Advertisement

Pupillometry

  • Bruno LaengEmail author
  • Dag Alnaes
Chapter
Part of the Studies in Neuroscience, Psychology and Behavioral Economics book series (SNPBE)

Abstract

The eye pupil is an organ optimally designed by evolution to control the amount of light entering the eye so as to obtain sharp visual images and allow monitoring of as much as possible of the visual field. The opposing pupillary movements of constrictions and dilations optimize some of these goals while at the same time may reduce the effectiveness of others. The pupils are controlled by subcortical anatomical structures of the brain that allow rapid adjustments of the pupil (in particular to strong light). However, higher-level cortical mechanisms in the brain can affect in a top-down manner pupil size, possibly to prepare the eye as for forthcoming visual events. Today it has become relatively easy and inexpensive to measure pupil size with current infrared eye-trackers. Yet, advancements in equipment and data analysis are still needed in order to apply pupillometry to situations outside the laboratory where luminance conditions cannot be controlled. Psychological studies have clearly implicated pupil responses as reliable indexes of motivational and emotional states. The most promising application of pupillometry stands in its ability to index robustly and reliably the level of cognitive workload or “mental effort” engaged during a task. Recent studies in neuroscience have clarified that the pupil reflects the activity of the Locus coeruleus, which is the brain’s hub of the norepinephrine system and whose activity has the effect of “energizing” the whole brain at a particular moment in time. Hence pupillary responses provide a window on attentional processes that are relevant for learning and memory.

Bibliography

  1. Aboyoun, D. C., & Dabbs, J. M. (1998). The Hess pupil dilation findings: Sex or novelty? Social Behavior and Personality, 26, 415–420.CrossRefGoogle Scholar
  2. Adams, D. B., Gold, A. R., & Burt, A. D. (1978). Rise in female-initiated sexual activity at ovulation and its suppression by oral contraceptives. The New England Journal of Medicine, 21, 1145–1150.CrossRefGoogle Scholar
  3. Ahern, S., & Beatty, J. (1979). Pupillary responses during information processing vary with scholastic aptitude test scores. Science, 205, 1289–1292.  https://doi.org/10.1126/science.472746.CrossRefPubMedGoogle Scholar
  4. Alnæs, D., Sneve, M. H., Espeseth, T., Endestad, T., van de Pavert, S. H. P., & Laeng, B. (2014). Pupil size signals mental effort deployed during multiple object tracking and predicts brain activity in the dorsal attention network and the Locus coeruleus. Journal of Vision, 14(4), 1–20. https://doi.org/10.1167/14.4.1.CrossRefPubMedGoogle Scholar
  5. Alvarez, G. A., & Cavanagh, P. (2005). Independent resources for attentional tracking in the left and right visual hemifields. Psychological Science, 16, 637–643.  https://doi.org/10.1111/j.1467-9280.2005.01587.x.CrossRefPubMedGoogle Scholar
  6. Arch, D. C. (1979). Pupil dilation measures in consumer research: Applications and limitations. In William L. Wilkie (Ed.), NA - Advances in consumer research (Vol. 06, pp. 166–168). Ann Abor, MI : Association for Consumer Research.Google Scholar
  7. Aston-Jones, G., & Cohen, J. D. (2005a). Adaptive gain and the role of the locus coeruleus-norepinephrine system in optimal performance. Journal of Comparative Neurology, 493, 99–110.  https://doi.org/10.1002/cne.20723.CrossRefPubMedGoogle Scholar
  8. Aston-Jones, G., & Cohen, J. D. (2005b). An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance. Annual Review of Neuroscience, 28, 403–450.  https://doi.org/10.1146/annurev.neuro.28.061604.135709.CrossRefPubMedGoogle Scholar
  9. Aston-Jones, G., Rajkowski, J., & Cohen, J. (2000). Locus coeruleus and regulation of behavioral flexibility and attention. Progress in Brain Research, 126, 165–182.  https://doi.org/10.1016/s0079-6123(00)26013-5.CrossRefPubMedGoogle Scholar
  10. Attard-Johnson, J., Bindemann, M., & Ó Ciardha, C. (2016). Heterosexual, Homosexual, and bisexual men’s pupillary responses to persons at different stages of sexual development. The Journal of Sex Research, 00(00), 1–12.Google Scholar
  11. Beatty, J. (1982). Task-evoked pupillary responses, processing load, and the structure of processing resources. Psychological Bulletin, 91, 276–292.CrossRefPubMedGoogle Scholar
  12. Beatty, J., & Kahneman, D. (1966). Pupillary changes in two memory tasks. Psychonomic Science, 5, 371–372.CrossRefGoogle Scholar
  13. Beatty, J., & Lucero-Wagoner, B. (2000). The pupillary system. In J. T. Cacioppo, L. G. Tassinary, & G. G. Berntson (Eds.), (2nd ed., pp. 142–162). New York: Cambridge University Press.Google Scholar
  14. Bernhardt, P. C., Dabbs, J. M., & Riad, J. K. (1996). Pupillometry system for use in social psychology. Behavior Research Methods, Instruments & Computers, 28(1), 61–66.CrossRefGoogle Scholar
  15. Berridge, C. W., & Waterhouse, B. D. (2003). The Locus coeruleus-noradrenergic system: Modulation of behavioral state and state-dependent cognitive processes. Brain Research. Brain Research Reviews, 42, 33–84.CrossRefPubMedGoogle Scholar
  16. Binda, P., Pereverzeva, M., & Murray, S. (2013). Pupil constrictions to photographs of the sun. Journal of Vision, 13(6), 1–9.Google Scholar
  17. Blackwell, R., Miniard, P., & Engel, J. (2001). Consumer Behavior (9th ed.). Orlando: Harcourt.Google Scholar
  18. Bombeke, K., Duthoo, W., Mueller, S. C., Hopf, J., & Boehler, C. N. (2016). Pupil size directly modulates the feedforward response in human primary visual cortex independently of attention. NeuroImage, 127, 67–73.  https://doi.org/10.1016/j.neuroimage.2015.11.072.CrossRefPubMedGoogle Scholar
  19. Bouret, S., Duvel, A., Onat, S., & Sara, S. J. (2003). Phasic activation of locus ceruleus neurons by the central nucleus of the amygdala. The Journal of Neuroscience, 23, 3491–3497.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Bouret, S., & Sara, S. J. (2005). Network reset: A simplified overarching theory of locus coeruleus noradrenaline function. Trends in Neurosciences, 28(11), 574–582.  https://doi.org/10.1016/j.tins.2005.09.002.CrossRefPubMedGoogle Scholar
  21. Bressler, S. L., Tang, W., Sylvester, C. M., Shulman, G. L., & Corbetta, M. (2008). Top-down control of human visual cortex by frontal and parietal cortex in anticipatory visual spatial attention. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 28, 10056–10061.  https://doi.org/10.1523/jneurosci.1776-08.2008.CrossRefGoogle Scholar
  22. Brisson, J., Mainville, M., Mailloux, D., Beaulieu, C., Serres, J., & Sirois, S. (2013). Pupil diameter measurement errors as a function of gaze direction in corneal reflection eyetrackers. Behavior Research Methods, 45, 1322–1331.  https://doi.org/10.3758/s13428-013-0327-0.CrossRefPubMedGoogle Scholar
  23. Campbell, F. W., & Gregory, A. H. (1960). Effect of size of pupil on visual acuity. Nature, 4743, 1121–1123.CrossRefGoogle Scholar
  24. Carbon, C. C., Hutzler, F., & Minge, M. (2006). Innovativeness in design investigated by eye movements and pupillometry. Psychology Science, 48(2), 173–186.Google Scholar
  25. Cavanagh, P., & Alvarez, G. A. (2005). Tracking multiple targets with multifocal attention. Trends Cognitive Science, 9, 349–354.  https://doi.org/10.1016/j.tics.2005.05.009.CrossRefGoogle Scholar
  26. Corbetta, M., Patel, G., & Shulman, G. L. (2008). The reorienting system of the human brain: From environment to theory of mind. Neuron, 58, 306–324.  https://doi.org/10.1016/j.neuron.2008.04.017.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Cornsweet, T. N. (1970). Visual perception. New York: Academic Press.Google Scholar
  28. Damsma, A., & van Rijn, H. (2017). Pupillary response indexes the metrical hierarchy of unattended rhythmic violations. Brain and Cognition, 111, 95–103.CrossRefPubMedGoogle Scholar
  29. Denton, E. J. (1956). The responses of the pupil of Gekko gekko to external light stimulus. J. Gen. Physiol., 40, 201–2016.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Denton, E. J., & Pirenne, M. H. (1952). On the functional stability of the retina. The Journal of General Physiology, 117, 55P.PubMedGoogle Scholar
  31. Drew, T., Horowitz, T. S., & Vogel, E. K. (2013). Swapping or dropping? Electrophysiological measures of difficulty during multiple object tracking. Cognition, 126, 213–223.Google Scholar
  32. Einhäuser, W., Koch, C., & Carter, O. L. (2010). Pupil dilation betrays the timing of decisions. Frontiers in Human Neuroscience, 4, 18.  https://doi.org/10.3389/fnhum.2010.00018.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Einhäuser, W., Stout, J., Koch, C., & Carter, O. (2008). Pupil dilation reflects perceptual selection and predicts subsequent stability in perceptual rivalry. Proceedings of National Academy Science United States America, 105, 1704–1709.  https://doi.org/10.1073/pnas.0707727105.CrossRefGoogle Scholar
  34. Eldar, E., Cohen, J. D., & Niv, Y. (2013). The effects of neural gain on attention and learning. Nature Neuroscience, 16(8), 1146–1153.  https://doi.org/10.1038/nn.3428.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Fan, J., Gu, X., Guise, K.G., Liu, X., Fossella, J., Wang, H., & Posner, M. I. (2009). Testing the behavioral interaction and integration of attentional networks. Brain and Cognition, 70(2), 209–220.  https://doi.org/10.1016/j.bandc.2009.02.002.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Feinberg, R., & Podolak, E. (1965). Latency of pupillary reflex to light stimulation and its relationship to aging. In A. T. Welford (Ed.), Behavior, Aging, and the Nervous System. Springfield, IL: C.C. Thomas Publisher.Google Scholar
  37. Foote, S. L., & Morrison, J. H. (1987). Extrathalamic modulation of cortical function. Annual Review of Neuroscience, 10, 67–95.  https://doi.org/10.1146/annurev.ne.10.030187.000435.CrossRefPubMedGoogle Scholar
  38. Franconeri, S. L., Alvarez, G. A., & Cavanagh, P. (2013). Flexible cognitive resources: Competitive content maps for attention and memory. Trends Cognitive Science, 17, 134–141.  https://doi.org/10.1016/j.tics.2013.01.010.CrossRefGoogle Scholar
  39. Gagl, B., Hawelka, S., & Huzler, F. (2011). Systematic influence of gaze position on pupil size measurement: Analysis and correction. Behavioral Research, 43, 1171–1181.CrossRefGoogle Scholar
  40. Gamlin, P. D. R., McDougal, D. H., Pokorny, J., Smith, V., Yau, K.-W., & Dacey, D. M. (2007). Human and macaque pupil responses driven by melanopsin-containing retinal ganglion cells. Vision Research, 47, 946–954.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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 Affected Behaviour Neuroscience, 10, 252–269.  https://doi.org/10.3758/cabn.10.2.252.CrossRefGoogle Scholar
  42. Gingras, B., Marin, M. M., Puig-Waldmüller, E., & Fitch, W. T. (2015). The eye is listening: Music-induced arousal and individual differences predict pupillary responses. Frontiers in Human Neuroscience, 9, 619.  https://doi.org/10.3389/fnhum.2015.00619.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Goldwater, B. C. (1972). Psychological significance of pupillary movements. Psychological Bulletin, 77, 340–355.CrossRefPubMedGoogle Scholar
  44. Granholm, E., Asarnow, R. F., Sarkin, A. J., & Dykes, K. L. (1996). Pupillary responses index cognitive resource limitations. Psychophysiology, 33(4), 457–461.  https://doi.org/10.1111/j.1469-8986.1996.tb01071.x.CrossRefPubMedGoogle Scholar
  45. Haro, J., Guasch, M., Vallès, B., et al. (2016). Is pupillary response a reliable index of word recognition? Evidence from a delayed lexical decision task. Behavioral Research.  https://doi.org/10.3758/s13428-016-0835-9.CrossRefGoogle Scholar
  46. Hermans, E. J., van Marle, H. J. F., Ossewaarde, L., Henckens, M. J. a. G., Qin, S., van Kesteren, M. T. R., … Fernández, G. (2011). Stress-related noradrenergic activity prompts large-scale neural network reconfiguration. Science, 334, 1151–1153.  https://doi.org/10.1126/science.1209603.CrossRefPubMedGoogle Scholar
  47. Hess, E. H. (1965). Attitude and pupil size. Scient. American, 212, 46–54.Google Scholar
  48. Hess, E. H. (1975). The role of pupil size in communication. Scientific American, 233(5), 110–112, 116–119.CrossRefPubMedGoogle Scholar
  49. Hess, E. H., & Polt, J. M. (1960). Pupil size as related to interest value of visual stimuli. Science, 132, 349–350.CrossRefPubMedGoogle Scholar
  50. Hess, E. H., & Polt, J. M. (1964). Pupil size in relation to mental activity during simple problem-solving. Science, 140, 1190–1192.  https://doi.org/10.1126/science.143.3611.1190.CrossRefGoogle Scholar
  51. Hou, R. H., Freeman, C., Langley, R. W., Szabadi, E., & Bradshaw, C. M. (2005). Does modafinil activate the locus coeruleus in man? Comparison of modafinil and clonidine on arousal and autonomic functions in human volunteers. Psychopharmacology (Berl), 181(3), 537–549.  https://doi.org/10.1007/s00213-005-0013-8.CrossRefGoogle Scholar
  52. Jainta, S., & Baccino, T. (2010). Analyzing the pupil response due to increased cognitive demand: An independent component analysis study. International Journal of Psychophysiology, 77, 1–7.CrossRefPubMedGoogle Scholar
  53. Janisse, P. (1974). Pupillary dynamics and behavior. New York: Plenum.CrossRefGoogle Scholar
  54. Janisse, P. (1977). Pupillometry: The psychology of the pupillary response. Hemisphere Publishing, Wiley.Google Scholar
  55. Joshi, S., Li, Y., Kalwani, R. M., & Gold, J. I. (2016). Relationships between pupil diameter and neuronal activity in the Locus coeruleus, Colliculi, and Cingulate Cortex. Neuron, 89(1), 221–234.  https://doi.org/10.1016/j.neuron.2015.11.028.CrossRefPubMedGoogle Scholar
  56. Just, M. A., & Carpenter, P. A. (1992). A capacity theory of comprehension: Individual differences in working memory. Psychological Review, 99(1), 122–149.  https://doi.org/10.1037/0033-295x.99.1.122.CrossRefPubMedGoogle Scholar
  57. Just, M. A., & Carpenter, P. A. (1993). The intensity dimension of thought: Pupillometric indices of sentence processing. Canadian Journal of Experimental Psychology, 47, 310–339.CrossRefPubMedGoogle Scholar
  58. Just, M. A., Carpenter, P. A., & Miyake, A. (2003). Neuroindices of cognitive workload: Neuroimaging, pupillometric and event-related potential studies of brain work. Theoretical Issues in Ergonomics Science, 4, 56–88.  https://doi.org/10.1080/14639220210159735.CrossRefGoogle Scholar
  59. Kahneman, D. (1973). Attention and effort. Englewood Cliffs, New Jersey: Prentice Hall.Google Scholar
  60. Kahneman, D. (2011). Thinking, fast and slow. New York: Farrar, Strauss, Giroux.Google Scholar
  61. Kahneman, D., & Beatty, J. (1966). Pupil diameter and load on memory. Science, 154, 1583–1585.CrossRefPubMedGoogle Scholar
  62. Kahneman, D., & Beatty, J. (1967). Pupillary responses in a pitch-discrimination task. Perception and Psychophysics, 2, 101–105.CrossRefGoogle Scholar
  63. Kahneman, D., Beatty, J., & Pollack, I. (1967). Perceptual deficit during a mental task. Science, 157, 218–219.CrossRefPubMedGoogle Scholar
  64. Kahneman, D., & Peavler, W. S. (1969). Incentive effects and pupillary changes in association learning. Journal of Experimental Psychology, 79, 312–318.CrossRefPubMedGoogle Scholar
  65. Kahneman, D., Tursky, B., Shapiro, D., & Crider, A. (1969). Pupillary, heart rate, and skin resistance changes during a mental task. Journal of Experimental Psychology, 79(1), 164–167.CrossRefPubMedGoogle Scholar
  66. Kawasaki, A., & Kardon, R. H. (2007). Intrinsically photosensitive retinal ganglion cells. Journal of Neuro-Ophthalmology, 27(3), 195–204.CrossRefGoogle Scholar
  67. King, A. S. (1972). Pupil size, eye direction, and message appeal: Some preliminary findings. Journal of Marketing, 36(3), 55–58.CrossRefGoogle Scholar
  68. Koss, M. C. (1986). Pupillary dilation as an index of central nervous system alpha 2-adrenoceptor activation. Journal of Pharmacological Methods, 15, 1–19.CrossRefPubMedGoogle Scholar
  69. Krugman, H. E. (1965). The impact of television advertising: Learning without involvement. Public Opinion Quarterly, 29(3), 349–356.CrossRefGoogle Scholar
  70. Laeng, B., & Endestad, T. (2013). Bright illusions reduce the eye’s pupil. PNAS, 109, 2162–2167.CrossRefGoogle Scholar
  71. Laeng, B., Eidet, L. M., Sulutvedt, U., & Panksepp, J. (2016). Music chills: The eye pupil as a mirror to music’s soul. Consciousness and Cognition, 44, s 161–178.  https://doi.org/10.1016/j.concog.2016.07.009. ISSN 1053-8100.CrossRefPubMedGoogle Scholar
  72. Laeng, B., Sirois, S., & Gredeback, G. (2012). Pupillometry: A window to the preconscious? Perspectives on Psychological Science, 7(1), 18–27. https://doi.org/10.1177/1745691611427305.CrossRefPubMedGoogle Scholar
  73. Laeng, B., Suegami, T., & Aminihajibashi, S. (2016). Wine labels: An eye-tracking and pupillometry study. International Journal of Wine Business Research, 28(4), 327–348.CrossRefGoogle Scholar
  74. Laeng, B., & Sulutvedt, U. (2014). The eye pupil adjusts to imaginary light. Psychological Science, 25(1), 188–197.  https://doi.org/10.1177/0956797613503556.CrossRefPubMedGoogle Scholar
  75. Laeng, B., Waterloo, K., Johnsen, S. H., Bakke, S. J., Låg, T., Simonsen, S. S., et al. (2007). The eyes remember it: Oculography and pupillometry during recollection in three amnesic patients. Journal of Cognitive Neuroscience, 19(11), 1888–1904.  https://doi.org/10.1162/jocn.2007.19.11.1888.CrossRefPubMedGoogle Scholar
  76. Laeng, B., Ørbo, M., Holmlund, T., & Miozzo, M. (2011). Pupillary stroop effects. Cognitive Processing, 12(1), 13–21.  https://doi.org/10.1007/s10339-010-0370-z.CrossRefPubMedGoogle Scholar
  77. Landgraf, S., Meer, E., & Krueger, F. (2010). Cognitive resource allocation for neural activity underlying mathematical cognition: A multi-method study. ZDM Mathematics Education, 42(6), 579–590.  https://doi.org/10.1007/s11858-010-0264-7.CrossRefGoogle Scholar
  78. Lavie, P. (1979). Ultradian rhythms in alertness: A pupillometric study. Biological Psychology, 9, 49–62.CrossRefPubMedGoogle Scholar
  79. Lee, D. H., Susskind, J. M., & Anderson, A. K. (2013). Social transmission of the sensory benefits of eye widening in fear expressions. Psychological Science, 24(6), 957–965.CrossRefPubMedGoogle Scholar
  80. Libby, W. L., Lacey, B. C., & Lacey, J. I. (1973). Pupillary and cardiac activity during visual attention. Psychophysiology, 10(3), 270–294.CrossRefPubMedGoogle Scholar
  81. Loewenfeld. (1958). Mechanisms of reflex dilatation of the pupil. Historical review and experimental analysis. Documenta Ophthalmologica, 12, 185.CrossRefPubMedGoogle Scholar
  82. Loewenfeld, I. E. (1999). The pupil: Anatomy, physiology, and clinical applications. Boston (MA): Butterworth Heinemann.Google Scholar
  83. Lowenstein, O., Feinberg, R., & Loewenfeld, I. E. (1963). Pupillary movements during acute and chronic fatigue. Investigative Ophthalmology & Visual Science, 2, 138–157.Google Scholar
  84. Lowenstein, O., & Loewenfeld, I. E. (1958). Electronic pupillography. A new instrument and some clinical applications. AMA Archives of Ophthalmology, 59, 352.Google Scholar
  85. MacLachlan, C., & Howland, H. C. (2002). Normal values and standard deviations for pupil diameter and interpupillary distance in subjects aged 1 month to 19 years. Ophthalmic and Physiological Optics, 22, 175–182.CrossRefGoogle Scholar
  86. Martinez-Conde, S. (2006). Fixational eye movements in normal and pathological vision. In S. Martinez-Conde, S. Macknik, L. M. Martinez, L. M. Alonso, & P. Tse (Eds.), Progress in brain research (Vol. 154). Elsevier B.V.Google Scholar
  87. McConkie, G. W., Kerr, P. W., Reddix, M. D., & Zola, D. (1988). Eye movement control during reading: I. The location of initial eye fixations on words. Vision Research, 28, 1107–1118.CrossRefPubMedGoogle Scholar
  88. McDougal, D. H. M., & Gamlin, P. D. R. (2008). Pupillary control pathways. In R. H. Masland, & T. Albright (Eds.), The senses: A comprehensive reference (pp. 521–536). San Diego, California: Academic Press.Google Scholar
  89. Moulden, B., Kingdom, F., & Gatley, L. F. (1990). The standard deviation of luminance as a metric for contrast in random-dot images. Perception, 19(1), 79–101.CrossRefPubMedGoogle Scholar
  90. Mouton, P. R., Pakkenberg, B., Gundersen, H. J., & Price, D. L. (1994). Absolute number and size of pigmented locus coeruleus neurons in young and aged individuals. Journal of Chemical Neuroanatomy, 7, 185–190.CrossRefPubMedGoogle Scholar
  91. Murphy, P. R., O’Connell, R. G., O’Sullivan, M., Robertson, I. H., & Balsters, J. H. (2014). Pupil diameter covaries with BOLD activity in human locus coeruleus. Human Brain Mapping, n/a–n/a.  https://doi.org/10.1002/hbm.22466.CrossRefPubMedGoogle Scholar
  92. Murphy, P. R., Robertson, I. H., Balsters, J. H., & O’Connell, R. G. (2011). Pupillometry and P3 index the locus coeruleus-noradrenergic arousal function in humans. Psychophysiology, 48, 1532–1543.  https://doi.org/10.1111/j.1469-8986.2011.01226.x.CrossRefPubMedGoogle Scholar
  93. Murray, R. B., Adler, M. W., & Korczyn, A. D. (1983). The pupillary effects of opioids. Life Sciences, 33, 495–509.CrossRefPubMedGoogle Scholar
  94. Navon, D. (1984). Resources—A theoretical soup stone? Psychological Review, 91(2), 216–234.CrossRefGoogle Scholar
  95. Nieuwenhuis, S., Aston-Jones, G., & Cohen, J. D. (2005). Decision making, the P3, and the locus coeruleus-norepinephrine system. Psychological Bulletin, 131, 510–532.  https://doi.org/10.1037/0033-2909.131.4.510.CrossRefPubMedGoogle Scholar
  96. Owen, A. M., & Coelman, M. R. (2006). Functional neuroimaging of the vegetative state. Nature Reviews Neuroscience, 9, 235–243.  https://doi.org/10.1038/nrn2330.CrossRefGoogle Scholar
  97. Papesh, M. H., & Goldinger, S. D. (2012). Pupil-BLAH-metry: Cognitive effort in speech planning reflected by pupil dilation. Attention, Perception, & Psychophysics, 74(4), 754–765.  https://doi.org/10.3758/s13414-011-0263-y.CrossRefGoogle Scholar
  98. Payne, D. T., Parry, M. E., & Harasymiw, S. J. (1967). A comparison of percentage of pupillary dilation with other measures of difficulty of mental multiplication items. Research Bulletin (67-42). Princeton, NJ: Educational Testing Service. http://onlinelibrary.wiley.com/doi/10.1002/j.2333-8504.1967.tb00551.x/pdf.
  99. Payne, D. T., Parry, M. E., & Harasymiw, S. J. (1968). Percentage pupillary dilation as a measure of item difficulty. Perception and Psychophysics, 4, 139–143.CrossRefGoogle Scholar
  100. Peavler, W. S. (1974). Pupil size, information overload, and performance differences. Psychophysiology, 11, 559–566.  https://doi.org/10.1111/j.1469-8986.1974.tb01114.x.CrossRefPubMedGoogle Scholar
  101. 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, 150, 85–89.Google Scholar
  102. Poock, G. K. (1973). Information processing vs pupil diameter. Perceptual and Motor Skills, 37(3), 1000–1002.CrossRefPubMedGoogle Scholar
  103. Porter, G., & Troscianko, T. (2003). Pupillary response to grating stimuli. Perception, 32, 156.Google Scholar
  104. Porter, G., Troscianko, T., & Gilchrist, I. D. (2007). Effort during visual search and counting: Insights from pupillometry. Quarterly Journal of Experimental Psychology, 60(2), 211–229.  https://doi.org/10.1080/17470210600673818.CrossRefGoogle Scholar
  105. Raizada, R. D. S., & Poldrack, R. a. (2008). Challenge-driven attention: Interacting frontal and brainstem systems. Frontiers in Human Neuroscience, 1, 3.  https://doi.org/10.3389/neuro.09.003.2007.
  106. Rajkowski, K., Kubiak, P., & Aston-Jones, G. (1993). Correlations between Locus coeruleus (LC) neural activity, pupil diameter and behavior in monkey support a role of LC in attention. Society of Neuroscience Abstracts, 974.Google Scholar
  107. Richman, J. E., Golden McAndrew, K., Decker., & Mullaney, S. (2004). An evaluation of pupil size standards used by police officers for detecting drug impairment. Optometry, 75, 2–8.Google Scholar
  108. Samuels, E. R., & Szabadi, E. (2008). Functional neuroanatomy of the noradrenergic Locus coeruleus: Its roles in the regulation of arousal and autonomic function. Current Neuropharmacology, 6, 235–253.CrossRefPubMedPubMedCentralGoogle Scholar
  109. Sara, S. J. (2009). The locus coeruleus and noradrenergic modulation of cognition. Nature Reviews Neuroscience, 10, 211–223.  https://doi.org/10.1038/nrn2573.CrossRefPubMedGoogle Scholar
  110. Sara, S. J., & Bouret, S. (2012). Orienting and reorienting: The Locus coeruleus mediates cognition through arousal. Neuron, 76, 130–141.  https://doi.org/10.1016/j.neuron.2012.09.011.CrossRefPubMedGoogle Scholar
  111. Sarter, M., Gehring, W. J., & Kozak, R. (2006). More attention must be paid: The neurobiology of attentional effort. Brain Research Reviews, 51, 145–160.  https://doi.org/10.1016/j.brainresrev.2005.11.002.CrossRefPubMedGoogle Scholar
  112. Scholl, B. J. (2009). What have we learned about attention from multiple-object tracking (and vice versa)? In D. Dedrick & L. Trick (Eds.), Computation, cognition, and Pylyshyn (pp. 49–77). Cambridge, MA: MIT Press.Google Scholar
  113. Schwalm, M., Keinath, A., & Zimmer, H. (2008). Pupillometry as a method for measuring mental workload within a simulated driving task. In D. de Waard, F. O. Flemisch, B. Lorenz, H. Oberheid, & K. A. Brookhuis (Eds.), Human factors for assistance and automation (pp. 1–13). Maastricht, The Netherlands: Shaker Publishing.Google Scholar
  114. Siegle, G. J., Steinhauer, S. R., Stenger, V. A., Konecky, R., & Carter, C. S. (2003). Use of concurrent pupil dilation assessment to inform interpretation and analysis of fMRI data. Neuroimage, 20, 114–124.  https://doi.org/10.1016/s1053-8119(03)00298-2.CrossRefPubMedGoogle Scholar
  115. Silverman, J., Mooney, J. M., & Shepherd, F. D. (1992, March). Infrared video cameras. Scientific American, 78–83.Google Scholar
  116. Simms, T. M. (1967). Pupillary response of male and female subjects to pupillary difference in male and female picture stimuli. Perception & Psychophysics, 2(11), 533–555.CrossRefGoogle Scholar
  117. Steinhauer, S. R., Siegle, G. J., Condray, R., & Pless, M. (2004). Sympathetic and parasympathetic innervation of pupillary dilation during sustained processing. International Journal of Psychophysiology, 52, 77–86.Google Scholar
  118. Susskind, J. M., Lee, D. H., Cusi, A., Feiman, R., Grabski, W., & Anderson, A. K. (2008). Expressing fear enhances sensory acquisition. Nature Neuroscience, 11, 843–850.  https://doi.org/10.1038/nn.2138.CrossRefPubMedGoogle Scholar
  119. Suzuki, T. W., Kunimatsu, J., & Tanaka, M. (2016). Correlation between pupil size and subjective passage of time in non-human primates. The Journal of Neuroscience, 36(44), 11331–11337.Google Scholar
  120. Svensson, T. H. (1987). Peripheral, autonomic regulation of locus coeruleus noradrenergic neurons in brain: Putative implications for psychiatry and psychopharmacology. Psychopharmacology, 92, 1–7.CrossRefPubMedGoogle Scholar
  121. Szabadi, E. (2012). Modulation of physiological reflexes by pain: role of the locus coeruleus. Frontiers in Integrative Neuroscience, 6, 94.  https://doi.org/10.3389/fnint.2012.00094.CrossRefPubMedPubMedCentralGoogle Scholar
  122. Tsukahara, J. S., Harrison, T. L., & Engle, R. W. (2016). The relationship between baseline pupil size and intelligence. Cognitive Psychology, 91, 109–123.Google Scholar
  123. Ueda, T., Nawa, Y., Yukawa, E., Taketani, F., & Hara, Y. (2006). Change in dynamic visual acuity (DVA) by pupil dilation. Human Factors: The Journal of the Human Factors and Ergonomics Society, 48, 651–655.CrossRefGoogle Scholar
  124. Unsworth, N., & Robison, M. K. (2017). A Locus coeruleus-norepinephrine account of individual differences in working memory capacity and attention control. Psychonomic Bulletin and Review.Google Scholar
  125. van der Meer, E., Beyer, R., Horn, J., Foth, M., Bornemann, B., Ries, J., … Wartenburger, I. (2010). Resource allocation and fluid intelligence: Insights from pupillometry. Psychophysiology, 47, 158–169.  https://doi.org/10.1111/j.1469-8986.2009.00884.x.CrossRefPubMedGoogle Scholar
  126. Wang, C.-A., & Munoz, D. P. (2014). Modulation of stimulus contrast on the human pupil orienting response. European Journal of Neuroscience, 40, 2822–2832.CrossRefPubMedGoogle Scholar
  127. Warga, M., Lüdtke, H., Wilhelm, H., & Wilhelm, B. J. (2009). How do spontaneous pupillary oscillations in light relate to light intensity. Vision Research, 49, 295–300.CrossRefPubMedGoogle Scholar
  128. Watson, A. B., & Yellott, J. I. (2012). A unified formula for light-adapted pupil size. Journal of Vision, 12(10), 1–16.Google Scholar
  129. Whipple, B., Ogden, G., & Komisaruk, B. R. (1992). Physiological Correlates of Imagery: Induced Orgasm in Women. Archives of Sexual Behavior, 21(2), 121–133.CrossRefPubMedGoogle Scholar
  130. Wilhelm, B., Wilhelm, H., & Lüdtke, H. (1999). Pupillography: Principles and applications in basic and clinical research. In J. Kuhlmann & M. Böttcher (Eds.), (pp. 1–10). München, Germany: Zuckscjwerdt Verlag.Google Scholar
  131. Wilhelm, B. J., Wilhelm, H., Moro, S., & Barbur, J. L. (2002). Pupil response components: Studies in patients with Parinaud’s syndrome. Brain, 125, 2296–2307.CrossRefPubMedGoogle Scholar
  132. Winn, B., Whitaker, D., Elliott, D. B., & Phillips, N. J. (1994). Factors affecting light-adapted pupil size in normal human subjects. Investigative Ophthalmology & Visual Science, 35(3), 1132–1137.Google Scholar
  133. Wu, E. X. W., Laeng, B., & Magnussen, S. (2011). Through the eyes of the own-race bias: Eyetracking and pupillometry during face recognition. Social Neuroscience.  https://doi.org/10.1080/17470919.2011.596946.CrossRefPubMedGoogle Scholar
  134. Zekveld, A. a., Heslenfeld, D. J., Johnsrude, I. S., Versfeld, N. J., & Kramer, S. E. (2014). The eye as a window to the listening brain: Neural correlates of pupil size as a measure of cognitive listening load. Neuroimage.  https://doi.org/10.1016/j.neuroimage.2014.06.069.CrossRefPubMedGoogle Scholar
  135. Zekveld, A. a., Kramer, S. E., & Festen, J. M. (2010). Pupil response as an indication of effortful listening: The influence of sentence intelligibility. Ear and hearing, 31(4), 480–490.  https://doi.org/10.1097/aud.0b013e3181d4f251.CrossRefPubMedGoogle Scholar
  136. Zénon, A. (2017). Time-domain analysis for extracting fast-paced pupil responses. Scientific Reports, 7, 41484.  https://doi.org/10.1038/srep41484.
  137. Zhu, Y., Iba, M., Rajkowski, J., & Aston-Jones, G. (2004). Projection from the orbitofrontal cortex to the locus coeruleus in monkeys revealed by anterograde tracing. Society of Neuroscience Abstracts, 30, 211–213.Google Scholar
  138. Zylberberg, A., Oliva, M., & Sigman, M., (2012). Pupil dilation: A fingerprint of temporal selection during the Attentional Blink. Frontiers in Psychology, 3(316).  https://doi.org/10.3389/fpsyg.2012.00316.

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of OsloOsloNorway

Personalised recommendations