Hostname: page-component-5cf477f64f-rdph2 Total loading time: 0 Render date: 2025-04-05T02:27:01.716Z Has data issue: false hasContentIssue false
  • English
  • Français

The impact of context on pattern separation for objects among younger and older apolipoprotein ϵ4 carriers and noncarriers

Published online by Cambridge University Press:  23 November 2022

Justin M. Palmer Open the ORCID record for Justin M. Palmer [Opens in a new window] ,
Matthew D. Grilli Open the ORCID record for Matthew D. Grilli [Opens in a new window] ,
Ashely V. Lawrence  and
Lee Ryan
Justin M. Palmer
Affiliation:
Department of Psychology, University of Arizona, Tucson, AZ, USA
Matthew D. Grilli
Affiliation:
Department of Psychology, University of Arizona, Tucson, AZ, USA Department of Neurology, University of Arizona, Tucson, AZ, USA McKnight Brain Institute, University of Arizona, Tucson, AZ, USA
Ashely V. Lawrence
Affiliation:
Department of Psychology, University of Arizona, Tucson, AZ, USA
Lee Ryan*
Affiliation:
Department of Psychology, University of Arizona, Tucson, AZ, USA Department of Neurology, University of Arizona, Tucson, AZ, USA McKnight Brain Institute, University of Arizona, Tucson, AZ, USA
*
Corresponding author: Lee Ryan, email: ryant@email.arizona.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective:

On continuous recognition tasks, changing the context objects are embedded in impairs memory. Older adults are worse on pattern separation tasks requiring identification of similar objects compared to younger adults. However, how contexts impact pattern separation in aging is unclear. The apolipoprotein (APOE) ϵ4 allele may exacerbate possible age-related changes due to early, elevated neuropathology. The goal of this study is to determine how context and APOE status affect pattern separation among younger and older adults.

Method:

Older and younger ϵ4 carriers and noncarriers were given a continuous object recognition task. Participants indicated if objects on a Repeated White background, Repeated Scene, or a Novel Scene were old, similar, or new. The proportions of correct responses and the types of errors made were calculated.

Results:

Novel scenes lowered recognition scores compared to all other contexts for everyone. Younger adults outperformed older adults on identifying similar objects. Older adults misidentified similar objects as old more than new, and the repeated scene exacerbated this error. APOE status interacted with scene and age such that in repeated scenes, younger carriers produced less false alarms, and this trend switched for older adults where carriers made more false alarms.

Conclusions:

Context impacted recognition memory in the same way for both age groups. Older adults underutilized details and over relied on holistic information during pattern separation compared to younger adults. The triple interaction in false alarms may indicate an even greater reliance on holistic information among older adults with increased risk for Alzheimer’s disease.

Keywords

recognition memorycontext shiftholisticdetails
Type
Research Article
Information
Journal of the International Neuropsychological Society , Volume 29 , Issue 5 , June 2023 , pp. 439 - 449
Copyright
Copyright © INS. Published by Cambridge University Press, 2022

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albin, R. L. (1993). Antagonistic pleiotropy, mutation accumulation, and human genetic disease. Genetica, 91, 279–286. https://doi.org/10.1007/BF01436004 CrossRefGoogle ScholarPubMed
Amer, T., Wynn, J. S., & Hasher, L. (2022). Cluttered memory representations shape cognition in old age. Trends in Cognitive Sciences, 26(3), 255–267. https://doi.org/10.1016/j.tics.2021.12.002 CrossRefGoogle ScholarPubMed
Bar, M. (2003). A cortical mechanism for triggering top-down facilitation in visual object recognition. Journal of Cognitive Neuroscience, 15, 600–609. https://doi.org/10.1162/089892903321662976 CrossRefGoogle ScholarPubMed
Bar, M. (2004). Visual objects in context. Nature Reviews Neuroscience, 5, 617–629. https://doi.org/10.1038/nrn1476 CrossRefGoogle ScholarPubMed
Bar, M., & Aminoff, E. (2003). Cortical analysis of visual context. Neuron, 38(2), 347–358. https://doi.org/10.1016/s0896-6273(03)00167-3 CrossRefGoogle ScholarPubMed
Bar, M., & Ullman, S. (1996). Spatial context in recognition. Perception, 25(3), 343–352. https://doi.org/10.1068/p250343 CrossRefGoogle ScholarPubMed
Barense, M. D., Gaffan, D., & Graham, K. S. (2007). The human medial temporal lobe processes online representations of complex objects. Neuropsychologia, 45(13), 2963–2974. https://doi.org/10.1016/j.neuropsychologia.'2007.05.023 CrossRefGoogle ScholarPubMed
Barense, M. D., Henson, R. R. A., Lee, A. C. H., & Graham, K. S. (2010). Medial temporal lobe activity during complex discrimination of faces, objects, and scenes: Effects of view point. Hippocampus, 20(3), 389–401. https://doi.org/10.1002/hipo.20641 Google Scholar
Biederman, I. (1981). On the semantic of a glance at a scene. In Kubovy, M., & Pomerantz, J. (Eds.), Perceptual organization (pp. 213–253). Lawrence Erlbaum Associates.Google Scholar
Biss, R. K., Campbell, K. L., & Hasher, L. (2013). Interference from previous distraction disrupts older adults' memory. The Journals of Gerontology. Series B, Psychological Sciences and Social Sciences, 68(4), 558–561. https://doi.org/10.1093/geronb/gbs074 CrossRefGoogle ScholarPubMed
Bloss, C. S., Delis, D. C., Salmon, D. P., & Bondi, M. W. (2010). APOE genotype is associated with left-handedness and visuospatial skills in children. Neurobiology of Aging, 31(5), 787–795. https://doi.org/10.1016/j.neurobiolaging.2008.05.021 CrossRefGoogle ScholarPubMed
Braak, H., Alafuzoff, I., Arzberger, T., Kretzschmar, H., & Del Tredici, K. (2006). Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathologica, 112(4), 389–404. https://doi.org/10.1007/s00401-006-0127-z CrossRefGoogle ScholarPubMed
Burke, S. N., Gaynor, L. S., Barnes, C. A., Bauer, R. M., Bizon, J. L., Roberson, E. D., & Ryan, L. (2018). Shared functions of perirhinal and parahippocampal cortices: Implications for cognitive aging. Trends in Neurosciences, 41(6), 349–359. https://doi.org/10.1016/j.tins.2018.03.001 CrossRefGoogle ScholarPubMed
Camfield, D. A., Fontana, R., Wesnes, K. A., Mills, J., & Croft, R. J. (2018). Effects of aging and depression on mnemonic discrimination ability. Aging, Neuropsychology, and Cognition, 25(3), 464–483. https://doi.org/10.1080/13825585.2017.1325827 CrossRefGoogle ScholarPubMed
Campbell, K. L., & Hasher, L. (2018). Hyper-binding only apparent under fully implicit test conditions. Psychology and Aging, 33(1), 176–181. https://doi.org/10.1037/pag0000216 CrossRefGoogle ScholarPubMed
Campbell, K. L., Hasher, L., & Thomas, R. C. (2010). Hyper-binding: A unique age effect. Psychological science, 21(3), 399–405. https://doi.org/10.1177/0956797609359910 CrossRefGoogle ScholarPubMed
Carr, V. A., Castel, A. D., & Knowlton, B. J. (2015). Age-related differences in memory after attending to distinctiveness or similarity during learning. Neuropsychology, Development, and Cognition. Section B: Aging, Neuropsychology, and Cognition, 22, 155–169. https://doi.org/10.1080/13825585.2014.898735 CrossRefGoogle ScholarPubMed
Craik, F. I. M., & Schloerscheidt, A. M. (2011). Age-related differences in recognition memory: Effects of materials and context change. Psychology and Aging, 26(3), 671–677. https://doi.org/10.1037/a0022203 CrossRefGoogle ScholarPubMed
Davidson, P. S. R., Vidjen, P., Trincao-Batra, S., & Collin, C. A. (2019). Older adults’ lure discrimination difficulties on the mnemonic similarity task are significantly correlated with their visual perception. The Journal of Gerontology: Series B, 74(8), 1298–1307. https://doi.org/10.1093/geronb/gby130 CrossRefGoogle ScholarPubMed
Dennis, N. A., Browndyke, J. N., Stokes, J., Need, A., Burke, J. R., Welsh-Bohmer, K. A., & Cabeza, R. (2010). Temporal lobe functional activity and connectivity in young adult APOE ε4 carriers. Alzheimer’s & Dementia, 6(4), 303–311. https://doi.org/10.1016/j.jalz.2009.07.003 CrossRefGoogle Scholar
Evans, S., Dowell, N. G., Tabet, N., King, S. L., Hutton, S. B., & Rusted, J. M. (2017). Disrupted neural activity patterns to novelty and effort in young adult APOE‐e4 carriers performing a subsequent memory task. Brain and Behavior, 7(2), e00612. https://doi.org/10.1002/brb3.612 CrossRefGoogle ScholarPubMed
Feenan, K., & Snodgrass, J. G. (1990). The effect of context on discrimination and bias in recognition memory for pictures and words. Memory and Cognition, 18(5), 515–527. https://doi.org/10.3758/bf03198484 CrossRefGoogle ScholarPubMed
Fenske, M. J., Aminoff, E., Gronau, N., & Bar, M. (2006). Top-down facilitation of visual object recognition: Object-based and context-based contributions. Progress in Brain Research, 155, 3–21. https://doi.org/10.1016/S0079-6123(06)55001-0 CrossRefGoogle ScholarPubMed
Filbey, F. M., Slack, K. J., Sunderland, T. P., & Cohen, R. M. (2006). Functional magnetic resonance imaging and magnetoencephalography differences associated with APOEϵ4 in young healthy adults. Neuroreport, 17(15), 1585–1590. https://doi.org/10.1097/01.wnr.0000234745.27571.d1 CrossRefGoogle ScholarPubMed
Filippini, N., MacIntosh, B. J., Hough, M. G., Goodwin, G. M., Frisoni, G. B., Smith, S. M., Matthews, P. M., Beckmann, C. F., & Mackay, C. E. (2009). Distinct patterns of brain activity in young carriers of the APOE-ϵ4 allele. Proceedings of the National Academy of Sciences, 106(17), 7209–7214. https://doi.org/10.1073/pnas.0811879106 CrossRefGoogle Scholar
Gutchess, A. H., Hebrank, A., Sutton, B. P., Leshikar, E., Chee, M. W. L., Tan, J. C., Goh, J. O. S., & Park, D. C. (2007). Contextual interference in recognition memory with age. NeuroImage, 35(3), 1338–1347. https://doi.org/10.1016/j.neuroimage.2007.01.043 CrossRefGoogle ScholarPubMed
Han, S. D., & Bondi, M. W. (2008). Revision of the apolipoprotein E compensatory mechanism recruitment hypothesis. Alzheimer’s and Dementia, 4(4), 251–254. https://doi.org/10.1016/j.jalz.2008.02.006 CrossRefGoogle ScholarPubMed
Hasher, L., & Zacks, R. T. (1979). Automatic and effortful processes in memory. Journal of Experimental Psychology, 108(3), 365–388.Google Scholar
Hayes, S. M., Baena, E., Truong, T. K., & Cabeza, R. (2010). Neural mechanisms of context effects on face recognition: Automatic binding and context shift decrements. Journal of Cognitive Neuroscience, 22(11), 2541–2554. https://doi.org/10.1162/jocn.2009.21379 CrossRefGoogle ScholarPubMed
Hayes, S. M., Glisky, E. L., McAllister, C., Greenleaf, J., Ketcham, K., Nadel, L., & Ryan, L. (2005). Contextual enhancement of object recognition is not influenced by aging. Paper presented at the Cognitive Neuroscience Society, New York.Google Scholar
Hayes, S. M., Nadel, L., & Ryan, L. (2007). The effect of scene context on episodic object recognition: Parahippocampal cortex mediates memory encoding and retrieval success. Hippocampus, 17, 873–889. https://doi.org/10.1002/hipo.20319 CrossRefGoogle ScholarPubMed
Ihle, A., Bunce, D., & Kliegel, M. (2012). APOE epsilon4 and cognitive function in early life: A meta-analysis. Neuropsychology, 26, 267–277. https://doi.org/10.1037/a0026769 CrossRefGoogle ScholarPubMed
Kensinger, E. A., & Schacter, D. L. (1999). When true memories suppress false memories: Effects of ageing. Cognitive Neuropsychology, 16(3-5), 399–415.CrossRefGoogle Scholar
Kirwan, C. B., & Stark, C. E. (2007). Overcoming interference: An fMRI investigation of pattern separation in the medial temporal lobe. Learning and Memory, 14, 625–633. https://doi.org/10.1101/lm.663507 CrossRefGoogle ScholarPubMed
Marchant, N. L., King, S. L., Tabet, N., & Rusted, J. M. (2010). Positive effects of cholinergic stimulation favor young APOE e4 carriers. Neuropsychopharmacology, 35(5), 1090–1096. https://doi.org/10.1038/npp.2009.214 CrossRefGoogle Scholar
Marr, D. (1971). Simple memory: A theory for archicortex. Philosophical Transactions of the Royal Society of London: Biological Sciences, 262(841), 23–81. https://doi.org/10.1098/rstb.1971.0078 Google ScholarPubMed
McClelland, J. L., McNaughton, B. L., & O’Reilly, R. C. (1995). Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. Psychological Reviews, 102(3), 419–457. https://doi.org/10.1037/0033-295X.102.3.419 CrossRefGoogle ScholarPubMed
Memel, M., & Ryan, L. (2017). Visual integration enhances associative memory equally for young and older adults without reducing hippocampal encoding activation. Neuropsychologia, 100, 195–206. https://doi.org/10.1016/j.neuropsychologia.2017.04.031 CrossRefGoogle Scholar
Mondadori, C. R. A., de Quervain, D. J. F., Buchmann, A., Mustovic, H., Wollmer, M. A., Schmidt, C. F., Boesiger, P., Hock, C., Nitsch, R. M., Papassotiropoulos, A., & Henke, K. (2007). Better memory and neural efficiency in young apolipoprotein E epsilon4 carriers. Cerebral Cortex, 17, 1934–47. https://doi.org/10.1093/cercor/bhl103 CrossRefGoogle ScholarPubMed
Mormann, F., Simon, K., Cerf, M., Ison, M. J., Kraskov, A., Tran, M., Knieling, S., Quiroga, R. Q., Koch, C., & Fried, I. (2017). Scene-selective coding by single neurons in the human parahippocampal cortex. Proceedings of the National Academy of Sciences of the United States, 114(5), 1153–1158. https://doi.org/10.1073/pnas.1608159113 CrossRefGoogle ScholarPubMed
Norman, K. A., & O’Reilly, R. C. (2003). Modeling hippocampal and neocortical contributions to recognition memory: A complementary-learning-systems approach. Psychological Reviews, 110, 611–646. https://doi.org/10.1037/0033-295X.110.4.611 CrossRefGoogle ScholarPubMed
Palmer, T. E. (1975). The effects of contextual scenes on the identification of objects. Memory & Cognition, 3(5), 519–526. https://doi.org/10.3758/BF03197524 CrossRefGoogle ScholarPubMed
Pidgeon, L. M., & Morcom, A. M. (2014). Age-related increases in false recognition: The role of perceptual and conceptual similarity. Frontiers in Aging Neuroscience, 6(283, https://doi.org/10.3389/fnagi.2014.00283 CrossRefGoogle ScholarPubMed
Racsmány, M., Bencze, D., Pajkossy, P., Szőllősi, Á., & Marián, M. (2021). Irrelevant background context decreases mnemonic discrimination and increases false memory. Scientific Reports, 11(1), 1–7. https://doi.org/10.1038/s41598-021-85627-2 CrossRefGoogle ScholarPubMed
Reagh, Z. M., Ho, H. D., Leal, S. L., Noche, J. A., Chun, A., Murray, E. A., & Yassa, M. A. (2016). Greater loss of object than spatial mnemonic discrimination in aged adults. Hippocampus, 26, 417–422. https://doi.org/10.1002/hipo.22562 CrossRefGoogle ScholarPubMed
Rolls, E. T. (2013). The mechanisms for pattern completion and pattern separation in the hippocampus. Frontiers in Systems Neuroscience, 7, 74. https://doi.org/10.3389/fnsys.2013.00074 CrossRefGoogle ScholarPubMed
Ruiz, J. R., Castillo, R., Labayen, I., Moreno, L. A., Fuentes, M. G., Lamuno, D. G., Granda, J. L. A., Lucia, A., Ortega, F. B., & AVENA Study Group (2010). Individual and combined effects of ApoE and MTHFR 677C/T polymorphisms on cognitive performance in Spanish adolescents: The AVENA study. The Journal of Pediatrics, 156(6), 978–984. https://doi.org/10.1016/j.jpeds.2009.12.018 CrossRefGoogle ScholarPubMed
Rusted, J. M., Evans, S. L., King, S. L., Dowell, N., Tabet, N., & Tofts, P. S. (2013). APOE e4 polymorphism in young adults is associated with improved attention and indexed by distinct neural signatures. NeuroImage, 65, 364–373. https://doi.org/10.1016/j.neuroimage.2012.10.010 CrossRefGoogle ScholarPubMed
Ryan, L., Cardoza, J. A., Barense, M. D., Kawa, K. H., Wallentin‐Flores, J., Arnold, W. T., & Alexander, G. E. (2012). Age‐related impairment in a complex object discrimination task that engages perirhinal cortex. Hippocampus, 22(10), 1978–1989. https://doi.org/10.1002/hipo.22069 CrossRefGoogle Scholar
Selkoe, D. J. (2001). Alzheimer’s disease: Genes, proteins, and therapy. Physiological Reviews, 81(2), 741–766. https://doi.org/10.1152/physrev.2001.81.2.741 CrossRefGoogle ScholarPubMed
Stark, S. M., & Stark, C. E. L. (2017). Age-related deficits in the mnemonic similarity task for objects and scenes. Behavioural Brain Research, 333, 109–117. https://doi.org/10.1016/j.bbr.2017.06.049 CrossRefGoogle ScholarPubMed
Stark, S. M., Stevenson, R., Wu, C., Rutledge, S., & Stark, C. E. (2015). Stability of age-related deficits in the mnemonic similarity task across task variations. Behavioral Neuroscience, 129(3), 257–268. https://doi.org/10.1037/bne0000055 CrossRefGoogle ScholarPubMed
Stark, S. M., Yassa, M. A., Lacy, J. W., & Stark, C. E. (2013). A task to assess behavioral pattern separation (BPS) in humans: Data from healthy aging and mild cognitive impairment. Neuropsychologia, 51(12), 2442–2449. https://doi.org/10.1016/j.neuropsychologia.2012.12.014 CrossRefGoogle ScholarPubMed
Toner, C. K., Pirogovsky, E., Kirwan, B., & Gilbert, P. E. (2009). Visual object pattern separation deficits in nondemented older adults. Learning and Memory, 16, 338–342. https://doi.org/10.1101/lm.1315109 CrossRefGoogle ScholarPubMed
Tuminello, E. R., & Han, S. D. (2011). The apolipoprotein E antagonistic pleiotropy hypothesis: Review and recommendations. International Journal of Alzheimer’s Disease, 2011(5), 1–12. https://doi.org/10.4061/2011/726197 CrossRefGoogle ScholarPubMed
Weissberger, G. H., Nation, D. A., Nguyen, C. P., Bondi, M. W., & Han, S. D. (2018). Meta-analysis of cognitive ability differences by apolipoprotein e genotype in young humans. Neuroscience & Biobehavioral Reviews, 94, 49–58. https://doi.org/10.1016/j.neubiorev.2018.08.009 CrossRefGoogle ScholarPubMed
Williams, G. C. (1957). Pleiotropy, natural selection, and the evolution of senescence: Evolution 11, 398-411 (1957). Science of Aging Knowledge Environment, 2001(1), cp13.Google Scholar
Wilson, I. A., Gallagher, M., Eichenbaum, H., & Tanila, H. (2006). Neurocognitive aging: Prior memories hinder new hippocampal encoding. Trends in Neuroscience, 29(12), 662–670. https://doi.org/10.1016/j.tins.2006.10.002 CrossRefGoogle ScholarPubMed
Yassa, M. A., Lacy, J. W., Stark, S. M., Albert, M. S., Gallagher, M., & Stark, C. E. L. (2011). Pattern separation deficits associated with increased hippocampal CA3 and dentate gyrus activity in nondemented older adults. Hippocampus, 21, 968–979. https://doi.org/10.1002/hipo.20808 Google ScholarPubMed
Yassa, M. A., & Stark, C. E. (2011). Pattern separation in the hippocampus. Trends in Neurosciences, 34(10), 515–525. https://doi.org/10.1016/j.tins.2011.06.006 CrossRefGoogle ScholarPubMed