The effects of life stress and neural learning signals on fluid intelligence

详细信息    查看全文

• 作者：Eva Friedel (1)
  Florian Schlagenhauf (1) (2)
  Anne Beck (1)
  Raymond J. Dolan (3)
  Quentin J.M. Huys (3) (4) (5)
  Michael A. Rapp (1) (6)
  Andreas Heinz (1) (7)
  
  1. Department of Psychiatry and Psychotherapy ; Charit茅 鈥?Universit盲tsmedizin Berlin ; Campus Charit茅 Mitte ; Charit茅platz 1 ; 10117 ; Berlin ; Germany
  2. Max Planck Institute for Human Cognitive and Brain Sciences ; Leipzig ; Germany
  3. Gatsby Computational Neuroscience Unit ; University College London ; London ; UK
  4. Translational Neuromodeling Unit ; Institute for Biomedical Engineering ; University of Zurich and ETH Zurich ; Zurich ; Switzerland
  5. Department of Psychiatry ; Psychotherapy and Psychosomatics ; University Hospital of Psychiatry ; Zurich ; Switzerland
  6. Social and Preventive Medicine ; University of Potsdam ; Potsdam ; Germany
  7. Cluster of Excellence NeuroCure ; Charite-Universit盲tsmedizin Berlin ; Berlin ; Germany
  
• 关键词：Reinforcement learning ; Prediction error signal ; Ventral striatum ; Stress ; Intelligence
• 刊名：European Archives of Psychiatry and Clinical Neuroscience
• 出版年：2015
• 出版时间：February 2015
• 年：2015
• 卷：265
• 期：1
• 页码：35-43
• 全文大小：411 KB
• 参考文献：1. Horn JL, Cattell RB (1966) Age differences in primary mental ability factors. J Gerontol 21(2):210鈥?20 CrossRef
  2. Sternberg RJ (2000) The holey grail of general intelligence. Science 289(5478):399鈥?01 CrossRef
  3. Montague PR, Dayan P, Sejnowski TJ (1996) A framework for mesencephalic dopamine systems based on predictive Hebbian learning. J Neurosci 16(5):1936鈥?947
  4. Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275(5306):1593鈥?599 CrossRef
  5. D鈥橝rdenne K, McClure SM, Nystrom LE, Cohen JD (2008) BOLD responses reflecting dopaminergic signals in the human ventral tegmental area. Science 319(5867):1264鈥?267. doi:10.1126/science.1150605 CrossRef
  6. O鈥橠oherty J, Dayan P, Schultz J, Deichmann R, Friston K, Dolan RJ (2004) Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304(5669):452鈥?54. doi:10.1126/science.1094285 CrossRef
  7. Sutton RBA (1998) Reinforcement Learning: An Introduction. A Bradford Book, Cambridge
  8. Daw ND, Niv Y, Dayan P (2005) Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control. Nat Neurosci 8(12):1704鈥?711. doi:10.1038/nn1560 CrossRef
  9. Morris G, Nevet A, Arkadir D, Vaadia E, Bergman H (2006) Midbrain dopamine neurons encode decisions for future action. Nat Neurosci 9(8):1057鈥?063. doi:10.1038/nn1743 CrossRef
  10. Schultz W (2010) Multiple functions of dopamine neurons. F1000 biology reports 2. doi:10.3410/B2-2
  11. Schott BH, Minuzzi L, Krebs RM, Elmenhorst D, Lang M, Winz OH, Seidenbecher CI, Coenen HH, Heinze HJ, Zilles K, Duzel E, Bauer A (2008) Mesolimbic functional magnetic resonance imaging activations during reward anticipation correlate with reward-related ventral striatal dopamine release. J Neurosci 28(52):14311鈥?4319. doi:10.1523/JNEUROSCI.2058-08.2008 CrossRef
  12. Schlagenhauf F, Rapp MA, Huys QJ, Beck A, Wustenberg T, Deserno L, Buchholz HG, Kalbitzer J, Buchert R, Bauer M, Kienast T, Cumming P, Plotkin M, Kumakura Y, Grace AA, Dolan RJ, Heinz A (2013) Ventral striatal prediction error signaling is associated with dopamine synthesis capacity and fluid intelligence. Hum Brain Mapp 34(6):1490鈥?499. doi:10.1002/hbm.22000 CrossRef
  13. Schlagenhauf F, Rapp MA, Huys QJ, Beck A, Wustenberg T, Deserno L, Buchholz HG, Kalbitzer J, Buchert R, Bauer M, Kienast T, Cumming P, Plotkin M, Kumakura Y, Grace AA, Dolan RJ, Heinz A (2012) Ventral striatal prediction error signaling is associated with dopamine synthesis capacity and fluid intelligence. Hum Brain Mapp. doi:10.1002/hbm.22000
  14. Robinson OJ, Overstreet C, Charney DR, Vytal K, Grillon C (2013) Stress increases aversive prediction error signal in the ventral striatum. Proc Natl Acad Sci USA 110(10):4129鈥?133. doi:10.1073/pnas.1213923110 CrossRef
  15. Garrett DD, Grady CL, Hasher L (2010) Everyday memory compensation: the impact of cognitive reserve, subjective memory, and stress. Psychol Aging 25(1):74鈥?3. doi:10.1037/a0017726 CrossRef
  16. Otto AR, Raio CM, Chiang A, Phelps EA, Daw ND (2013) Working-memory capacity protects model-based learning from stress. Proc Natl Acad Sci USA 110(52):20941鈥?0946. doi:10.1073/pnas.1312011110 CrossRef
  17. Cavanagh JF, Frank MJ, Allen JJ (2011) Social stress reactivity alters reward and punishment learning. Soc Cogn Affect Neurosci 6(3):311鈥?20. doi:10.1093/scan/nsq041 CrossRef
  18. Petzold A, Plessow F, Goschke T, Kirschbaum C (2010) Stress reduces use of negative feedback in a feedback-based learning task. Behav Neurosci 124(2):248鈥?55. doi:10.1037/a0018930 CrossRef
  19. Porcelli AJ, Delgado MR (2009) Acute stress modulates risk taking in financial decision making. Psychol Sci 20(3):278鈥?83. doi:10.1111/j.1467-9280.2009.02288.x CrossRef
  20. Bogdan R, Pizzagalli DA (2006) Acute stress reduces reward responsiveness: implications for depression. Biol Psychiatry 60(10):1147鈥?154. doi:10.1016/j.biopsych.2006.03.037 CrossRef
  21. Baumeister RF, Twenge JM, Nuss CK (2002) Effects of social exclusion on cognitive processes: anticipated aloneness reduces intelligent thought. J Pers Soc Psychol 83(4):817鈥?27 CrossRef
  22. Valenti O, Lodge DJ, Grace AA (2011) Aversive stimuli alter ventral tegmental area dopamine neuron activity via a common action in the ventral hippocampus. J Neurosci 31(11):4280鈥?289. doi:10.1523/JNEUROSCI.5310-10.2011 CrossRef
  23. Cao JL, Covington HE 3rd, Friedman AK, Wilkinson MB, Walsh JJ, Cooper DC, Nestler EJ, Han MH (2010) Mesolimbic dopamine neurons in the brain reward circuit mediate susceptibility to social defeat and antidepressant action. The Journal of neuroscience : the official journal of the Society for Neuroscience 30(49):16453鈥?6458. doi:10.1523/JNEUROSCI.3177-10.2010 CrossRef
  24. Lighthall NR, Sakaki M, Vasunilashorn S, Nga L, Somayajula S, Chen EY, Samii N, Mather M (2012) Gender differences in reward-related decision processing under stress. Soc Cogn Affect Neurosci 7(4):476鈥?84. doi:10.1093/scan/nsr026 CrossRef
  25. Lindenberger U, Baltes PB (1997) Intellectual functioning in old and very old age: cross-sectional results from the Berlin aging study. Psychol Aging 12(3):410鈥?32 CrossRef
  26. Reitan RM (1955) The relation of the trail making test to organic brain damage. J Consult Psychol 19:393鈥?94 CrossRef
  27. Stroop JR (1935) Studies of interference in serial verbal reactions. J Exp Psychol 18:643鈥?62 CrossRef
  28. Wechsler D (1955) Wechsler adult intelligence scale manual. Psychological Corporation, New York
  29. Beckers K, Behrends U, Canavan A (1992) Deutsche version des river mead behavioral memory test. Thames Valley Test Company, Bury St Edmunds
  30. Horn W (1983) L-P-S Leistungspr眉fsystem, vol 2. Auflage. Hogrefe, G枚ttingen
  31. Holmes THRR (1967) The social readjustment rating scale. J Psychosom Res 11(2):213鈥?18 CrossRef
  32. O鈥橠oherty JP, Hampton A, Kim H (2007) Model-based fMRI and its application to reward learning and decision making. Ann N Y Acad Sci 1104:35鈥?3. doi:10.1196/annals.1390.022 CrossRef
  33. Huys QJ, Cools R, Golzer M, Friedel E, Heinz A, Dolan RJ, Dayan P (2011) Disentangling the roles of approach, activation and valence in instrumental and pavlovian responding. Plos Comput Biol 7(4):e1002028. doi:10.1371/journal.pcbi.1002028 CrossRef
  34. Huys QJ, Eshel N, O鈥橬ions E, Sheridan L, Dayan P, Roiser JP (2012) Bonsai trees in your head: how the pavlovian system sculpts goal-directed choices by pruning decision trees. Plos Comput Biol 8(3):e1002410. doi:10.1371/journal.pcbi.1002410 CrossRef
  35. Kahnt T, Park SQ, Cohen MX, Beck A, Heinz A, Wrase J (2009) Dorsal striatal-midbrain connectivity in humans predicts how reinforcements are used to guide decisions. J Cogn Neurosci 21(7):1332鈥?345. doi:10.1162/jocn.2009.21092 CrossRef
  36. Park SQ, Kahnt T, Beck A, Cohen MX, Dolan RJ, Wrase J, Heinz A (2010) Prefrontal cortex fails to learn from reward prediction errors in alcohol dependence. J Neurosci 30(22):7749鈥?753. doi:10.1523/JNEUROSCI.5587-09.2010 CrossRef
  37. Ashburner J, Friston KJ (2005) Unified segmentation. NeuroImage 26(3):839鈥?51. doi:10.1016/j.neuroimage.2005.02.018 CrossRef
  38. Pessiglione M, Seymour B, Flandin G, Dolan RJ, Frith CD (2006) Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 442(7106):1042鈥?045. doi:10.1038/nature05051 CrossRef
  39. Bray S, O鈥橠oherty J (2007) Neural coding of reward-prediction error signals during classical conditioning with attractive faces. J Neurophysiol 97(4):3036鈥?045. doi:10.1152/jn.01211.2006 CrossRef
  40. Cohen MX, Ranganath C (2005) Behavioral and neural predictors of upcoming decisions. Cogn Affect Behav Neurosci 5(2):117鈥?26 CrossRef
  41. Cohen MX (2007) Individual differences and the neural representations of reward expectation and reward prediction error. Cogn Affect Behav Neurosci 2(1):20鈥?0. doi:10.1093/scan/nsl021 CrossRef
  42. Gershman SJ, Pesaran B, Daw ND (2009) Human reinforcement learning subdivides structured action spaces by learning effector-specific values. Journal Neurosci 29(43):13524鈥?3531. doi:10.1523/JNEUROSCI.2469-09.2009 CrossRef
  43. Krugel LK, Biele G, Mohr PN, Li SC, Heekeren HR (2009) Genetic variation in dopaminergic neuromodulation influences the ability to rapidly and flexibly adapt decisions. Proc Natl Acad Sci USA 106(42):17951鈥?7956. doi:10.1073/pnas.0905191106 CrossRef
  44. Murray GK, Corlett PR, Clark L, Pessiglione M, Blackwell AD, Honey G, Jones PB, Bullmore ET, Robbins TW, Fletcher PC (2008) Substantia nigra/ventral tegmental reward prediction error disruption in psychosis. Molecular psychiatry. 13 (3): 239, 267鈥?76. doi:10.1038/sj.mp.4002058
  45. O鈥橠oherty JP, Dayan P, Friston K, Critchley H, Dolan RJ (2003) Temporal difference models and reward-related learning in the human brain. Neuron 38(2):329鈥?37 CrossRef
  46. Palminteri S, Boraud T, Lafargue G, Dubois B, Pessiglione M (2009) Brain hemispheres selectively track the expected value of contralateral options. J Neurosci 29(43):13465鈥?3472. doi:10.1523/JNEUROSCI.1500-09.2009 CrossRef
  47. Rodriguez PF, Aron AR, Poldrack RA (2006) Ventral-striatal/nucleus-accumbens sensitivity to prediction errors during classification learning. Hum Brain Mapp 27(4):306鈥?13. doi:10.1002/hbm.20186 CrossRef
  48. Schonberg T, O鈥橠oherty JP, Joel D, Inzelberg R, Segev Y, Daw ND (2010) Selective impairment of prediction error signaling in human dorsolateral but not ventral striatum in Parkinson鈥檚 disease patients: evidence from a model-based fMRI study. NeuroImage 49(1):772鈥?81. doi:10.1016/j.neuroimage.2009.08.011 CrossRef
  49. Tobler PN, O鈥橠oherty JP, Dolan RJ, Schultz W (2006) Human neural learning depends on reward prediction errors in the blocking paradigm. J Neurophysiol 95(1):301鈥?10. doi:10.1152/jn.00762.2005 CrossRef
  50. Valentin VV, O鈥橠oherty JP (2009) Overlapping prediction errors in dorsal striatum during instrumental learning with juice and money reward in the human brain. J Neurophysiol 102(6):3384鈥?391. doi:10.1152/jn.91195.2008 CrossRef
  51. Buchel C, Holmes AP, Rees G, Friston KJ (1998) Characterizing stimulus-response functions using nonlinear regressors in parametric fMRI experiments. NeuroImage 8(2):140鈥?48. doi:10.1006/nimg.1998.0351 CrossRef
  52. Schwabe L, Wolf OT (2009) Stress prompts habit behavior in humans. J Neurosci 29(22):7191鈥?198. doi:10.1523/JNEUROSCI.0979-09.2009 CrossRef
  53. O鈥橠oherty JP (2004) Reward representations and reward-related learning in the human brain: insights from neuroimaging. Curr Opin Neurobiol 14(6):769鈥?76. doi:10.1016/j.conb.2004.10.016 CrossRef
  54. Hampton AN, Bossaerts P, O鈥橠oherty JP (2006) The role of the ventromedial prefrontal cortex in abstract state-based inference during decision making in humans. The Journal of neuroscience : the official journal of the Society for Neuroscience 26(32):8360鈥?367. doi:10.1523/JNEUROSCI.1010-06.2006 CrossRef
  55. Daw ND, Gershman SJ, Seymour B, Dayan P, Dolan RJ (2011) Model-based influences on humans鈥?choices and striatal prediction errors. Neuron 69(6):1204鈥?215. doi:10.1016/j.neuron.2011.02.027 CrossRef
  56. Morgan D, Grant KA, Gage HD, Mach RH, Kaplan JR, Prioleau O, Nader SH, Buchheimer N, Ehrenkaufer RL, Nader MA (2002) Social dominance in monkeys: dopamine D2 receptors and cocaine self-administration. Nat Neurosci 5(2):169鈥?74. doi:10.1038/nn798 CrossRef
  57. Patchev AV, Rodrigues AJ, Sousa N, Spengler D, Almeida OF (2013) The future is now: early life events pre-set adult behavior. Acta Physiol (Oxf). doi:10.1111/apha.12140
  58. Bouma EM, Riese H, Doornbos B, Ormel J, Oldehinkel AJ (2012) Genetically based reduced MAOA and COMT functioning is associated with the cortisol stress response: a replication study. Mol Psychiatry 17(2):119鈥?21. doi:10.1038/mp.2011.115 CrossRef
  59. Breiter HC, Aharon I, Kahneman D, Dale A, Shizgal P (2001) Functional imaging of neural responses to expectancy and experience of monetary gains and losses. Neuron 30(2):619鈥?39 CrossRef
  60. Cooper JC, Knutson B (2008) Valence and salience contribute to nucleus accumbens activation. NeuroImage 39(1):538鈥?47. doi:10.1016/j.neuroimage.2007.08.009 CrossRef
  61. Jabbi M, Korf J, Kema IP, Hartman C, van der Pompe G, Minderaa RB, Ormel J, den Boer JA (2007) Convergent genetic modulation of the endocrine stress response involves polymorphic variations of 5-HTT COMT and MAOA. Mol Psychiatry 12(5):483鈥?90. doi:10.1038/sj.mp.4001975
  62. Nisbett RE, Aronson J, Blair C, Dickens W, Flynn J, Halpern DF, Turkheimer E (2012) Intelligence: new findings and theoretical developments. Am Psychol 67(2):130鈥?59. doi:10.1037/a0026699 CrossRef
  63. Heinz A, Smolka MN (2006) The effects of catechol O-methyltransferase genotype on brain activation elicited by affective stimuli and cognitive tasks. Rev Neurosci 17(3):359鈥?67 CrossRef
  64. Barnett JH, Heron J, Goldman D, Jones PB, Xu K (2009) Effects of catechol-O-methyltransferase on normal variation in the cognitive function of children. Am J Psychiatry 166(8):909鈥?16. doi:10.1176/appi.ajp.2009.08081251 CrossRef
  65. Thompson JM, Sonuga-Barke EJ, Morgan AR, Cornforth CM, Turic D, Ferguson LR, Mitchell EA, Waldie KE (2012) The catechol-O-methyltransferase (COMT) Val158Met polymorphism moderates the effect of antenatal stress on childhood behavioural problems: longitudinal evidence across multiple ages. Dev Med Child Neurol 54(2):148鈥?54. doi:10.1111/j.1469-8749.2011.04129.x CrossRef
  
• 刊物类别：Medicine
• 刊物主题：Medicine & Public Health
  Psychiatry
  Neurosciences
  Neurology
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1433-8491

文摘

Fluid intelligence (fluid IQ), defined as the capacity for rapid problem solving and behavioral adaptation, is known to be modulated by learning and experience. Both stressful life events (SLES) and neural correlates of learning [specifically, a key mediator of adaptive learning in the brain, namely the ventral striatal representation of prediction errors (PE)] have been shown to be associated with individual differences in fluid IQ. Here, we examine the interaction between adaptive learning signals (using a well-characterized probabilistic reversal learning task in combination with fMRI) and SLES on fluid IQ measures. We find that the correlation between ventral striatal BOLD PE and fluid IQ, which we have previously reported, is quantitatively modulated by the amount of reported SLES. Thus, after experiencing adversity, basic neuronal learning signatures appear to align more closely with a general measure of flexible learning (fluid IQ), a finding complementing studies on the effects of acute stress on learning. The results suggest that an understanding of the neurobiological correlates of trait variables like fluid IQ needs to take socioemotional influences such as chronic stress into account.