Age-related differences in the temporal dynamics of spectral power during memory encoding

Autoři: M. Karl Healey aff001;  Michael J. Kahana aff002
Působiště autorů: Department of Psychology, Michigan State University, East Lansing, MI, United States of America aff001;  Department of Psychology, University of Pennsylvania, Philadelphia, PA, United States of America aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article


We examined oscillatory power in electroencephalographic recordings obtained while younger (18-30 years) and older (60+ years) adults studied lists of words for later recall. Power changed in a highly consistent way from word-to-word across the study period. Above 14 Hz, there were virtually no age differences in these neural gradients. But gradients below 14 Hz reliably discriminated between age groups. Older adults with the best memory performance showed the largest departures from the younger adult pattern of neural activity. These results suggest that age differences in the dynamics of neural activity across an encoding period reflect changes in cognitive processing that may compensate for age-related decline.

Klíčová slova:

Age groups – Cognition – Cognitive impairment – Elderly – Electroencephalography – Memory – Memory recall – Scalp


1. Newson RS, Kemps EB. The nature of subjective cognitive complaints of older adults. International Journal of Aging Human Development. 2006;63(2):139–151. doi: 10.2190/1EAP-FE20-PDWY-M6P1 17137031

2. Werkle-Bergner M, Freunberger R, Sander MC, Lindenberger U, Klimesch W. Inter-individual performance differences in younger and older adults differentially relate to amplitude modulations and phase stability of oscillations controlling working memory contents. NeuroImage. 2012;60(1):71–82. doi: 10.1016/j.neuroimage.2011.11.071 22178810

3. Stark SM, Yassa MA, Stark CEL. Individual differences in spatial pattern separation performance associated with healthy aging in humans. Learning & Memory. 2010;17(6):284–288. doi: 10.1101/lm.1768110

4. Healey MK, Kahana MJ. A Four–Component Model of Age–Related Memory Change. Psychological Review. 2016;123(1):23–69. doi: 10.1037/rev0000015 26501233

5. Tulving E, Rosenbaum RS. What do explanations of the distinctiveness effect need to explain? In: Hunt RR, Worthen JB, editors. Distinctiveness and Memory. New York, NY: Oxford University Press; 2006. p. 407–423.

6. Naveh-Benjamin M. Adult-Age Differences in Memory Performance: Tests of an Associative Deficit Hypothesis. Journal of Experimental Psychology: Learning, Memory, and Cognition. 2000;26:1170–1187. doi: 10.1037//0278-7393.26.5.1170 11009251

7. Hasher L, Zacks RT. Working memory, comprehension, and aging: A review and a new view. In: Bower GH, editor. The psychology of learning and motivation: Advances in research and theory. San Diego: Academic Press; 1988. p. 193–225.

8. Benjamin AS. Representational Explanations of “Process” Dissociations in Recognition: The DRYAD Theory of Aging and Memory Judgments. Psychological Review. 2010;117(4):1055–1079. doi: 10.1037/a0020810 20822289

9. Healey MK, Kahana MJ. Age-Related Changes in the Dynamics of Memory Encoding Processes Provide a Biomarker of Successful Aging. Submitted. Submitted;.

10. Ward G, Maylor EA. Age-related deficits in free recall: The role of rehearsal. Quarterly Journal Of Experimental Psychology. 2005;58A(1):98–119. doi: 10.1080/02724980443000223

11. Pergola G, Danet L, Pitel AL, Carlesimo GA, Segobin S, Pariente J, et al. The regulatory role of the human mediodorsal thalamus. Trends in cognitive sciences. 2018;22(11):1011–1025. doi: 10.1016/j.tics.2018.08.006 30236489

12. Katzman R, Brown T, Fuld P, Peck A, Schechter R, Schimmel H. Validation of a short Orientation-Memory-Concentration Test of cognitive impairment. The American Journal of Psychiatry. 1983;140(6):734–739. doi: 10.1176/ajp.140.6.734 6846631

13. Steyvers M, Shiffrin RM, Nelson DL. Word association spaces for predicting semantic similarity effects in episodic memory. In: Healy AF, editor. Cognitive Psychology and its Applications: Festschrift in Honor of Lyle Bourne, Walter Kintsch, and Thomas Landauer. Washington, DC: American Psychological Association; 2004.

14. Healey MK, Long NM, Kahana MJ. Contiguity in Episodic Memory. Psychonomic Bulletin & Review. 2019;.

15. Bell AJ, Sejnowski TJ. An information-maximization approach to blind separation and blind deconvolution. Neural Computation. 1995;7(6):1129–1159. doi: 10.1162/neco.1995.7.6.1129 7584893

16. Nolan H, Whelan R, Reilly R. FASTER: fully automated statistical thresholding for EEG artifact rejection. Journal of neuroscience methods. 2010;192(1):152–162. doi: 10.1016/j.jneumeth.2010.07.015 20654646

17. Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics. Journal of Neuroscience Methods. 2004;134:9–21. doi: 10.1016/j.jneumeth.2003.10.009 15102499

18. Onton J, Makeig S. Information-based modeling of event-related brain dynamics. Progress in brain research. 2006;159:99–120. doi: 10.1016/S0079-6123(06)59007-7 17071226

19. Long NM, Kahana MJ. Modulation of task demands suggests that semantic processing interferes with the formation of episodic associations. Journal of Experimental Psychology: Learning, Memory, and Cognition. 2017;43(2):167–176. doi: 10.1037/xlm0000300 27617775

20. Nyhus E, Curran T. Functional role of gamma and theta oscillations in episodic memory. Neuroscience & Biobehavioral Reviews. 2010;34(7):1023–1035. doi: 10.1016/j.neubiorev.2009.12.014

21. Sederberg PB, Gauthier LV, Terushkin V, Miller JF, Barnathan JA, Kahana MJ. Oscillatory correlates of the primacy effect in episodic memory. NeuroImage. 2006;32(3):1422–1431. doi: 10.1016/j.neuroimage.2006.04.223 16814568

22. Weidemann CT, Mollison MV, Kahana MJ. Electrophysiological correlates of high-level perception during spatial navigation. Psychonomic Bulletin & Review. 2009;16(2):313–319. doi: 10.3758/PBR.16.2.313

23. Curran T, Friedman W. ERP old/new effects at different retention intervals in recency discrimination tasks. 2004;8:107–120.

24. Kahana MJ, Howard MW, Zaromb F, Wingfield A. Age dissociates recency and lag recency effects in free recall. Journal of Experimental Psychology: Learning, Memory, and Cognition. 2002;28:530–540. doi: 10.1037//0278-7393.28.3.530 12018505

25. Wahlheim CN, Huff MJ. Age differences in the focus of retrieval: Evidence from dual-list free recall. Psychology and Aging. 2015;30(4):768. doi: 10.1037/pag0000049 26322551

26. Polyn SM, McCluey JD, Morton NW, Woolard AA, Luksik AS, Heckers S. Temporal context and the organisational impairment of memory search in schizophrenia. Cognitive neuropsychiatry. 2015;20(4):296–310. doi: 10.1080/13546805.2015.1031372 25861879

27. Pajkossy P, Keresztes A, Racsmány M. The interplay of trait worry and trait anxiety in determining episodic retrieval: The role of cognitive control. The Quarterly Journal of Experimental Psychology. 2017;70(11):2234–2250. doi: 10.1080/17470218.2016.1230142 27603582

28. Gibson BS, Healey MK, Gondoli DM. Modeling the Effect of Attention-Deficit Hyperactivity Disorder on Episodic Memory. Journal of Abnormal Psychology. 2019;.

29. Sahakyan L, Kwapil TR. Moving Beyond Summary Scores: Decomposing Free Recall Performance to Understand Episodic Memory Deficits in Schizotypy. Journal of Experimental Psychology: General. 2018;Advance online publication. doi: 10.1037/xge0000401

30. Healey MK, Crutchley P, Kahana MJ. Individual differences in memory search and their relation to intelligence. Journal of Experimental Psychology: General. 2014;143(4):1553–1569. doi: 10.1037/a0036306

31. Sederberg PB, Miller JF, Howard WH, Kahana MJ. The temporal contiguity effect predicts episodic memory performance. Memory & Cognition. 2010;38(6):689–699. doi: 10.3758/MC.38.6.689

32. Spillers GJ, Unsworth N. Variation in working memory capacity and temporal–contextual retrieval from episodic memory. Journal Experimental Psychology: Learning, Memory and Cognition. 2011;37(6):1532–1539.

33. Caplan JB, Bottomley M, Kang P, Dixon RA. Distinguishing rhythmic from non-rhythmic brain activity during rest in healthy neurocognitive aging. NeuroImage. 2015;112:341–352. doi: 10.1016/j.neuroimage.2015.03.001 25769279

34. Sander MC, Werkle-Bergner M, Lindenberger U. Amplitude modulations and inter-trial phase stability of alpha-oscillations differentially reflect working memory constraints across the lifespan. NeuroImage. 2012;59(1):646–654. doi: 10.1016/j.neuroimage.2011.06.092 21763439

35. Roca-Stappung M, Fernández T, Becerra J, Mendoza-Montoya O, Espino M, Harmony T. Healthy aging: relationship between quantitative electroencephalogram and cognition. Neuroscience letters. 2012;510(2):115–120. doi: 10.1016/j.neulet.2012.01.015 22266305

36. Voytek B, Kramer MA, Case J, Lepage KQ, Tempesta ZR, Knight RT, et al. Age-Related Changes in 1/f Neural Electrophysiological Noise. The Journal of Neuroscience. 2015;35(38):13257–13265. doi: 10.1523/JNEUROSCI.2332-14.2015 26400953

37. Zanto TP, Toy B, Gazzaley A. Delays in neural processing during working memory encoding in normal aging. Neuropsychologia. 2010;48(1):13–25. doi: 10.1016/j.neuropsychologia.2009.08.003 19666036

38. Buckner RL. Memory and executive function in aging and AD: multiple factors that cause decline and reserve factors that compensate. Neuron. 2004;44(1):195–208. doi: 10.1016/j.neuron.2004.09.006 15450170

39. Gutchess A, Welsh RC, Hedden T, Bangert A, Minear M, Liu L, et al. Aging and the neural correlates of successful picture encoding: frontal activations compensate for decreased medial-temporal activity. Journal of Cognitive Neuroscience. 2005;17(1):84–96. doi: 10.1162/0898929052880048 15701241

40. Zimmerman S, Hasher L, Goldstein D. Cognitive Ageing: a Positive Perspective. In: Kapur N, editor. The Paradoxical Brain. Cambridge, U. K.: Cambridge University Press; 2011. p. 130–150.

41. Lighthall NR, Huettel SA, Cabeza R. Functional compensation in the ventromedial prefrontal cortex improves memory-dependent decisions in older adults. The Journal of Neuroscience. 2014;34(47):15648–15657. doi: 10.1523/JNEUROSCI.2888-14.2014 25411493

42. Daselaar SM, Iyengar V, Davis SW, Eklund K, Hayes SM, Cabeza RE. Less wiring, more firing: low-performing older adults compensate for impaired white matter with greater neural activity. Cerebral Cortex. 2015;25(4):983–990. doi: 10.1093/cercor/bht289 24152545

43. Wingfield A, Kahana MJ. The dynamics of memory retrieval in older adults. Canadian Journal of Experimental Psychology. 2002;56:187–199. doi: 10.1037/h0087396 12271749

44. Laming D. An improved algorithm for predicting free recalls. Cognitive Psychology. 2008;57:179–219. doi: 10.1016/j.cogpsych.2008.01.001 18329010

45. Jensen O, Gelfand J, Kounios J, Lisman JE. Oscillations in the alpha band (9-12 Hz) increase with memory load during retention in a short-term memory task. Cerebral Cortex. 2002;12:877–882. doi: 10.1093/cercor/12.8.877 12122036

46. Guran CNA, Herweg NA, Bunzeck N. Age-related decreases in the retrieval practice effect directly relate to changes in alpha-beta oscillations. Journal of Neuroscience. 2019;39(22):4344–4352. doi: 10.1523/JNEUROSCI.2791-18.2019 30902871

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