Pupil size signals novelty and predicts later retrieval success for declarative memories of natural scenes

Journal of Vision

Volumn 13, Issue 2, 2013, Pages

  Naber, Marnix ^a   Frässle, Stefan ^a   Rutishauser, Ueli ^b,c   Einhäuser, Wolfgang ^a,d  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^c CEDARS SINAI MEDICAL CENTER   (United States)

^d Center for Interdisciplinary Research (ZiF)   (Germany)

Author keywords

Memory; Natural scene; Pupil

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; BRAIN MAPPING; COMPARATIVE STUDY; EMOTION; FEMALE; HIPPOCAMPUS; HUMAN; LEARNING; MALE; MEMORY; MEMORY DISORDER; PATHOPHYSIOLOGY; PHOTOSTIMULATION; PHYSIOLOGY; PUPIL; REFERENCE VALUE; TEMPORAL LOBE; VISION;

ADOLESCENT; ADULT; BRAIN MAPPING; EMOTIONS; FEMALE; HIPPOCAMPUS; HUMANS; LEARNING; MALE; MEMORY; MEMORY DISORDERS; PHOTIC STIMULATION; PUPIL; REFERENCE VALUES; TEMPORAL LOBE; VISUAL PERCEPTION; YOUNG ADULT;

MLCS; MLOWN;

EID: 84878362765     PISSN: None     EISSN: 15347362     Source Type: Journal    
DOI: 10.1167/13.2.11     Document Type: Article

References (94)

1. Bakin, J. S., & Weinberger, N. M. (1996). Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proceedings of the National Academy of Sciences USA, 93(20), 11219-11224.
2. Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, 57, 289-300.
3. Berridge, C. W., & Foote, S. L. (1991). Effects of locus coeruleus activation on electroencephalographic activity in neocortex and hippocampus. Journal of Neuroscience, 11(10), 3135-3145.
4. Bitsios, P., Szabadi, E., & Bradshaw, C. M. (2002). Relationship of the 'fear-inhibited light reflex' to the level of state/trait anxiety in healthy subjects. International Journal of Psychophysiology, 43(2), 177-184.
5. Bradshaw, J. (1967). Pupil size as a measure of arousal during information processing. Nature, 216(5114), 515-516.
6. Brainard, D. (1997). The Psychophysics Toolbox. Spatial Vision, 10(4), 433-436.
7. Chadwick, M., Hassabis, D., Weiskopf, N., & Maguire, E. (2010). Decoding individual episodic memory traces in the human hippocampus. Current Biology, 20(6), 544-547.
8. Charney, D. S., Scheier, I. H., & Redmond, D. E. (1995). Noradrenergic neural substrates for anxiety and fear. In F. E. Bloom & D. J. Kupfer (Eds.), Psychopharmacology: The fourth generation of progress (pp. 387-396). New York: Raven Press.
9. Cornelissen, F., Peters, E., & Palmer, J. (2002). The Eyelink Toolbox: Eye tracking with MATLAB and the Psychophysics Toolbox. Behavioral Research Methods, Instruments, & Computers, 34(4), 613- 617.
10. Daniels, L., Hock, H. S., & Huisman, A. (2009). The effect of spatial attention on pupil dynamics. Perception, 38, 16.
11. Desimone, R. (1996). Neural mechanisms for visual memory and their role in attention. Proceedings of the National Academy of Sciences USA, 93(24), 13494-13499.
12. Einhäuser, W., Koch, C., & Carter, O. (2010). Pupil dilation betrays the timing of decisions. Frontiers in Human Neuroscience, 4, 18.
13. Einhäuser, W., Stout, J., Koch, C., & Carter, O. (2008). Pupil dilation reflects perceptual selection and predicts subsequent stability in perceptual rivalry. Proceedings of the National Academy of Sciences USA, 105(5), 1704-1709.
14. Fabiani, M., & Donchin, E. (1995). Encoding processes and memory organization: A model of the von Restorff effect. Journal of Experimental Psychology: Learning, Memory, & Cognition, 21(1), 224-240.
15. Fountoulakis, K. N., St Kaprinis, G., & Fotiou, F. (2004). Is there a role for pupillometry in the diagnostic approach of Alzheimer's disease?. A review of the data. Journal of the American Geriatrics Society, 52(1), 166-168.
16. Francis, P. T., Palmer, A. M., Snape, M., & Wilcock, G. K. (1999). The cholinergic hypothesis of Alzheimer's disease: a review of progress. Journal of Neurology, Neurosurgery & Psychiatry, 66(2), 137- 147.
17. Friedman, D., Hakerem, G., Sutton, S., & Fleiss, J. L. (1973). Effect of stimulus uncertainty on the pupillary dilation response and the vertex evoked potential. Electroencephalography & Clinical Neurophysiology, 34(5), 475-484.
18. Gardner, R. M., Beltramo, J. S., & Krinsky, R. (1975). Pupillary changes during encoding, storage, and retrieval of information. Perceptual & Motor Skills, 41(3), 951-955.
19. Gardner, R. M., Philp, P., & Radacy, S. (1978). Pupillary changes during recall in children. Journal of Experimental Child Psychology, 25(1), 168-172.
20. Gilzenrat, M. S., Nieuwenhuis, S., Jepma, M., & Cohen, J. D. (2010). Pupil diameter tracks changes in control state predicted by the adaptive gain theory of locus coeruleus function. Cognitive, Affective, & Behavioral Neuroscience, 10(2), 252- 269.
21. Gonsalves, B., Kahn, I., Curran, T., Norman, K., & Wagner, A. (2005). Memory strength and repetition suppression: Multimodal imaging of medial temporal cortical contributions to recognition. Neuron, 47(5), 751-761.
22. Granholm, E., Asarnow, R. F., Sarkin, A. J., & Dykes, K. L. (1996). Pupillary responses index cognitive resource limitations. Psychophysiology, 33(4), 457- 461.
23. Grill-Spector, K., Henson, R., & Martin, A. (2006). Repetition and the brain: Neural models of stimulus-specific effects. Trends in Cognitive Sciences, 10(1), 14-23.
24. Harrison, N., Singer, T., Rotshtein, P., Dolan, R., & Critchley, H. (2006). Pupillary contagion: Central mechanisms engaged in sadness processing. Social Cognitive & Affective Neuroscience, 1(1), 5-17.
25. Hassabis, D., Chu, C., Rees, G., Weiskopf, N., Molyneux, P., & Maguire, E. (2009). Decoding neuronal ensembles in the human hippocampus. Current Biology, 19(7), 546-554.
26. Hasselmo, M. E. (2006). The role of acetylcholine in learning and memory. Current Opinion in Neurobiology, 16(6), 710-715.
27. Hasselmo, M. E., & Giocomo, L. M. (2006). Cholinergic modulation of cortical function. Journal of Molecular Neuroscience, 30(1-2), 133-135.
28. Heaver, B., & Hutton, S. B. (2011). Keeping an eye on the truth? Pupil size changes associated with recognition memory. Memory, 19(4), 398-405.
29. Hess, E. H., & Polt, J. M. (1964). Pupil size in relation to mental activity during simple problem-solving. Science, 143(3611), 1190-1192.
30. Jepma, M., Deinum, J., Asplund, C. L., Rombouts, S. A., Tamsma, J. T., Tjeerdema, N., et al. (2011). Neurocognitive function in dopamine-b-hydroxylase deficiency. Neuropsychopharmacology, 36(8), 1608-1619.
31. Jepma, M., & Nieuwenhuis, S. (2011). Pupil diameter predicts changes in the exploration-exploitation trade-off: Evidence for the adaptive gain theory. Journal of Cognitive Neuroscience, 23(7), 1587- 1596.
32. Johnson, J., McDuff, S., Rugg, M., & Norman, K. (2009). Recollection, familiarity, and cortical reinstatement: A multivoxel pattern analysis. Neuron, 63(5), 697-708.
33. Kafkas, A., & Montaldi, D. (2011). Recognition memory strength is predicted by pupillary responses at encoding while fixation patterns distinguish recollection from familiarity. Quarterly Journal of Experimental Psychology (Hove), 64(10), 1971-1989.
34. Kahneman, D. (1973). Attention and effort. Englewood Cliffs, NJ: Prentice Hall.
35. Kahneman, D., & Beatty, J. (1966). Pupil diameter and load on memory. Science, 154(756), 1583-1585.
36. Karatekin, C. (2004). Development of attentional allocation in the dual task paradigm. International Journal of Psychophysiology, 52(1), 7-21.
37. Karatekin, C., Couperus, J. W., & Marcus, D. J. (2004). Attention allocation in the dual-task paradigm as measured through behavioral and psychophysiological responses. Psychophysiology, 41(2), 175-185.
38. Kilgard, M. P., & Merzenich, M. M. (1998). Cortical map reorganization enabled by nucleus basalis activity. Science, 279(5357), 1714-1718.
39. Kishiyama, M. M., Yonelinas, A. P., & Lazzara, M. M. (2004). The von Restorff effect in amnesia: The contribution of the hippocampal system to noveltyrelated memory enhancements. Journal of Cognitive Neuroscience, 16(1), 15-23.
40. Knight, R. (1996). Contribution of human hippocampal region to novelty detection. Nature, 383(6597), 256-259.
41. Koss, M. C. (1986). Pupillary dilation as an index of central nervous system alpha 2-adrenoceptor activation. Journal of Pharmacological Methods, 15(1), 1-19.
42. Kukolja, J., Thiel, C. M., & Fink, G. R. (2009). Cholinergic stimulation enhances neural activity associated with encoding but reduces neural activity associated with retrieval in humans. Journal of Neuroscience, 29(25), 8119-8128.
43. Kumaran, D., & Maguire, E. (2009). Novelty signals: A window into hippocampal information processing. Trends in Cognitive Sciences, 13(2), 47-54.
44. Li, F. F., VanRullen, R., Koch, C., & Perona, P. (2002). Rapid natural scene categorization in the near absence of attention. Proceedings of the National Academy of Sciences USA, 99(14), 9596- 9601.
45. Lisman, J. E., & Grace, A. A. (2005). The hippocampal- VTA loop: Controlling the entry of information into long-term memory. Neuron, 46(5), 703-713.
46. Loewenfeld, I., & Lowenstein, O. (1993). The pupil: Anatomy, physiology, and clinical applications. Detroit: Wayne State University Press.
47. Macmillan, N., & Creelman, C. (2005). Detection theory (2nd ed.). Mahwah, NJ: Lawrence Erlbaum Associates.
48. Maw, N. N., & Pomplun, M. (2004). Studying human face recognition with the gaze-contingent window technique. In K. Forbus, D. Gentner, & T. Regier (Eds.), Proceedings of the Twenty-Sixth Annual Meeting of the Cognitive Science Society. (pp. 927- 932). Mahwah, NJ: Lawrence Erlbaum Associates, Inc.
49. McDuff, S., Frankel, H., & Norman, K. (2009). Multivoxel pattern analysis reveals increased memory targeting and reduced use of retrieved details during single-agenda source monitoring. Journal of Neuroscience, 29(2), 508-516.
50. McGaugh, J. L., & Roozendaal, B. (2008). Drug enhancement of memory consolidation: Historical perspective and neurobiological implications. Psychopharmacology (Berlin), 202(1-3), 3-14.
51. Montaldi, D., Spencer, T., Roberts, N., & Mayes, A. (2006). The neural system that mediates familiarity memory. Hippocampus, 16(5), 504-520.
52. Naber, M., Frässle, S., & Einhäuser, W. (2011). Perceptual rivalry: Reflexes reveal the gradual nature of visual awareness. PLoS One, 6(6), e20910.
53. Nagai, M., Wada, M., & Sunaga, N. (2002). Trait anxiety affects the pupillary light reflex in college students. Neuroscience Letters, 328(1), 68-70.
54. Nieuwenhuis, S., de Geus, E. J., & Aston-Jones, G. (2011). The anatomical and functional relationship between the P3 and autonomic components of the orienting response. Psychophysiology, 48, 162-175.
55. Otero, S. C., Weekes, B. S., & Hutton, S. B. (2011). Pupil size changes during recognition memory. Psychophysiology, 4, 1346-1353.
56. Otten, L. J., & Donchin, E. (2000). Relationship between P300 amplitude and subsequent recall for distinctive events: Dependence on type of distinctiveness attribute. Psychophysiology, 37, 644-661.
57. Paller, K. A., Kutas, M., & Mayes, A. R. (1987). Neural correlates of encoding in an incidental learning paradigm. Electroencephalography & Clinical Neurophysiology, 67(4), 360-371.
58. Paller, K. A., & Wagner, A. D. (2002). Observing the transformation of experience into memory. Trends in Cognitive Sciences, 6(2), 93-102.
59. Phillips, M. A., Szabadi, E., & Bradshaw, C. M. (2000). Comparison of the effects of clonidine and yohimbine on spontaneous pupillary fluctuations in healthy human volunteers. Psychopharmacology (Berlin), 150(1), 85-89.
60. Polyn, S., Natu, V., Cohen, J., & Norman, K. (2005). Category-specific cortical activity precedes retrieval during memory search. Science, 310(5756), 1963- 1966.
61. Power, A. E. (2004). Slow-wave sleep, acetylcholine, and memory consolidation. Proceedings of the National Academy of Sciences USA, 101(7), 1795- 1796.
62. Prettyman, R., Bitsios, P., & Szabadi, E. (1997). Altered pupillary size and darkness and light reflexes in Alzheimer's disease. Journal of Neurology, Neurosurgery, & Psychiatry, 62(6), 665-668.
63. Raisig, S., Welke, T., Hagendorf, H., & van der Meer, E. (2010). I spy with my little eye: Detection of temporal violations in event sequences and the pupillary response. International Journal of Psychophysiology, 76(1), 1-8.
64. Rajkowski, J., Kubiak, P., & Aston-Jones, G. (1994). Locus coeruleus activity in monkey: Phasic and tonic changes are associated with altered vigilance. Brain Research Bulletin, 35(5-6), 607-616.
65. Ranganath, C., & Blumenfeld, R. (2005). Doubts about double dissociations between short- and long-term memory. Trends in Cognitive Sciences, 9(8), 374- 380.
66. Ranganath, C., & Rainer, G. (2003). Neural mechanisms for detecting and remembering novel events. Nature Review Neuroscience, 4(3), 193-202.
67. Ratcliff, R., Sheu, C. F., & Gronlund, S. D. (1992). Testing global memory models using ROC curves. Psychological Review, 99, 518-535.
68. Rissman, J., Greely, H., & Wagner, A. (2010). Detecting individual memories through the neural decoding of memory states and past experience. Proceedings of the National Academy of Sciences USA, 107(21), 9849-9854.
69. Rutishauser, U., Mamelak, A., & Schuman, E. (2006). Single-trial learning of novel stimuli by individual neurons of the human hippocampus-amygdala complex. Neuron, 49(6), 805-813.
70. Rutishauser, U., Ross, I. B., Mamelak, A. N., & Schuman, E. M. (2010). Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature, 464(7290), 903-907.
71. Rutishauser, U., Schuman, E., & Mamelak, A. (2008). Activity of human hippocampal and amygdala neurons during retrieval of declarative memories. Proceedings of the National Academy of Sciences USA, 105(1), 329-334.
72. Samuels, E. R., & Szabadi, E. (2008). Functional neuroanatomy of the noradrenergic locus coeruleus: Its roles in the regulation of arousal and autonomic function part II: Physiological and pharmacological manipulations and pathological alterations of locus coeruleus activity in humans. Current Neuropharmacology, 6(3), 254-285.
73. Sara, S. J. (2009). The locus coeruleus and noradrenergic modulation of cognition. Nature Reviews Neuroscience, 10(3), 211-223.
74. Silver, M. A., Shenhav, A., & D'Esposito, M. (2008). Cholinergic enhancement reduces spatial spread of visual responses in human early visual cortex. Neuron, 60(5), 904-914.
75. Simpson, H. M., & Hale, S. M. (1969). Pupillary changes during a decision-making task. Perceptual & Motor Skills, 29(2), 495-498.
76. Simpson, H. M., & Molloy, F. M. (1971). Effects of audience anxiety on pupil size. Psychophysiology, 8(4), 491-496.
77. Sokolov, E. N. (1963). Higher nervous functions: The orienting reflex. Annual Review of Physiology, 25, 545-580.
78. Squire, L. R., Stark, C. E., & Clark, R. E. (2004). The medial temporal lobe. Annual Review of Neuroscience, 27, 279-306.
79. Squire, L. R., Wixted, J. T., & Clark, R. E. (2007). Recognition memory and the medial temporal lobe: A new perspective. Nature Review Neuroscience, 8(11), 872-883.
80. Standing, L. (1973). Learning 10,000 pictures. Quarterly Journal of Experimental Psychology, 25(2), 207-222.
81. Standing, L., Conezio, J., & Haber, R. N. (1970). Perception and memory for pictures: Single-trial learning of 2500 visual stimuli. Psychonomic Science, 19, 73-74.
82. Steinhauer, S. R., Boller, F., Zubin, J., & Pearlman, S. (1983). Pupillary dilation to emotional visual stimuli revisited. Psychophysiology, 20, 472.
83. Sterpenich, V., D'Argembeau, A., Desseilles, M., Balteau, E., Albouy, G., Vandewalle, G., et al. (2006). The locus ceruleus is involved in the successful retrieval of emotional memories in humans. Journal of Neuroscience, 26(28), 7416- 7423.
84. Tulving, E. (2002). Episodic memory: From mind to brain. Annual Review of Psychology, 53, 1-25.
85. Vankov, A., Hervé-Minvielle, A., & Sara, S. J. (1995). Response to novelty and its rapid habituation in locus coeruleus neurons of the freely exploring rat. European Journal of Neuroscience, 7(6), 1180-1187.
86. Viskontas, I., Knowlton, B., Steinmetz, P., & Fried, I. (2006). Differences in mnemonic processing by neurons in the human hippocampus and parahippocampal regions. Journal of Cognitive Neuroscience, 18(10), 1654-1662.
87. Võ, M. L., Jacobs, A. M., Kuchinke, L., Hofmann, M., Conrad, M., Schacht, A., et al. (2008). The coupling of emotion and cognition in the eye: Introducing the pupil old/new effect. Psychophysiology, 45(1), 130-140.
88. von Restorff, H. (1933). Über die Wirkung von Bereichsbildungen im Spurenfeld. Psychologische Forschung, 18, 299-342.
89. Wais, P. E., Wixted, J. T., Hopkins, R. O., & Squire, L. R. (2006). The hippocampus supports both the recollection and the familiarity components of recognition memory. Neuron, 49, 459-466.
90. Warburton, E. C., Koder, T., Cho, K., Massey, P. V., Duguid, G., Barker, G. R., et al. (2003). Cholinergic neurotransmission is essential for perirhinal cortical plasticity and recognition memory. Neuron, 38(6), 987-996.
91. Wixted, J. T. (2007). Dual-process theory and signaldetection theory of recognition memory. Psychological Review, 114(1), 152-176.
92. Xiang, J., & Brown, M. (1998). Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe. Neuropharmacology, 37(4-5), 657-676.
93. Yonelinas, A., Otten, L., Shaw, K., & Rugg, M. (2005). Separating the brain regions involved in recollection and familiarity in recognition memory. Journal of Neuroscience, 25(11), 3002-3008.
94. Yoss, R. E., Moyer, N. J., & Hollenhorst, R. W. (1970). Pupil size and spontaneous pupillary waves associated with alertness, drowsiness, and sleep. Neurology, 20(6), 545-554.