Pupil size tracks perceptual content and surprise

European Journal of Neuroscience

Volumn 41, Issue 8, 2015, Pages 1068-1078

  Kloosterman, Niels A ^a   Meindertsma, Thomas ^a,b   van Loon, Anouk M ^a,c   Lamme, Victor A F ^a   Bonneh, Yoram S ^d   Donner, Tobias H ^a,e  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

^d UNIVERSITY OF HAIFA   (Israel)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Brain state; Human; Perceptual bistability; Perceptual decision making; Pupillometry

Indexed keywords

ACTION POTENTIAL; ADULT; ARTICLE; BRAIN FUNCTION; BRAIN STEM; COGNITION; EVENT RELATED POTENTIAL; EYE POSITION; EYE TRACKING; FEMALE; HUMAN; HUMAN EXPERIMENT; MAGNETOENCEPHALOGRAPHY; MALE; MOTOR PERFORMANCE; NERVOUS SYSTEM PARAMETERS; NORMAL HUMAN; PERCEPTION; PRIORITY JOURNAL; PUPIL; PUPIL REFLEX; TASK PERFORMANCE; VISUAL STIMULATION; MIDDLE AGED; MOVEMENT PERCEPTION; PHYSIOLOGY; VISION; YOUNG ADULT;

ADULT; FEMALE; HUMANS; MALE; MIDDLE AGED; MOTION PERCEPTION; PUPIL; VISUAL PERCEPTION; YOUNG ADULT;

EID: 84928090885     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12859     Document Type: Article

References (51)

1. Aston-Jones, G. & Cohen, J.D. (2005) An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu. Rev. Neurosci., 28, 403-450.
2. Bárány, E.H. & Halldén, U. (1948) Phasic inhibition of the light reflex of the pupil during retinal rivalry. J. Neurophysiol., 11, 25-30.
3. Bonneh, Y.S. & Donner, T.H. (2011) Motion induced blindness. Scholarpedia, 6, 3321.
4. Bonneh, Y.S., Cooperman, A. & Sagi, D. (2001) Motion-induced blindness in normal observers. Nature, 411, 798-801.
5. Bonneh, Y.S., Donner, T.H., Cooperman, A., Heeger, D.J. & Sagi, D. (2014) Motion-induced blindness and troxler fading: common and different mechanisms. PLoS One, 9, e92894.
6. Donner, T.H., Sagi, D., Bonneh, Y.S. & Heeger, D.J. (2008) Opposite neural signatures of motion-induced blindness in human dorsal and ventral visual cortex. J. Neurosci., 28, 10298-10310.
7. Donner, T.H., Sagi, D., Bonneh, Y.S. & Heeger, D.J. (2013) Retinotopic patterns of correlated fluctuations in visual cortex reflect the dynamics of spontaneous perceptual suppression. J. Neurosci., 33, 2188-2198.
8. Efron, B. & Tibshirani, R. (1998) An Introduction to the Bootstrap. Chapman & Hall/CRC, Boca Raton.
9. Einhauser, W., Stout, J., Koch, C. & Carter, O. (2008) Pupil dilation reflects perceptual selection and predicts subsequent stability in perceptual rivalry. Proc. Natl. Acad. Sci. USA, 105, 1704-1709.
10. Einhauser, W., Koch, C. & Carter, O.L. (2010) Pupil dilation betrays the timing of decisions. Front. Hum. Neurosci., 4, 18.
11. Eldar, E., Cohen, J.D. & Niv, Y. (2013) The effects of neural gain on attention and learning. Nat. Neurosci., 16, 1146-1153.
12. Fahle, M.W., Stemmler, T. & Spang, K.M. (2011) How much of the "unconscious" is just pre-threshold? Front. Hum. Neurosci., 5, 120.
13. Fiedler, S. & Glockner, A. (2012) The dynamics of decision making in risky choice: an eye-tracking analysis. Front. Psychol., 3, 335.
14. Frassle, S., Sommer, J., Jansen, A., Naber, M. & Einhauser, W. (2014) Binocular rivalry: frontal activity relates to introspection and action but not to perception. J. Neurosci., 34, 1738-1747.
15. Friston, K. (2010) The free-energy principle: a unified brain theory? Nat. Rev. Neurosci., 11, 127-138.
16. de Gee, J.W., Knapen, T. & Donner, T.H. (2014) Decision-related pupil dilation reflects upcoming choice and individual bias. Proc. Natl. Acad. Sci. USA, 111, E618-E625.
17. 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. Cogn. Affect. Behav. Ne., 10, 252-269.
18. Green, D.M. & Swets, J.A. (1966) Signal detection theory and psychophysics. Wiley, New York.
19. Hess, E.H. & Polt, J.M. (1964) Pupil size in relation to mental activity during simple problem-solving. Science, 143, 1190-1192.
20. Hoeks, B. & Levelt, W.J.M. (1993) Pupillary dilation as a measure of attention: a quantitative systems analysis. Behav. Res. Meth. Ins. C., 25, 16-26.
21. Hupe, J.M., Lamirel, C. & Lorenceau, J. (2009) Pupil dynamics during bistable motion perception. J. Vision, 9, 10.
22. Kahneman, D. & Beatty, J. (1966) Pupil diameter and load on memory. Science, 154, 1583-1585.
23. Kloosterman, N.A., Meindertsma, T., Hillebrand, A., van Dijk, B.W., Lamme, V.A.F. & Donner, T.H. (2015) Top-down modulation in human visual cortex predicts the stability of a perceptual illusion. J. Neurophysiol., 113, 1063-1076.
24. Laeng, B. & Endestad, T. (2012) Bright illusions reduce the eye's pupil. Proc. Natl. Acad. Sci. USA, 109, 2162-2167.
25. Laeng, B. & Sulutvedt, U. (2014) The eye pupil adjusts to imaginary light. Psychol. Sci., 25, 188-197.
26. Lee, S.H. & Dan, Y. (2012) Neuromodulation of brain states. Neuron, 76, 209-222.
27. Loewenfeld, I.E. & Lowenstein, O. (1993) The pupil: anatomy, physiology, and clinical applications. Iowa State University Press, Ames.
28. van Loon, A.M., Knapen, T., Scholte, H.S., St John-Saaltink, E., Donner, T.H. & Lamme, V.A. (2013) GABA shapes the dynamics of bistable perception. Curr. Biol., 23, 823-827.
29. Lowe, S.W. & Ogle, K.N. (1966) Dynamics of the pupil during binocular rivalry. Arch. Ophthalmol.-Chic., 75, 395-403.
30. Luce, R.D. (1986) Response time: their role in inferring elementary mental organization. Oxford University Press, New York.
31. Maris, E. & Oostenveld, R. (2007) Nonparametric statistical testing of EEG- and MEG-data. J. Neurosci. Meth., 164, 177-190.
32. Mathot, S., van der Linden, L., Grainger, J. & Vitu, F. (2013) The pupillary light response reveals the focus of covert visual attention. PLoS One, 8, e78168.
33. 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.
34. 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. Hum. Brain Mapp., 35, 4140-4154.
35. Naber, M., Frassle, S. & Einhauser, W. (2011) Perceptual rivalry: reflexes reveal the gradual nature of visual awareness. PLoS One, 6, e20910.
36. Naber, M., Frassle, S., Rutishauser, U. & Einhauser, W. (2013) Pupil size signals novelty and predicts later retrieval success for declarative memories of natural scenes. J. Vision, 13, 11.
37. Nassar, M.R., Rumsey, K.M., Wilson, R.C., Parikh, K., Heasly, B. & Gold, J.I. (2012) Rational regulation of learning dynamics by pupil-linked arousal systems. Nat. Neurosci., 15, 1040-1046.
38. Oostenveld, R., Fries, P., Maris, E. & Schoffelen, J.M. (2011) FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput. Intell. Neurosci., 2011, 156869.
39. Parikh, V., Kozak, R., Martinez, V. & Sarter, M. (2007) Prefrontal acetylcholine release controls cue detection on multiple timescales. Neuron, 56, 141-154.
40. Pinto, L., Goard, M.J., Estandian, D., Xu, M., Kwan, A.C., Lee, S.-H., Harrison, T.C., Feng, G. & Dan, Y. (2013) Fast modulation of visual perception by basal forebrain cholinergic neurons. Nat. Neurosci., 16, 1857-1863.
41. Preuschoff, K., 't Hart, B.M. & Einhauser, W. (2011) Pupil dilation signals surprise: evidence for noradrenaline's role in decision making. Front. Neurosci., 5, 115.
42. Reimer, J., Froudarakis, E., Cadwell, C.R., Yatsenko, D., Denfield, G.H. & Tolias, A.S. (2014) Pupil fluctuations track fast switching of cortical states during quiet wakefulness. Neuron, 84, 355-362.
43. Ress, D., Backus, B.T. & Heeger, D.J. (2000) Activity in primary visual cortex predicts performance in a visual detection task. Nat. Neurosci., 3, 940-945.
44. Sarter, M., Parikh, V. & Howe, W.M. (2009) Phasic acetylcholine release and the volume transmission hypothesis: time to move on. Nat. Rev. Neurosci., 10, 383-390.
45. Shalom, D.E., de Sousa Serro, M.G., Giaconia, M., Martinez, L.M., Rieznik, A. & Sigman, M. (2013) Choosing in freedom or forced to choose? Introspective blindness to psychological forcing in stage-magic PLoS One, 8, e58254.
46. Wang, C.A. & Munoz, D.P. (2014) Modulation of stimulus contrast on the human pupil orienting response. Eur. J. Neurosci., 40, 2822-2832.
47. Wang, C.A., Boehnke, S.E., White, B.J. & Munoz, D.P. (2012) Microstimulation of the monkey superior colliculus induces pupil dilation without evoking saccades. J. Neurosci., 32, 3629-3636.
48. Wierda, S.M., van Rijn, H., Taatgen, N.A. & Martens, S. (2012) Pupil dilation deconvolution reveals the dynamics of attention at high temporal resolution. Proc. Natl. Acad. Sci. USA, 109, 8456-8460.
49. de-Wit, L.H., Kubilius, J., Wagemans, J. & de Beeck, H.P.O. (2012) Bistable Gestalts reduce activity in the whole of V1, not just the retinotopically predicted parts. J. Vision, 12, 12.
50. Yu, A.J. (2012) Change is in the eye of the beholder. Nat. Neurosci., 15, 933-935.
51. Zylberberg, A., Oliva, M. & Sigman, M. (2012) Pupil dilation: a fingerprint of temporal selection during the "attentional blink". Front. Psychol., 3, 316.