How the size of the to-be-learned material influences the encoding and later retrieval of associative memories: A pupillometric assessment

Autoři: Péter Pajkossy aff001;  Mihály Racsmány aff001
Působiště autorů: Institute of Cognitive Neuroscience and Psychology, Research Centre for Natural Sciences, Budapest, Hungary aff001;  Department of Cognitive Science, Budapest University of Technology and Economic, Budapest, Hungary aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226684


Pupillometry have recently added valuable insights about the cognitive and possible neurobiological processes underlying episodic memory. Most of the studies, however, investigated recognition memory, which only partially relies on cue-driven recollection, the hallmark feature of episodic memory. Here we measured pupil size during a paired associate learning task, where participants encoded word-pairs, and after a short delay they took part in a cued recall. Importantly, we manipulated the size of the learning set: participants either learnt two, four or eight word-pairs in a row. As expected, increasing set size resulted in larger forgetting, assumingly as a consequence of weaker memory strength for the word-pairs. Our results show an important difference between pupil size changes observed during encoding and retrieval. During retrieval, the pupil instantly begun to dilate, as a sign of increased processing load accompanying the retrieval of the target memory. Importantly, large set size was also associated with larger pupil dilation during retrieval. This supports the notion that pupil dilation can be regarded as a marker of memory strength. In contrast, during encoding, pupil dilation decreased with increasing amount of encoded information, which might be due to the overuse of attentional resources. Furthermore, we also found that serial position during encoding modulated subsequent memory effects: for the first three serial positions, successful recall was predicted by larger pupil dilation during encoding, whereas such subsequent memory effect was absent for later serial positions. These results suggest that the amount of information independently modulates pupil dilation during encoding and retrieval, and support the assumption that pupillometric investigation of paired associate learning could be an informative way to investigate the cognitive and neurobiological processes of episodic memory.

Klíčová slova:

Analysis of variance – Cognition – Learning – Memory – Memory recall – Pupil – Reaction time – Semantics


1. Hess EH. Attitude and pupil size. Sci Am. 1965; 212(4): 46–55.

2. Kahneman D, Beatty J. Pupil diameter and load on memory. Science 1966; 154: 1583–1585. doi: 10.1126/science.154.3756.1583 5924930

3. Beatty J. Task-evoked pupillary responses, processing load, and the structure of processing resources. Psychol. Bull. 1982; 91: 276–292. 7071262

4. Beatty J, Lucero-Wagoner B. The pupillary system. In: Cacioppo JT, Tassinary LG, Berntson GG, editors. Handbook of psychophysiology. 2nd Edition. Cambridge University Press. Cambridge. 2000. pp. 142–162.

5. Kahneman D. Attention and effort, Prentice Hall, Engelwood Cliffs. 1973.

6. Preuschoff K, t Hart B M, Einhauser W. Pupil dilation signals surprise: Evidence for noradrenaline’s role in decision making. Front Neurosci. 2011; 5:115. doi: 10.3389/fnins.2011.00115 21994487

7. Alnæs D, Sneve MH, Espeseth T, Endestad T, van de Pavert SHP, Laeng B. Pupil size signals mental effort deployed during multiple object tracking and predicts brain activity in the dorsal attention network and the locus coeruleus. J Vis. 2014; 14(4): 1–20. doi: 10.1167/14.4.1 24692319

8. Unsworth N, Robison MK. Tracking arousal state and mind wandering with pupillometry. Cogn Affect Behav Neurosci. 2018; 18(4): 638–664. doi: 10.3758/s13415-018-0594-4 29654476

9. Jepma M, Nieuwenhuis S. Pupil diameter predicts changes in the exploration–exploitation trade-off: Evidence for the adaptive gain theory. J Cogn Neurosci. 2011; 23(7): 1587–1596. doi: 10.1162/jocn.2010.21548 20666595

10. Pajkossy P, Szőllősi Á, Demeter G, Racsmány M. Tonic noradrenergic activity modulates explorative behavior and attentional set shifting: evidence from pupillometry and gaze pattern analysis. Psychophysiology. 2017; 54(12): 1839–184. doi: 10.1111/psyp.12964 28755458

11. Murphy PR, O’Connell RG, O’Sullivan M, Robertson IH, Balsters JH. Pupil diameter covaries with BOLD activity in human locus coeruleus. Hum Brain Mapp. 35 2014; 4140–4154. doi: 10.1002/hbm.22466 24510607

12. Joshi S, Li Y, Kalwani RM, Gold JI. Relationships between pupil diameter and neuronal activity in the locus coeruleus, colliculi, and cingulate cortex. Neuron. 2016; 89(1): 221–234. doi: 10.1016/j.neuron.2015.11.028 26711118

13. Aston-Jones G, Cohen JD. An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance. Annu. Rev. Neurosci. 2005; 28: 403–450. doi: 10.1146/annurev.neuro.28.061604.135709 16022602

14. Bouret S, Sara SJ. Network reset: A simplified overarching theory of locus coeruleus noradrenaline function. Trends Neurosci. 2005; 28: 574–582. doi: 10.1016/j.tins.2005.09.002 16165227

15. Tulving E. Elements of episodic memory. New York, NJ: Oxford University Press. 1983

16. Conway MA. Episodic memories. Neuropsychologia. 2009; 49:2305–2313.

17. Moscovitch M. Memory and working-with-memory: a component process model based on modules and central systems. In Schacter DL & Tulving E, editors. Memory systems. Cambridge, MA: MIT Press. 1994. pp. 269–310.

18. Conway MA, Pleydell-Pearce CW. The construction of autobiographical memories in the self-memory system. Psychol Rev. 2000; 107(2): 261–288. doi: 10.1037/0033-295x.107.2.261 10789197

19. Võ MLH, Jacobs AM, Kuchinke L, Hofmann M, Conrad M, Schacht A, et al. The coupling of emotion and cognition in the eye: Introducing the pupil old/new effect. Psychophysiology. 2008; 45(1): 130–140. doi: 10.1111/j.1469-8986.2007.00606.x 17910733

20. Papesh MH, Goldinger SD, Hout MC. Memory strength and specificity revealed by pupillometry. Int J Psychophysiol. 2012; 83(1): 56–64. doi: 10.1016/j.ijpsycho.2011.10.002 22019480

21. Otero SC, Weekes BS, Hutton SB. Pupil size changes during recognition memory. Psychophysiology. 2011; 48(10): 1346–1353. doi: 10.1111/j.1469-8986.2011.01217.x 21575007

22. Bradley MM, Lang PJ. Memory, emotion, and pupil diameter: Repetition of natural scenes. Psychophysiology. 2015; 52(9): 1186–1193. doi: 10.1111/psyp.12442 25943211

23. Heaver B, Hutton S B. Keeping an eye on the truth? Pupil size changes associated with recognition memory. Memory. 2011; 19(4): 398–405. doi: 10.1080/09658211.2011.575788 21678156

24. Naber M, Frässle S, Rutishauser U, Einhäuser W. Pupil size signals novelty and predicts later retrieval success for declarative memories of natural scenes. J Vis. 2013; 13(2): 1–20.

25. Rugg MD, Curran T. Event-related potentials and recognition memory. Trends Cogn Sci. 2007; 11: 251–257. doi: 10.1016/j.tics.2007.04.004 17481940

26. Paller KA, Wagner AD. Observing the transformation of experience into memory. Trends Cog Sci. 2002; 6(2): 93–102.

27. 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. 2011; 64(10): 1971–1989.

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

29. Wixted JT. Dual-process theory and signal-detection theory of recognition memory. Psychol rev. 2007; 114(1): 152–176. doi: 10.1037/0033-295X.114.1.152 17227185

30. Bergt A, Urai AE, Donner TH, Schwabe L. Reading memory formation from the eyes. Eur J Neurosci. 2018; 47(12):1525–1533. doi: 10.1111/ejn.13984 29862585

31. Kucewicz MT, Dolezal J, Kremen V, Berry BM, Miller LR, Magee AL et al. Pupil size reflects successful encoding and recall of memory in humans. Sci Rep. 2018; 8(1):4949. doi: 10.1038/s41598-018-23197-6 29563536

32. Van Rijn H, Dalenberg J, Borst J, Sprenger SA. Pupil dilation co-varies with memory strength of individual traces in a delayed response paired-associate task. PLoS One 2012; 7: e51134. doi: 10.1371/journal.pone.0051134 23227244

33. Allan K, Rugg MD. An event-related potential study of explicit memory on tests of cued recall and recognition. Neuropsychologia. 1997; 35(4): 387–397. doi: 10.1016/s0028-3932(96)00094-2 9106268

34. Nobel PA, Shiffrin RM. Retrieval processes in recognition and cued recall. J Exp Psychol Learn Mem Cog. 2001; 27(2): 384–413.

35. Miller AL, Gross MP, & Unsworth N. Individual differences in working memory capacity and long-term memory: The influence of intensity of attention to items at encoding as measured by pupil dilation. J Mem Lang. 2019; 104:25–42.

36. Kónya A, Pintér G. Kategória norma a verbális emlékezet vizsgálatához [Category norms for verbal memory research]. Hung Psychol Rev. 1985; 2: 93–111.

37. Donaldson DI, Rugg MD. Event-related potential studies of associative recognition and recall: electrophysiological evidence for context dependent retrieval processes. Cog Brain Res. 1999;8(1):1–6.

38. Wilding EL., & Ranganath C. Electrophysiological correlates of episodic memory processes. In: Luck SJ, Kappenman ES, editors. Oxford library of psychology. The Oxford handbook of event-related potential components. New York, NY, US: Oxford University Press. 2012. pp. 373–395.

39. Loewenfeld IE. The Pupil: Anatomy, Physiology, and Clinical Applications. Boston: Butterworth-Heinemann; 1999.

40. Wang CA, Boehnke SE, Itti L, Munoz DP. Transient pupil response is modulated by contrast-based saliency. J Neurosci. 2014; 34(2):408–17. doi: 10.1523/JNEUROSCI.3550-13.2014 24403141

41. Barbur JL. Learning from the pupil-studies of basic mechanisms and clinical applications. In: Chalupa LM, Werner JS, editors. The visual neurosciences. vol. 1. Cambridge, MA: MIT Press. 2004. pp. 641–656.

42. Lynn R. Attention, arousal and the orientation reaction. Oxford, UK: Pergamon Press; 1966.

43. Sokolov EN. Higher nervous functions; the orienting reflex. Annu Rev Physiol 1963; 25:545–580. doi: 10.1146/ 13977960

44. Wolffsohn JS, Gilmartin B, Mallen EA, Tsujimura SI. Continuous recording of accommodation and pupil size using the Shin‐Nippon SRW‐5000 autorefractor. Ophthalmic Physiol Opt. 2001; 21(2): 108–113. 11261344

45. Wang CA, Munoz DP. A circuit for pupil orienting responses: implications for cognitive modulation of pupil size. Curr Opin Neurobiol. 2015; 33:134–40. doi: 10.1016/j.conb.2015.03.018 25863645

46. Wang CA, Boehnke SE, White BJ, Munoz DP. Microstimulation of the monkey superior colliculus induces pupil dilation without evoking saccades. J Neurosci. 2012; 32(11):3629–36. doi: 10.1523/JNEUROSCI.5512-11.2012 22423086

47. Conway MA. A structural model of autobiographical memory. In: Conway MA, Rubin DC, Spinnier H, Wagenaar WA, editors. Theoretical Perspectives on Autobiographical Memory. Netherlands:Kluwer Academic Publishers; 1992. pp. 167–194.

48. Moscovitch M. Memory and working-with-memory: A component process model based on modules and central systems. J Cogn Neurosci. 1992; 4(3):257–67. doi: 10.1162/jocn.1992.4.3.257 23964882

49. Semon RW. The mneme. G. Allen & Unwin Limited; 1921.

50. Tulving E. Ecphoric processes in episodic memory. Philos. Trans. Royal Soc. B. 1983; 302: 361–371.

51. Moscovitch M, Cabeza R, Winocur G, Nadel L. Episodic memory and beyond: the hippocampus and neocortex in transformation. Annu Rew Psychol. 2016; 67:105–34.

52. Granholm E, Asarnow RF, Sarkin AJ, & Dykes KL. Pupillary responses index cognitive resource limitations. Psychophysiology 1996; 33: 457–461. doi: 10.1111/j.1469-8986.1996.tb01071.x 8753946

53. Van Gerven PWM, Paas F, Van Merrienboer JJG, & Schmidt HG. Memory load and the cognitive pupillary response in aging. Psychophysiology, 2004; 41: 167–174. doi: 10.1111/j.1469-8986.2003.00148.x 15032982

54. Naber M, Hommel B, Colzato LS. Improved human visuomotor performance and pupil constriction after choline supplementation in a placebo-controlled double-blind study. Sci Rep. 2015; 5:13188. doi: 10.1038/srep13188 26271904

55. Easton A, Douchamps V, Eacott M, Lever C. A specific role for septohippocampal acetylcholine in memory? Neuropsychologia. 2012; 50(13):3156–3168. doi: 10.1016/j.neuropsychologia.2012.07.022 22884957

56. Atri A, Sherman S, Norman KA, Kirchhoff BA, Nicolas MM, Greicius MD et al. Blockade of central cholinergic receptors impairs new learning and increases proactive interference in a word paired-associate memory task. Behav Neurosci. 2014; 118(1):223.

57. Kafkas A, Montaldi D. How do memory systems detect and respond to novelty? Neurosci Lett. 2018; 680:60–8. doi: 10.1016/j.neulet.2018.01.053 29408218

58. Larsen RS, & Waters J. Neuromodulatory Correlates of Pupil Dilation. Front Neural Circuit. 2018; 12:21.

59. Reimer J, McGinley MJ, Liu Y, Rodenkirch C, Wang Q, McCormick DA et al. Pupil fluctuations track rapid changes in adrenergic and cholinergic activity in cortex. Nat Commun. 2016; 7:13289. doi: 10.1038/ncomms13289 27824036

60. Chen Z, Cowan N. Chunk limits and length limits in immediate recall: a reconciliation. J Exp Psychol Learn Mem Cog. 2005; 31(6): 1235–1249.

61. McGaugh JL. Memory—a century of consolidation. Science, 2000; 287(5451): 248–251. doi: 10.1126/science.287.5451.248 10634773

62. Meeter M, Murre JM. Consolidation of Long-Term Memory: Evidence and Alternatives. Psychol Bul. 2004; 130(6): 843–857.

Článek vyšel v časopise


2019 Číslo 12