Gaze direction reveals implicit item and source memory in older adults

Autoři: Inés Antón-Méndez aff001;  Andrew Talk aff002;  Simone Johnston aff002
Působiště autorů: Discipline of Linguistics, School of Humanities, Arts and Social Sciences, University of New England, Armidale, Australia aff001;  School of Psychology, University of New England, Armidale, Australia aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article


This study looked at eye movements in relation to source memory in older adults. Participants first studied images of common objects appearing in different quadrants of a screen. After a delay, they were shown cues one at a time presented in all four quadrants. Participants stated whether or not the cue had been seen before and in which location. Participants also rated level of confidence in their responses. In trials where participants either claimed they have not seen a previously presented cue or placed it in an incorrect location, they looked significantly more at the correct quadrant. The proportion of time looking at the correct quadrants during incorrect responses was not related to confidence ratings. These results suggest that eye gaze during the memory task does not reflect memory retrieval below the threshold of verbal report. They instead point to an implicit form of source memory in humans that is accessible to eye movements but not to verbal responses.

Klíčová slova:

Attention – Elderly – Eye movements – Eyes – Memory – Memory recall – Sensory cues – Word recognition


1. Shimamura AP, Squire LR. A neuropsychological study of fact memory and source amnesia. J Exp Psychol Learn Mem Cogn. 1987;13(3):464. doi: 10.1037//0278-7393.13.3.464 2956356

2. Doerksen S, Shimamura AP. Source memory enhancement for emotional words. Emotion. 2001;1(1):5. doi: 10.1037/1528-3542.1.1.5 12894807

3. Glisky EL, Polster MR, Routhieaux BC. Double dissociation between item and source memory. Neuropsychology. 1995;9(2):229.

4. Cansino S, Trejo-Morales P, Estrada-Manilla C, Pasaye-Alcaraz EH, Aguilar-Castañeda E, Salgado-Lujambio P, et al. Brain activity during source memory retrieval in young, middle-aged and old adults. J Brain Res. 2015;1618:168–80.

5. Cansino S. Episodic memory decay along the adult lifespan: A review of behavioral and neurophysiological evidence. Int J Psychophysiol [Internet]. 2009;71(1):64–9. Available from: 18725253

6. Eichenbaum H, Yonelinas AP, Ranganath C. The medial temporal lobe and recognition memory. Annu Rev Neurosci. 2007;30:123–52. doi: 10.1146/annurev.neuro.30.051606.094328 17417939

7. Yonelinas AP. The nature of recollection and familiarity: A review of 30 years of research. J Mem Lang. 2002;46(3):441–517.

8. Yonelinas AP. The contribution of recollection and familiarity to recognition and source-memory judgments: A formal dual-process model and an analysis of receiver operating characterstics. J Exp Psychol Learn Mem Cogn [Internet]. 1999 [cited 2019 Jan 11];25(6):1415. Available from: 10605829

9. Hannula DE, Althoff RR, Warren DE, Riggs L, Cohen NJ, Ryan JD. Worth a glance: using eye movements to investigate the cognitive neuroscience of memory. Front Hum Neurosci. 2010;4(October):166.

10. Molitor RJ, Ko PC, Hussey EP, Ally BA. Memory‐related eye movements challenge behavioral measures of pattern completion and pattern separation. Hippocampus. 2014;24(6):666–72. doi: 10.1002/hipo.22256 24493460

11. Pertzov Y, Avidan G, Zohary E. Accumulation of visual information across multiple fixations. J Vis. 2009;9(10):2. doi: 10.1167/9.10.2 19810783

12. Troyer AK, Winocur G, Craik FIM, Moscovitch M. Source memory and divided attention: Reciprocal costs to primary and secondary tasks. Neuropsychology. 1999;13(4):467. 10527055

13. Parnell R, Grasby K, Talk A. The prefrontal cortex is required for incidental encoding but not recollection of source information in rodents. Behav Brain Res. 2012;232(1):77–83. doi: 10.1016/j.bbr.2012.03.040 22504146

14. Talk AC, Grasby KL, Rawson T, Ebejer JL. Preconditioning of Spatial and Auditory Cues: Roles of the Hippocampus, Frontal Cortex, and Cue-Directed Attention. Brain Sci. 2016;6(4):63.

15. Hannula DE, Ranganath C. The eyes have it: hippocampal activity predicts expression of memory in eye movements. Neuron. 2009;63(5):592–9. doi: 10.1016/j.neuron.2009.08.025 19755103

16. Talk A, Antón-Méndez I, Pennefather B. Graded expression of source memory revealed by analysis of gaze direction. Allen P, editor. PLoS One [Internet]. 2017 Nov 27 [cited 2017 Dec 4];12(11):e0188727. Available from:

17. Urgolites ZJ, Smith CN, Squire LR. Eye movements support the link between conscious memory and medial temporal lobe function. Proc Natl Acad Sci U S A [Internet]. 2018 Jul 17 [cited 2019 Sep 19];115(29):7599–604. Available from:

18. Ryan JD, Althoff RR, Whitlow S, Cohen NJ. Amnesia is a deficit in relational memory. Psychol Sci. 2000;11(6):454–61. doi: 10.1111/1467-9280.00288 11202489

19. Hannula DE, Ryan JD, Tranel D, Cohen NJ. Rapid onset relational memory effects are evident in eye movement behavior, but not in hippocampal amnesia. J Cogn Neurosci. 2007;19(10):1690–705. doi: 10.1162/jocn.2007.19.10.1690 17854282

20. Weber FD, Wang J-Y, Born J, Inostroza M. Sleep benefits in parallel implicit and explicit measures of episodic memory. Learn Mem [Internet]. 2014;21(4):190–8. Available from: 24634354

21. Goldsmith M, Koriat A, Pansky A. Strategic regulation of grain size in memory reporting over time. J Mem Lang. 2005;52(4):505–25.

22. Koriat A, Goldsmith M. Monitoring and control processes in the strategic regulation of memory accuracy. Psychol Rev. 1996;103(3):490. doi: 10.1037/0033-295x.103.3.490 8759045

23. Mickes L, Hwe V, Wais PE, Wixted JT. Strong memories are hard to scale. J Exp Psychol Gen [Internet]. 2011 [cited 2019 Sep 20];140(2):239–57. Available from: 21417544

24. Psychology Software Tools. E-Prime. Pittsburgh, PA; 2012.

25. Jaeger TF. Categorical data analysis: Away from ANOVAs (transformational or not) and towards logit mixed models. J Mem Lang [Internet]. 2008 Nov [cited 2013 Aug 1];59(4):434–46. Available from: 19884961

26. Bates MD, Castellano KE, Rabe-Hesketh S, Skrondal A, Statistics B. Handling correlations between covariates and random slopes in multilevel models. J Educ Behav Stat. 2014;39(6):524–49.

27. R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2015.

28. Barr DJ, Levy R, Scheepers C, Tily HJ. Random effects structure for confirmatory hypothesis testing: Keep it maximal. J Mem Lang [Internet]. 2013 Apr [cited 2013 Aug 7];68(3):255–78. Available from:

29. Mirman D, Dixon JA, Magnuson JS. Statistical and computational models of the visual world paradigm: Growth curves and individual differences. J Mem Lang [Internet]. 2008 Nov [cited 2015 Mar 1];59(4):475–94. Available from: 19060958

30. Kafkas A, Montaldi D. Recognition memory strength is predicted by pupillary responses at encoding while fixation patterns distinguish recollection from familiarity. Q J Exp Psychol [Internet]. 2011 Oct [cited 2019 Feb 1];64(10):1971–89. Available from:

31. Olsen RK, Sebanayagam V, Lee Y, Moscovitch M, Grady CL, Rosenbaum RS, et al. The relationship between eye movements and subsequent recognition: Evidence from individual differences and amnesia. Cortex [Internet]. 2016 Dec 1 [cited 2019 Sep 19];85:182–93. Available from:

32. Knight RT. Decreased response to novel stimuli after prefrontal lesions in man. Electroencephalogr Clin Neurophysiol Potentials Sect [Internet]. 1984 Feb 1 [cited 2019 Feb 8];59(1):9–20. Available from:

33. Daffner KR, Mesulam MM, Scinto LFM, Acar D, Calvo V, Faust R, et al. The central role of the prefrontal cortex in directing attention to novel events. Brain [Internet]. 2000 May 1 [cited 2019 Feb 8];123(5):927–39. Available from:

34. Kishiyama MM, Yonelinas AP, Knight RT. Novelty enhancements in memory are dependent on lateral prefrontal cortex. J Neurosci [Internet]. 2009 Jun 24 [cited 2019 Feb 8];29(25):8114–8. Available from:

35. Rawson T, O’Kane M, Talk A. The medial prefrontal cortex and memory of cue location in the rat. Neurobiol Learn Mem [Internet]. 2010 Jan 1 [cited 2019 Feb 12];93(1):132–6. Available from:

36. Postman L, Keppel G. Conditions of cumulative proactive inhibition. J Exp Psychol Gen [Internet]. 1977 [cited 2019 Nov 15];106(4):376–403. Available from:

37. Hartshorne JK. Visual Working Memory Capacity and Proactive Interference. Lauwereyns J, editor. PLoS One [Internet]. 2008 Jul 23 [cited 2019 Nov 15];3(7):e2716. Available from: 18648493

38. Yeung LK, Ryan JD, Cowell RA, Barense MD. Recognition memory impairments caused by false recognition of novel objects. J Exp Psychol Gen. 2013;142(4):1384–97. doi: 10.1037/a0034021 23937183

39. Shimamura AP, Jurica PJ. Memory interference effects and aging: Findings from a test of frontal lobe function. Neuropsychology [Internet]. 1994 [cited 2019 Nov 15];8(3):408–12. Available from:

40. Craik FIM, Rose NS, Gopie N. Recognition without awareness: Encoding and retrieval factors. J Exp Psychol Learn Mem Cogn. 2015;41(5):1271–81. doi: 10.1037/xlm0000137 26010824

41. Voss JL, Baym CL, Paller KA. Accurate forced-choice recognition without awareness of memory retrieval. Learn Mem [Internet]. 2008 Jun 1 [cited 2019 Feb 8];15(6):454–9. Available from:

42. Voss JL, Paller KA. An electrophysiological signature of unconscious recognition memory. Nat Neurosci [Internet]. 2009 Mar 8 [cited 2019 Feb 8];12(3):349–55. Available from: 19198606

43. Laeng B, Waterloo K, Johnsen SH, Bakke SJ, Låg T, Simonsen SS, et al. The Eyes Remember It: Oculography and Pupillometry during Recollection in Three Amnesic Patients. J Cogn Neurosci [Internet]. 2007 Nov 24 [cited 2019 Sep 18];19(11):1888–904. Available from: 17958490

44. Siedlecki KL, Salthouse TA, Berish DE. Is There Anything Special About the Aging of Source Memory? Psychol Aging [Internet]. 2005 [cited 2019 Jan 11];20(1):19–32. Available from: 15769211

45. Johnson MK. The relation between source memory and episodic memory: Comment on Siedlecki et al. (2005). Psychol Aging [Internet]. 2005 [cited 2019 Jan 11];20(3):529–31. Available from: 16248712

46. Tulving E. Episodic and semantic memory. In: Tulving E, Donaldson W, editors. Organization of memory [Internet]. New York, NY, and London: Academic Press; 1972. p. 381–402.

47. Tulving E. Essentials of episodic memory. New York, NY: Oxford University Press; 1983.

48. Haskins AL, Yonelinas AP, Quamme JR, Ranganath C. Perirhinal Cortex Supports Encoding and Familiarity-Based Recognition of Novel Associations. Neuron [Internet]. 2008 Aug 28 [cited 2019 Sep 27];59(4):554–60. Available from: 18760692

49. Mickes L, Wais PE, Wixted JT. Recollection Is a Continuous Process. Psychol Sci [Internet]. 2009 Apr 1 [cited 2019 Sep 27];20(4):509–15. Available from: 19320859

50. Spencer WD, Raz N. Differential Effects of Aging on Memory for Content and Context: A Meta-Analysis. Psychol Aging. 1995;10(4):527–39. doi: 10.1037//0882-7974.10.4.527 8749580

51. Multhaup KS. Aging, source, and decision criteria: When false fame errors do and do not occur. Psychol Aging [Internet]. 1995 [cited 2019 Jan 17];10(3):492–7. Available from: 8527069

52. Hekkanen ST, McEvoy C. False memories and source-monitoring problems: criterion differences. Appl Cogn Psychol [Internet]. 2002 Jan 1 [cited 2019 Feb 1];16(1):73–85. Available from:

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2019 Číslo 12
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