Rational regulation of learning dynamics by pupil-linked arousal systems

Nature Neuroscience

Volumn 15, Issue 7, 2012, Pages 1040-1046

  Nassar, Matthew R ^a   Rumsey, Katherine M ^a   Wilson, Robert C ^b   Parikh, Kinjan ^a   Heasly, Benjamin ^a   Gold, Joshua I ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AROUSAL; ARTICLE; BAYES THEOREM; FEMALE; HUMAN; HUMAN EXPERIMENT; INFORMATION PROCESSING; LEARNING; MALE; MATHEMATICAL ANALYSIS; NORMAL HUMAN; PRIORITY JOURNAL; PUPIL; RELIABILITY; TASK PERFORMANCE;

ADULT; AROUSAL; FEMALE; HUMANS; LEARNING; MALE; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; PUPIL; YOUNG ADULT;

EID: 84862853075     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3130     Document Type: Article

References (35)

1. Behrens, T.E., Woolrich, M.W., Walton, M.E. & Rushworth, M.F. Learning the value of information in an uncertain world. Nat. Neurosci. 10, 1214-1221 (2007). (Pubitemid 47339952)
2. Nassar, M.R., Wilson, R.C., Heasly, B. & Gold, J.I. An approximately Bayesian delta-rule model explains the dynamics of belief updating in a changing environment. J. Neurosci. 30, 12366-12378 (2010).
3. Yu, A.J. & Dayan, P. Uncertainty, neuromodulation, and attention. Neuron 46, 681-692 (2005). (Pubitemid 40797391)
4. Nieuwenhuis, S., De Geus, E.J. & Aston-Jones, G. The anatomical and functional relationship between the P3 and autonomic components of the orienting response. Psychophysiology 2, 162-175 (2011).
5. Aston-Jones, G. & Cohen, J.D. An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu. Rev. Neurosci. 28, 403-450 (2005). (Pubitemid 41098911)
6. Jepma, M. & Nieuwenhuis, S. Pupil diameter predicts changes in the exploration-exploitation trade-off: evidence for the adaptive gain theory. J. Cogn. Neurosci. 23, 1587-1596 (2011).
7. Gilzenrat, M.S., Nieuwenhuis, S., Jepma, M. & Cohen, J.D. Pupil diameter tracks changes in control state predicted by the adaptive gain theory of locus coeruleus function. Cogn. Affect. Behav. Neurosci. 10, 252-269 (2010).
8. Krugman, H.E. Some applications of pupil measurement. J. Mark. Res. 1, 15-19 (1964).
9. Granholm, E. & Steinhauer, S.R. Pupillometric measures of cognitive and emotional processes. Int. J. Psychophysiol. 52, 1-6 (2004). (Pubitemid 38328519)
10. Schmidt, H.S. & Fortin, L.D. Electronic pupillography in disorders of arousal. in Sleeping and Waking Disorders: Indication and Technique (ed. Guilleminault, C.) 127-143 (Addison-Wesley, 1982).
11. Kahneman, D. & Beatty, J. Pupil diameter and load on memory. Science 154, 1583-1585 (1966).
12. Richer, F. & Beatty, J. Contrasting effects of response uncertainty on the task-evoked pupillary response and reaction time. Psychophysiology 24, 258-262 (1987). (Pubitemid 17071797)
13. Hakerem, G., Sutton, S. & Zubin, J. Pupillary reactions to light in schizophrenic patients and normals. Ann. NY Acad. Sci. 105, 820-831 (1964).
14. Einhäuser, W., Stout, J., Koch, C. & Carter, O. Pupil dilation reflects perceptual selection and predicts subsequent stability in perceptual rivalry. Proc. Natl. Acad. Sci. USA 105, 1704-1709 (2008). (Pubitemid 351346578)
15. Van Olst, E.H., Heemstra, M.L. & Ten Kortenaar, T. Stimulus significance and the orienting reaction. in The Orienting Reflex in Humans: International Conference Proceedings (eds. Kimmel, H., Olst, E.H. & van Orlebeke, J.F.) 521-547 (Erlbaum, 1979).
16. Sutton, R.S. & Barto, A.G. Reinforcement Learning: An Introduction (MIT Press, Cambridge, Massachusetts, 1998).
17. Adams, R.P. & MacKay, D.J.C. Bayesian online changepoint detection. Preprint at http://arxiv.org/abs/0710.3742v1 (2007).
18. Fearnhead, P. & Liu, Z. On-line inference for multiple changepoint problems. J. R. Stat. Soc. Series B Stat. Methodol. 69, 589-605 (2007).
19. Wilson, R.C., Nassar, M.R. & Gold, J.I. Bayesian online learning of the hazard rate in change-point problems. Neural Comput. 22, 2452-2476 (2010).
20. Yerkes, R.M. & Dodson, J.D. The relation of strength of stimulus to rapidity of habit-formation. J. Comp. Neurol. Psychol. 18, 459-482 (1908).
21. Behrens, T.E., Woolrich, M.W., Walton, M.E. & Rushworth, M.F. Learning the value of information in an uncertain world. Nat. Neurosci. 10, 1214-1221 (2007). (Pubitemid 47339952)
22. Raisig, S., Welke, T., Hagendorf, H. & van der Meer, E. I spy with my little eye: detection of temporal violations in event sequences and the pupillary response. Int. J. Psychophysiol. 76, 1-8 (2010).
23. Friedman, D., Hakerem, G., Sutton, S. & Fleiss, J.L. Effect of stimulus uncertainty on the pupillary dilation response and the vertex evoked potential. Electroencephalogr. Clin. Neurophysiol. 34, 475-484 (1973).
24. Preuschoff, K., 't Hart, B.M. & Einhäuser, W. Pupil dilation signals surprise: evidence for noradrenaline's role in decision making. Front. Neurosci. 5, 115 (2011).
25. Aston-Jones, G., Ennis, M., Pieribone, V.A., Nickell, W.T. & Shipley, M.T. The brain nucleus locus coeruleus: restricted afferent control of a broad efferent network. Science 234, 734-737 (1986). (Pubitemid 17184220)
26. Sara, S.J., Vankov, A. & Hervé, A. Locus coeruleus-evoked responses in behaving rats: a clue to the role of noradrenaline in memory. Brain Res. Bull. 35, 457-465 (1994). (Pubitemid 24342097)
27. Aston-Jones, G., Rajkowski, J. & Kubiak, P. Conditioned responses of monkey locus coeruleus neurons anticipate acquisition of discriminative behavior in a vigilance task. Neuroscience 80, 697-715 (1997). (Pubitemid 27334615)
28. Tully, K. & Bolshakov, V.Y. Emotional enhancement of memory: how norepinephrine enables synaptic plasticity. Mol. Brain 3, 15 (2010).
29. Harley, C.W. A role for norepinephrine in arousal, emotion and learning? Limbic modulation by norepinephrine and the Kety hypothesis. Prog. Neuropsychopharmacol. Biol. Psychiatry 11, 419-458 (1987).
30. Corbetta, M., Patel, G. & Shulman, G.L. The reorienting system of the human brain: from environment to theory of mind. Neuron 58, 306-324 (2008). (Pubitemid 351615192)
31. Bouret, S. & Sara, S.J. Network reset: a simplified overarching theory of locus coeruleus noradrenaline function. Trends Neurosci. 28, 574-582 (2005). (Pubitemid 41476687)
32. Critchley, H.D., Mathias, C.J. & Dolan, R.J. Neural activity in the human brain relating to uncertainty and arousal during anticipation. Neuron 29, 537-545 (2001). (Pubitemid 32206490)
33. Critchley, H.D. Neural mechanisms of autonomic, affective, and cognitive integration. J. Comp. Neurol. 493, 154-166 (2005). (Pubitemid 41636198)
34. Krugel, L.K., Biele, G., Mohr, P.N., Li, S.C. & Heekeren, H.R. Genetic variation in dopaminergic neuromodulation influences the ability to rapidly and flexibly adapt decisions. Proc. Natl. Acad. Sci. USA 106, 17951-17956 (2009).
35. Matsumoto, M., Matsumoto, K., Abe, H. & Tanaka, K. Medial prefrontal cell activity signaling prediction errors of action values. Nat. Neurosci. 10, 647-656 (2007). (Pubitemid 46652446)