate is the primary source of separation signals when changes in the input are small.”
BackgroundNeural plasticity in the ageing brain
Burke, S. N., & Barnes, C. A. (2005) · Nature reviews. Neuroscience · doi:10.1038/nrn1809 · Cited by 1,600 · see citing works
Telephone Interview for Cognitive Status
Brandt, J., Spencer, M., & Folstein, M. F. (1988) · PsycTESTS Dataset · doi:10.1037/t28542-000 · Cited by 1,504 · see citing works
Patterns of Brain Activation in People at Risk for Alzheimer's Disease
Bookheimer, S. Y., Strojwas, M. H., Cohen, M. S., Saunders, A. M., Pericak-Vance, M. A., Mazziotta, J. C., & Small, G. W. (2000) · New England Journal of Medicine · doi:10.1056/nejm200008173430701 · Cited by 1,328 · see citing works
Norman, K. A., & O'Reilly, R. C. (2003) · Psychological Review · doi:10.1037/0033-295x.110.4.611 · Cited by 1,312 · see citing works
Cognitive Neuroscience and the Study of Memory
Milner, B. A., Squire, L. R., & Kandel, E. R. (1998) · Neuron · doi:10.1016/s0896-6273(00)80987-3 · Cited by 1,300 · see citing works
Calibrated functional MRI: Mapping the dynamics of oxidative metabolism
Davis, T. L., Kwong, K. K., Weisskoff, R. M., & Rosen, B. R. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.4.1834 · Cited by 1,054 · see citing works
Pattern Separation in the Human Hippocampal CA3 and Dentate Gyrus
Bakker, A., Kirwan, C. B., Miller, M. I., & Stark, C. E. L. (2008) · Science · doi:10.1126/science.1152882 · Cited by 1,050 · see citing works
Self-citationDentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network
McHugh, T. J., Jones, M. W., Quinn, J. J., Balthasar, N., Coppari, R., Elmquist, J. K., Lowell, B. B., Fanselow, M. S., Wilson, M. A., & Tonegawa, S. (2007) · Science · doi:10.1126/science.1140263 · Cited by 958 · see citing works
Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD
Dickerson, B. C., Salat, D. H., Greve, D. N., Chua, E. F., Rand-Giovannetti, E., Rentz, D. M., Bertram, L., Mullin, K., Tanzi, R. E., Blacker, D., et al. (2005) · Neurology · doi:10.1212/01.wnl.0000171450.97464.49 · Cited by 910 · see citing works
Self-citationCabeza, R. E. L. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhg133 · Cited by 781 · see citing works
Distinct Ensemble Codes in Hippocampal Areas CA3 and CA1
Leutgeb, S., Leutgeb, J. K., Treves, A., Moser, M., & Moser, E. I. (2004) · Science · doi:10.1126/science.1100265 · Cited by 774 · see citing works
Celone, K., Calhoun, V. D., Dickerson, B. C., Atri, A., Chua, E. F., Miller, S. L., DePeau, K. M., Rentz, D., Selkoe, D. J., Blacker, D., et al. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2250-06.2006 · Cited by 733 · see citing works
Self-citationRegionally specific loss of neurons in the aging human hippocampus.
West, M. (1993) · Neurobiology of Aging · doi:10.1016/0197-4580(93)90113-p · Cited by 638 · see citing works
Medial temporal lobe function and structure in mild cognitive impairment
Dickerson, B. C., Salat, D. H., Bates, J. F., Atiya, M., Killiany, R., Greve, D. N., Dale, A. M., Stern, C. E., Blacker, D., Albert, M., et al. (2004) · Annals of Neurology · doi:10.1002/ana.20163 · Cited by 561 · see citing works
Self-citationGist-Based False Recognition of Pictures in Older and Younger Adults
Koutstaal, W., & Schacter, D. L. (1997) · Journal of Memory and Language · doi:10.1006/jmla.1997.2529 · Cited by 521 · 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
Hasselmo, M. E., Schnell, E., & Barkai, E. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-07-05249.1995 · Cited by 463 · see citing works
Introduction to functional magnetic resonance imaging principles and techniques
Buxton, R. B. (2003) · Cited by 448 · see citing works
Smith, T. D., Adams, M., Gallagher, M., Morrison, J., & Rapp, P. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-17-06587.2000 · Cited by 404 · see citing works
Self-citationEffects of Healthy Aging on Hippocampal and Rhinal Memory Functions: An Event-Related fMRI Study
Daselaar, S. M., Fleck, M. S., Dobbins, I. G., Madden, D. J., & Cabeza, R. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhj112 · Cited by 392 · see citing works
Miller, S. L., Celone, K., DePeau, K. M., Diamond, E. L., Dickerson, B. C., Rentz, D. M., Pihlajamaki, M. M., & Sperling, R. A. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706818105 · Cited by 380 · see citing works
Overcoming interference: An fMRI investigation of pattern separation in the medial temporal lobePreprint
Kirwan, C. B., & Stark, C. E. L. (2007) · Learning & Memory · doi:10.1101/lm.663507 · Cited by 361 · see citing works
Self-citationO'Reilly, R. C., & Norman, K. A. (2002) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(02)02005-3 · Cited by 351 · see citing works
Neurocognitive aging: prior memories hinder new hippocampal encoding
Wilson, I. A., Gallagher, M., Eichenbaum, H., & Tanila, H. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.10.002 · Cited by 343 · see citing works
Self-citationEffects of aging on the neural correlates of successful item and source memory encoding.
Dennis, N. A., Hayes, S. M., Prince, S. E., Madden, D. J., Huettel, S. A., & Cabeza, R. E. L. (2008) · Journal of Experimental Psychology Learning Memory and Cognition · doi:10.1037/0278-7393.34.4.791 · Cited by 315 · see citing works
Aging and source monitoring: Cognitive processes and neuropsychological correlates.
Henkel, L. A., Johnson, M. K., & Leonardis, D. M. D. (1998) · Journal of Experimental Psychology General · doi:10.1037/0096-3445.127.3.251 · Cited by 302 · see citing works
Jennings, J. M., & Jacoby, L. L. (1997) · Psychology and Aging · doi:10.1037//0882-7974.12.2.352 · Cited by 286 · see citing works
Small, S. A., Chawla, M. K., Buonocore, M. H., Rapp, P. R., & Barnes, C. A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400285101 · Cited by 281 · see citing works
Age-Associated Alterations of Hippocampal Place Cells Are Subregion Specific
Wilson, I. A., Ikonen, S., Gallagher, M., Eichenbaum, H., & Tanila, H. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1744-05.2005 · Cited by 278 · see citing works
Self-citationGeinisman, Y., de Toledo-Morrell, L., Morrell, F., Persina, I. S., & Rossi, M. (1992) · Hippocampus · doi:10.1002/hipo.450020411 · Cited by 264 · see citing works
Yassa, M. A., & Stark, C. E. L. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.09.016 · Cited by 252 · see citing works
Self-citationVisual object pattern separation deficits in nondemented older adultsPreprint
Toner, C. K., Pirogovsky, E., Kirwan, C. B., & Gilbert, P. E. (2009) · Learning & Memory · doi:10.1101/lm.1315109 · Cited by 245 · see citing works
Miller, S. L., Fenstermacher, E., Bates, J., Blacker, D., Sperling, R. A., & Dickerson, B. C. (2007) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.2007.124149 · Cited by 241 · see citing works
A Double Dissociation between Hippocampal Subfields
Lee, I., Rao, G., & Knierim, J. J. (2004) · Neuron · doi:10.1016/j.neuron.2004.05.010 · Cited by 236 · see citing works
Sperling, R. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1379.009 · Cited by 236 · see citing works
Neural Processes Supporting Young and Older Adults' Emotional Memories
Kensinger, E., & Schacter, D. (2008) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2008.20080 · Cited by 233 · see citing works
Stark, C. E. L., & Okado, Y. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-17-06748.2003 · Cited by 220 · see citing works
Self-citationAnces, B. M., Liang, C. L., Leontiev, O., Perthen, J. E., Fleisher, A., Lansing, A. E., & Buxton, R. B. (2008) · Human Brain Mapping · doi:10.1002/hbm.20574 · Cited by 216 · see citing works
Age-related changes in Arc transcription and DNA methylation within the hippocampus
Penner, M. R., Roth, T. L., Chawla, M. K., Hoang, L. T., Roth, E. D., Lubin, F. D., Sweatt, J. D., Worley, P. F., & Barnes, C. A. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.01.009 · Cited by 215 · see citing works
Jennings, J. M., & Jacoby, L. L. (1997) · Psychology and Aging · doi:10.1037/0882-7974.12.2.352 · Cited by 211 · see citing works
Imaging hippocampal function across the human life span: Is memory decline normal or not?
Small, S. A., Tsai, W. Y., DeLaPaz, R., Mayeux, R., & Stern, Y. (2002) · Annals of Neurology · doi:10.1002/ana.10105 · Cited by 205 · see citing works
Senescent synapses and hippocampal circuit dynamics
Burke, S. N., & Barnes, C. A. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2009.12.003 · Cited by 199 · see citing works
Cerebral perfusion and oxygenation differences in Alzheimer's disease risk
Fleisher, A., Podraza, K. M., Bangen, K. J., Taylor, C. S., Sherzai, A. Z., Sidhar, K., Liu, T. T., Dale, A. M., & Buxton, R. B. (2008) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2008.01.012 · Cited by 182 · see citing works
Gazzaley, A. H., Siegel, S. J., Kordower, J. H., Mufson, E. J., & Morrison, J. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.7.3121 · Cited by 177 · see citing works
Miller, M. I., Beg, M. F., Ceritoglu, C., & Stark, C. E. L. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503892102 · Cited by 173 · see citing works
Self-citationFamilial risk for Alzheimer's disease alters fMRI activation patterns
Bassett, S. S., Yousem, D. M., Cristinzio, C., Kusevic, I., Yassa, M. A., Caffo, B. S., & Zeger, S. L. (2006) · Brain · doi:10.1093/brain/awl089 · Cited by 171 · see citing works
Self-citationKruse, N., Persson, S., Alcolea, D. A., Bahl, J., Baldeiras, I., Capello, E., Chiasserini, D., Emeršič, A., Engelborghs, S., Eren, E., et al. (2015) · IRIS eCampus Telematic University (Università degli Studi eCampus) · doi:10.1016/j.neurobiolaging · Cited by 154 · see citing works
The neural origins of specific and general memory: the role of the fusiform cortex
Garoff-Eaton, R. J., Slotnick, S. D., & Schacter, D. L. (2004) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2004.09.014 · Cited by 150 · see citing works
Age-related Changes in Object Processing and Contextual Binding Revealed Using fMR Adaptation
Chee, M. W. L., Goh, J. O. S., Venkatraman, V., Tan, J. C., Gutchess, A. H., Sutton, B. P., Hebrank, A., Leshikar, E. D., & Park, D. C. (2006) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2006.18.4.495 · Cited by 149 · see citing works
Cacucci, F., Yi, M., Wills, T. J., Chapman, P. F., & O'Keefe, J. M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802908105 · Cited by 142 · see citing works
Spatial Memory and Aging: Performance on a Human Analog of the Morris Water Maze
Newman, M. C., & Kaszniak, A. W. (2000) · Aging Neuropsychology and Cognition · doi:10.1076/1382-5585(200006)7:2;1-u;ft086 · Cited by 138 · see citing works
High‐resolution fMRI investigation of the medial temporal lobe
Kirwan, C. B., Jones, C. K., Miller, M. I., & Stark, C. E. L. (2006) · Human Brain Mapping · doi:10.1002/hbm.20331 · Cited by 127 · see citing works
Self-citationPlace cell rigidity correlates with impaired spatial learning in aged rats
Wilson, I. A., Ikonen, S., McMahan, R. W., Gallagher, M., Eichenbaum, H., & Tanila, H. (2002) · Neurobiology of Aging · doi:10.1016/s0197-4580(02)00080-5 · Cited by 112 · see citing works
Self-citationAge-related Alterations in Simple Declarative Memory and the Effect of Negative Stimulus Valence
Murty, V. P., Sambataro, F., Das, S. B., Tan, H., Callicott, J., Goldberg, T., Meyer-Lindenberg, A., Weinberger, D., & Mattay, V. (2009) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21130 · Cited by 106 · see citing works
Hedden, T., & Gabrieli, J. D. E. (2005) · Current Opinion in Neurology · doi:10.1097/01.wco.0000189875.29852.48 · Cited by 91 · see citing works
Nicolle, M. M., Colombo, P. J., Gallagher, M., & McKinney, M. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-21-09604.1999 · Cited by 87 · see citing works
Self-citationImaging the Aβ-Related Neurotoxicity of Alzheimer Disease
Moreno, H., Wu, W. E., Lee, T., Brickman, A. M., Mayeux, R. P., Brown, T. R., & Small, S. A. (2007) · Archives of Neurology · doi:10.1001/archneur.64.10.1467 · Cited by 82 · see citing works
Hippocampal and neocortical activation during repetitive encoding in older persons
Rand‐Giovannetti, E., Chua, E. F., Driscoll, A. E., Schacter, D. L., Albert, M., & Sperling, R. A. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2004.12.013 · Cited by 80 · see citing works
Self-citationSepto-hippocampal cholinergic and neurotrophin markers in age-induced cognitive decline
Sugaya, K., Greene, R., Personett, D. A., Robbins, M., Kent, C., Bryan, D., Skiba, E., Gallagher, M., & McKinney, M. (1998) · Neurobiology of Aging · doi:10.1016/s0197-4580(98)00072-4 · Cited by 74 · see citing works
Self-citationThe Nature of Subjective Cognitive Complaints of Older Adults
Newson, R. S., & Kemps, E. (2006) · The International Journal of Aging and Human Development · doi:10.2190/1eap-fe20-pdwy-m6p1 · Cited by 65 · see citing works
Effects of Age on the Neural Correlates of Retrieval Cue Processing are Modulated by Task Demands
Duverne, S., Motamedinia, S., & Rugg, M. D. (2008) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21001 · Cited by 63 · see citing works
Introduction to Functional Magnetic Resonance Imaging, Principles and Techniques
Rossitti, S. (2002) · Acta Radiologica · doi:10.1258/rsmacta.43.5.547a · Cited by 30 · see citing works
Place cells of aged rats in two visually identical compartments
Wilson, I. A., Ikonen, S., Gurevicius, K., McMahan, R. W., Gallagher, M., Eichenbaum, H., & Tanila, H. (2004) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2004.09.006 · Cited by 20 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 2
- Small SA Perera GM DeLaPaz R Mayeux R Stern Y 1999 Differential regional dysfunction of the hippocampal formation among elderly with memory decline and Alzheimer's disease Ann Neurol 45 466 472 10211471
- Talairach J Tournoux P 1988 A Co-Planar Steres Jotactic Atlas of the Human Brain Stuttgard, Germany Thieme
Cited by
Sorted by citations
Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation
Sahay, A., Scobie, K. N., Hill, A. S., O'Carroll, C. M., Kheirbek, M. A., Burghardt, N. S., Fenton, A. A., Dranovsky, A., & Hen, R. (2011) · Nature · doi:10.1038/nature09817 · Cited by 1,567 · see citing works
Pattern separation in the hippocampus
Yassa, M. A., & Stark, C. E. L. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.06.006 · Cited by 1,544 · see citing works
Self-citationEpisodic memory and beyond: the hippocampus and neocortex in transformation
Moscovitch, M., Cabeza, R., Winocur, G., & Nadel, L. (2016) · Annual Review of Psychology · doi:10.1146/annurev-psych-113011-143733 · Cited by 1,062 · see citing works
The role of adult hippocampal neurogenesis in brain health and disease
Toda, T., Parylak, S. L., Linker, S. B., & Gage, F. H. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0036-2 · Cited by 719 · see citing works
Pattern separation: a common function for new neurons in hippocampus and olfactory bulb
Sahay, A., Wilson, D. A., & Hen, R. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.012 · Cited by 514 · see citing works
Nutrition for the ageing brain: Towards evidence for an optimal diet
Vauzour, D., Camprubi-Robles, M., Miquel-Kergoat, S., Andres-Lacueva, C., Bánáti, D., Barberger-Gateau, P., Bowman, G. L., Caberlotto, L., Clarke, R., Hogervorst, E., et al. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2016.09.010 · Cited by 241 · see citing works
Exercise and Hippocampal Memory Systems
Voss, M. W., Soto, C., Yoo, S., Sodoma, M., Vivar, C., & van Praag, H. (2019) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2019.01.006 · Cited by 235 · see citing works
Apolipoprotein E4, inhibitory network dysfunction, and Alzheimer’s disease
Najm, R., Jones, E. A., & Huang, Y. (2019) · Molecular Neurodegeneration · doi:10.1186/s13024-019-0324-6 · Cited by 183 · see citing works
False memories with age: neural and cognitive underpinnings
Devitt, A. L., & Schacter, D. L. (2016) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2016.08.030 · Cited by 171 · see citing works
Yassa, M. A., Hazlett, R. L., Stark, C. E. L., & Hoehn-Saric, R. (2012) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2012.04.013 · Cited by 155 · see citing works
Self-citationHippocampal activation is associated with longitudinal amyloid accumulation and cognitive decline
Leal, S. L., Landau, S. M., Bell, R. K., & Jagust, W. J. (2017) · eLife · doi:10.7554/elife.22978 · Cited by 117 · see citing works
Hernandez, A. R., Hernandez, C. M., Campos, K., Truckenbrod, L., Federico, Q., Moon, B., McQuail, J. A., Maurer, A. P., Bizon, J. L., & Burke, S. N. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00391 · Cited by 111 · see citing works
Kent, B. A., Beynon, A. L., Hornsby, A. K. E., Bekinschtein, P., Bussey, T. J., Davies, J. S., & Saksida, L. M. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.10.015 · Cited by 94 · see citing works
Building up and wearing down episodic memory: mnemonic discrimination and relational binding
Ngo, C. T., Lin, Y., Newcombe, N. S., & Olson, I. R. (2019) · Journal of Experimental Psychology General · doi:10.1037/xge0000583 · Cited by 65 · see citing works
Sleep in humans stabilizes pattern separation performance
Hanert, A., Weber, F. D., Pedersen, A., Born, J., & Bartsch, T. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.1189-17.2017 · Cited by 52 · see citing works
Masterson, T. D., Kirwan, C. B., Davidson, L. E., & LeCheminant, J. D. (2016) · Brain Imaging and Behavior · doi:10.1007/s11682-015-9366-8 · Cited by 33 · see citing works
Callow, D. D., Won, J., Pena, G. S., Jordan, L. S., Arnold-Nedimala, N. A., Kommula, Y., Nielson, K. A., & Smith, J. C. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.645258 · Cited by 27 · see citing works
- Authors
- Yassa, M. A., Lacy, J. W., Stark, S. M., Albert, M. S., Gallagher, M., & Stark, C. E. L.
- Affiliations
- University of California, Irvine (US)
- Johns Hopkins University (US)
- Corresponding author
- Stark, Craig E.L.
- ORCID
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2011-08-23
- Volume
- 21
- Issue
- 9
- Pages
- 968-979
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- PMC
- PMC3010452
- OpenAlex
- W2067065650
- Cited by
- 595
- References
- 72
- Citations by year
- 2026: 32 · 2025: 44 · 2024: 49 · 2023: 39 · 2022: 30 · 2021: 54 · 2020: 40 · 2019: 38 · 2018: 53 · 2017: 48 · 2016: 29 · 2015: 44 · 2014: 28 · 2013: 28 · 2012: 22
- FWCI
- 12.38
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Aging (2 P01 AG09973, P50AG005146, P01AG009973, P50AG05146)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Functions and Memory
- Keywords
- pattern separation, hippocampal CA3, dentate gyrus, healthy aging, age-related memory decline, hippocampal hyperactivity, older adults, neural correlates of memory
- MeSH terms
- Adolescent, Adult, Aged, Aged, 80 and over, Aging, Animals, Brain Mapping, Discrimination, Psychological, Female, Humans, Magnetic Resonance Imaging, Male, Memory, Models, Biological, Nerve Net, Oxygen, Pattern Recognition, Visual, Reaction Time, Temporal Lobe, Transfer, Psychology, Dentate Gyrus, Rats, CA3 Region, Hippocampal
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review