A sensitive and specific neural signature for picture-induced negative affect

PLoS Biology

Volumn 13, Issue 6, 2015, Pages 1-28

  Chang, Luke J ^a   Gianaros, Peter J ^b   Manuck, Stephen B ^b   Krishnan, Anjali ^a   Wager, Tor D ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; AROUSAL; ARTICLE; AVERSION; BRAIN CORTEX; BRAIN FUNCTION; EMOTION; FEMALE; HUMAN; HUMAN EXPERIMENT; INSULA; MACHINE LEARNING; MALE; NORMAL HUMAN; PAIN; PICTURE INDUCED NEGATIVE EMOTION SIGNATURE; SALIENCE NETWORK; SENSITIVITY AND SPECIFICITY; SUBCORTEX; ADOLESCENT; AFFECT; BRAIN; MIDDLE AGED; NOCICEPTION; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; AFFECT; BRAIN; FEMALE; HEALTHY VOLUNTEERS; HUMANS; MACHINE LEARNING; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; PAIN PERCEPTION; SENSITIVITY AND SPECIFICITY; YOUNG ADULT;

EID: 84934756388     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002180     Document Type: Article

References (94)

1. Gross JJ, Barrett LF. Emotion Generation and Emotion Regulation: One or Two Depends on Your Point of View. Emot Rev. 2011; 3(1):8-16. PMID: 21479078
2. Suls J, Bunde J. Anger, anxiety, and depression as risk factors for cardiovascular disease: the problems and implications of overlapping affective dispositions. Psychol Bull. 2005; 131(2):260-300. PMID: 15740422
3. Tooby J, Cosmides L. The evolutionary psychology of the emotions and their relationship to internal regulatory variables. In: Lewis M, Haviland-Jones JM, Barrett LF, editors. Handbook of Emotions. 3rd ed. NY: Guilford Press; 2008.
4. Keay KA, Bandler R. Parallel circuits mediating distinct emotional coping reactions to different types of stress. Neuroscience and biobehavioral reviews. 2001; 25(7-8):669-78. PMID: 11801290
5. Price JL. Prefrontal cortical networks related to visceral function and mood. Ann N Y Acad Sci. 1999; 877:383-96. PMID: 10415660
6. Roy M, Shohamy D, Wager TD. Ventromedial prefrontal-subcortical systems and the generation of affective meaning. Trends Cogn Sci. 2012; 16(3):147-56. doi: 10. 1016/j. tics. 2012. 01. 005 PMID: 22310704
7. Davidson RJ, Irwin W. The functional neuroanatomy of emotion and affective style. Trends Cogn Sci. 1999; 3(1):11-21. PMID: 10234222
8. Ortony A, Clore GL, Collins A. The cognitive structure of emotions. Cambridge: Cambridge University Press; 1990.
9. Chang LJ, Smith A, Dufwenberg M, Sanfey AG. Triangulating the neural, psychological, and economic bases of guilt aversion. Neuron. 2011; 70(3):560-72. doi: 10. 1016/j. neuron. 2011. 02. 056 PMID: 21555080
10. Xiang T, Lohrenz T, Montague PR. Computational Substrates of Norms and Their Violations during Social Exchange. J Neurosci. 2013; 33(3):1099-108. doi: 10. 1523/JNEUROSCI. 1642-12. 2013 PMID: 23325247
11. Kring AM. Emotion disturbances as transdiagnostic processes in psychopathology. In: Lewis M, Haviland- Jones JM, Barrett LF, editors. Handbook of Emotion. 3rd ed. New York: Guilford Press; 2008.
12. Lindquist KA, Wager TD, Kober H, Bliss-Moreau E, Barrett LF. The brain basis of emotion: a meta-analytic review. Behav Brain Sci. 2012; 35(3):121-43. doi: 10. 1017/S0140525X11000446 PMID: 22617651
13. Wager TD, Feldman-Barrett L, Bliss-Moreau E, Lindquist K, Duncan S, Kober H, et al. The Neuroimaging of Emotion. In: Lewis M, Haviland-Jones JM, Feldman-Barrett L, editors. Handbook of emotions. New York: Guilford Press; 2008.
14. Etkin A, Wager TD. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am J Psychiatry. 2007; 164(10):1476-88. PMID: 17898336
15. Hamilton JP, Etkin A, Furman DJ, Lemus MG, Johnson RF, Gotlib IH. Functional neuroimaging of major depressive disorder: a meta-analysis and new integration of base line activation and neural response data. Am J Psychiatry. 2012; 169(7):693-703. doi: 10. 1176/appi. ajp. 2012. 11071105 PMID: 22535198
16. Drevets WC, Price JL, Furey ML. Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct Funct. 2008; 213(1-2):93-118. doi: 10. 1007/s00429-008-0193-1 PMID: 18651174
17. Kober H, Barrett LF, Joseph J, Bliss-Moreau E, Lindquist K, Wager TD. Functional grouping and cortical- subcortical interactions in emotion: a meta-analysis of neuroimaging studies. Neuroimage. 2008; 42(2):998-1031. doi: 10. 1016/j. neuroimage. 2008. 03. 059 PMID: 18579414
18. Barrett LF. Are Emotions Natural Kinds? Perspect Psychol Sci. 2006; 1(1):28-58.
19. Fu CH, Mourao-Miranda J, Costafreda SG, Khanna A, Marquand AF, Williams SC, et al. Pattern classification of sad facial processing: toward the development of neurobiological markers in depression. Biol Psychiatry. 2008; 63(7):656-62. PMID: 17949689
20. Wager TD, Gianaros PJ. The social brain, stress, and psychopathology. JAMA psychiatry. 2014; 71 (6):622-4. doi: 10. 1001/jamapsychiatry. 2014. 288 PMID: 24740473
21. Siegle GJ, Carter CS, Thase ME. Use of FMRI to predict recovery from unipolar depression with cognitive behavior therapy. Am J Psychiatry. 2006; 163(4):735-8. PMID: 16585452
22. Baliki MN, Petre B, Torbey S, Herrmann KM, Huang LJ, Schnitzer TJ, et al. Corticostriatal functional connectivity predicts transition to chronic back pain. Nature Neuroscience. 2012; 15(8):1117. doi: 10. 1038/nn. 3153 PMID: 22751038
23. Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, Hamani C, et al. Deep brain stimulation for treatment-resistant depression. Neuron. 2005; 45(5):651-60. PMID: 15748841
24. Schlaepfer TE, Cohen MX, Frick C, Kosel M, Brodesser D, Axmacher N, et al. Deep Brain Stimulation to Reward Circuitry Alleviates Anhedonia in Refractory Major Depression. Neuropsychopharmacology. 2007.
25. Kapur S, Phillips AG, Insel TR. Why has it taken so long for biological psychiatry to develop clinical tests and what to do about it? Mol Psychiatry. 2012; 17(12):1174-9. doi: 10. 1038/mp. 2012. 105 PMID: 22869033
26. Wager TD, Waugh CE, Lindquist M, Noll DC, Fredrickson BL, Taylor SF. Brain mediators of cardiovascular responses to social threat: part I: Reciprocal dorsal and ventral sub-regions of the medial prefrontal cortex and heart-rate reactivity. Neuroimage. 2009; 47(3):821-35. doi: 10. 1016/j. neuroimage. 2009. 05. 043 PMID: 19465137
27. Critchley HD. Neural mechanisms of autonomic, affective, and cognitive integration. The Journal of comparative neurology. 2005; 493(1):154-66. PMID: 16254997
28. Yarkoni T, Poldrack RA, Nichols TE, Van Essen DC, Wager TD. Large-scale automated synthesis of human functional neuroimaging data. Nat Methods. 2011; 8(8):665-70. doi: 10. 1038/nmeth. 1635 PMID: 21706013
29. Hariri AR, Mattay VS, Tessitore A, Kolachana B, Fera F, Goldman D, et al. Serotonin transporter genetic variation and the response of the human amygdala. Science. 2002; 297(5580):400-3. PMID: 12130784
30. Whalen PJ, Kagan J, Cook RG, Davis FC, Kim H, Polis S, et al. Human amygdala responsivity to masked fearful eye whites. Science. 2004; 306(5704):2061. PMID: 15604401
31. Wager TD, van Ast VA, Hughes BL, Davidson ML, Lindquist MA, Ochsner KN. Brain mediators of cardiovascular responses to social threat, part II: Prefrontal-subcortical pathways and relationship with anxiety. Neuroimage. 2009; 47(3):836-51. doi: 10. 1016/j. neuroimage. 2009. 05. 044 PMID: 19465135.
32. Uddin LQ, Kinnison J, Pessoa L, Anderson ML. Beyond the tripartite cognition-emotion-interoception model of the human insular cortex. J Cogn Neurosci. 2014; 26(1):16-27. doi: 10. 1162/jocn_a_00462 PMID: 23937691
33. Pessoa L. On the relationship between emotion and cognition. Nat Rev Neurosci. 2008; 9(2):148-58. doi: 10. 1038/nrn2317 PMID: 18209732
34. Phan KL, Taylor SF, Welsh RC, Ho SH, Britton JC, Liberzon I. Neural correlates of individual ratings of emotional salience: a trial-related fMRI study. Neuroimage. 2004; 21(2):768-80. PMID: 14980580
35. Wager TD, Atlas LY, Lindquist MA, Roy M, Woo CW, Kross E. An fMRI-based neurologic signature of physical pain. The New England journal of medicine. 2013; 368(15):1388-97. doi: 10. 1056/ NEJMoa1204471 PMID: 23574118
36. Haxby JV, Gobbini MI, Furey ML, Ishai A, Schouten JL, Pietrini P. Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science. 2001; 293(5539):2425-30. PMID: 11577229
37. Kamitani Y, Tong F. Decoding the visual and subjective contents of the human brain. Nat Neurosci. 2005; 8(5):679-85. PMID: 15852014
38. Mitchell TM, Hutchinson R, Niculescu RS, Pereira F, Wang XR, Just M, et al. Learning to decode cognitive states from brain images. Mach Learn. 2004; 57(1-2):145-75.
39. Kay KN, Naselaris T, Prenger RJ, Gallant JL. Identifying natural images from human brain activity. Nature. 2008; 452(7185):352-7. doi: 10. 1038/nature06713 PMID: 18322462
40. LeDoux J. Rethinking the emotional brain. Neuron. 2012; 73(4):653-76. doi: 10. 1016/j. neuron. 2012. 02. 004 PMID: 22365542
41. Vul E, Harris C, Winkielman P, Pashler H. Puzzlingly High Correlations in fMRI Studies of Emotion, Personality, and Social Cognition. Perspect Psychol Sci. 2009; 4(3):274-90.
42. Poldrack RA. Can cognitive processes be inferred from neuroimaging data? Trends in cognitive sciences. 2006; 10(2):59-63. PMID: 16406760
43. Yarkoni T, Barch DM, Gray JR, Conturo TE, Braver TS. BOLD correlates of trial-by-trial reaction time variability in gray and white matter: a multi-study fMRI analysis. PLoS ONE. 2009; 4(1):e4257. doi: 10. 1371/journal. pone. 0004257 PMID: 19165335
44. Peelen MV, Atkinson AP, Vuilleumier P. Supramodal representations of perceived emotions in the human brain. J Neurosci. 2010; 30(30):10127-34. doi: 10. 1523/JNEUROSCI. 2161-10. 2010 PMID: 20668196
45. Baucom LB, Wedell DH, Wang J, Blitzer DN, Shinkareva SV. Decoding the neural representation of affective states. Neuroimage. 2012; 59(1):718-27. doi: 10. 1016/j. neuroimage. 2011. 07. 037 PMID: 21801839
46. Kassam KS, Markey AR, Cherkassky VL, Loewenstein G, Just MA. Identifying Emotions on the Basis of Neural Activation. PLoS ONE. 2013; 8(6):e66032. PMID: 23840392
47. Kragel PA, Labar KS. Multivariate pattern classification reveals autonomic and experiential representations of discrete emotions. Emotion. 2013; 13(4):681-90. doi: 10. 1037/a0031820 PMID: 23527508
48. Craddock RC, Holtzheimer PE 3rd, Hu XP, Mayberg HS. Disease state prediction from resting state functional connectivity. Magn Reson Med. 2009; 62(6):1619-28. doi: 10. 1002/mrm. 22159 PMID: 19859933
49. Doehrmann O, Ghosh SS, Polli FE, Reynolds GO, Horn F, Keshavan A, et al. Predicting treatment response in social anxiety disorder from functional magnetic resonance imaging. JAMA psychiatry. 2013; 70(1):87-97. doi: 10. 1001/2013. jamapsychiatry. 5 PMID: 22945462
50. Lang PJ, Bradley MM, Cuthbert BN. International Affective Picture System (IAPS): Affective ratings of pictures and instruction manual. Gainesville, FL: University of Florida, 2005. doi: 10. 1016/j. psychres. 2015. 04. 002 PMID: 25890694
51. Lench HC, Flores SA, Bench SW. Discrete Emotions Predict Changes in Cognition, Judgment, Experience, Behavior, and Physiology: A Meta-Analysis of Experimental Emotion Elicitations. Psychological Bulletin. 2011; 137(5):834-55. doi: 10. 1037/a0024244 PMID: 21766999
52. Barch DM, Burgess GC, Harms MP, Petersen SE, Schlaggar BL, Corbetta M, et al. Function in the human connectome: task-fMRI and individual differences in behavior. Neuroimage. 2013; 80:169-89. doi: 10. 1016/j. neuroimage. 2013. 05. 033 PMID: 23684877
53. Wager TD, Atlas LY, Leotti LA, Rilling JK. Predicting individual differences in placebo analgesia: contributions of brain activity during anticipation and pain experience. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2011; 31(2):439-52. doi: 10. 1523/JNEUROSCI. 3420-10. 2011 PMID: 21228154
54. Rao RB, Fung G, Rosales R, editors. On the Dangers of Cross-Validation. An Experimental Evaluation. SDM; 2008: SIAM.
55. Libkuman TM, Otam H, Kern R, Viger SG, Novak N. Multidimensional normative ratings for the international affective picture system. Behav Res Methods. 2007; 39(2):326-34. PMID: 17695361
56. Krishnan A, Chang LJ, Woo CW, Ruzic L, Gu X, Fan J, et al. Somatic and vicarious pain are represented by dissociable multivariate brain patterns. Under Review.
57. Yeo BT, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M, et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. Journal of neurophysiology. 2011; 106(3):1125-65. doi: 10. 1152/jn. 00338. 2011 PMID: 21653723
58. Friston KJ. Functional and effective connectivity: a review. Brain connectivity. 2011; 1(1):13-36. doi: 10. 1089/brain. 2011. 0008 PMID: 22432952
59. Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, et al. Correspondence of the brain's functional architecture during activation and rest. Proc Natl Acad Sci U S A. 2009; 106(31):13040-5. doi: 10. 1073/pnas. 0905267106 PMID: 19620724
60. Allen EA, Erhardt EB, Damaraju E, GrunerW, Segall JM, Silva RF, et al. A baseline for the multivariate comparison of resting-state networks. Front Syst Neurosci. 2011; 5:2. doi: 10. 3389/fnsys. 2011. 00002 PMID: 21442040
61. Bullmore E, Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci. 2009; 10(3):186-98. doi: 10. 1038/nrn2575 PMID: 19190637
62. Craddock RC, Jbabdi S, Yan CG, Vogelstein JT, Castellanos FX, Di Martino A, et al. Imaging human connectomes at the macroscale. Nat Methods. 2013; 10(6):524-39. doi: 10. 1038/nmeth. 2482 PMID: 23722212
63. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, et al. Dissociable intrinsic connectivity networks for salience processing and executive control. Journal of Neuroscience. 2007; 27 (9):2349-56. PMID: 17329432
64. Denny BT, Kober H, Wager TD, Ochsner KN. A meta-analysis of functional neuroimaging studies of self- and other judgments reveals a spatial gradient for mentalizing in medial prefrontal cortex. J Cogn Neurosci. 2012; 24(8):1742-52. doi: 10. 1162/jocn_a_00233 PMID: 22452556
65. Van Snellenberg JX, Wager TD. Cognitive and motivational functions of the human prefrontal cortex. Luria's legacy in the 21st century. 2009:30-62.
66. Stoodley CJ, Schmahmann JD. Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex. 2010; 46(7):831-44. doi: 10. 1016/j. cortex. 2009. 11. 008 PMID: 20152963
67. Woo CW, Koban L, Kross E, Lindquist MA, Banich MT, Ruzic L, et al. Separate Neural Representations for Physical Pain and Social Rejection. Nat Commun. 2014; 5: 5380
68. Scherer KR. Appraisal theories. In Dalgleish T., & Power M. (Eds.). Handbook of cognition and emotion. Chichester: Wiley. 1999; p. 637-63.
69. Brosch T, Sander D. Comment: The Appraising Brain: Towards a Neuro-Cognitive Model of Appraisal Processes in Emotion. Emot Rev. 2013; 5(2):163-8.
70. Niedenthal PM. Embodying emotion. Science. 2007; 316(5827):1002-5. PMID: 17510358
71. MacLean P. Psychosomatic disease and the visceral brain; recent developments bearing on the Papez theory of emotion. Psychosomatic medicine. 1949; 11(6):338-53. PMID: 15410445
72. Ledoux J. The Emotional Brain. New York: Simon & Schuster; 1996.
73. Rainville P, Duncan GH, Price DD, Carrier B, Bushnell MC. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science. 1997; 277(5328):968-71. PMID: 9252330
74. Calder AJ, Keane J, Manes F, Antoun N, Young AW. Impaired recognition and experience of disgust following brain injury. Nat Neurosci. 2000; 3(11):1077-8. PMID: 11036262
75. Craig AD. How do you feel-now? The anterior insula and human awareness. Nature Reviews Neuroscience. 2009; 10(1):59-70. doi: 10. 1038/nrn2555 PMID: 19096369
76. Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, et al. Correspondence of the brain's functional architecture during activation and rest. Proceedings of the National Academy of Sciences of the United States of America. 2009; 106(31):13040-5. doi: 10. 1073/pnas. 0905267106 PMID: 19620724
77. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL. A default mode of brain function. Proc Natl Acad Sci U S A. 2001; 98(2):676-82. PMID: 11209064
78. Barrett LF. The Future of Psychology: Connecting Mind to Brain. Perspect Psychol Sci. 2009; 4 (4):326-39. PMID: 19844601
79. Gianaros PJ, Marsland AL, Kuan DC, Schirda BL, Jennings JR, Sheu LK, et al. An inflammatory pathway links atherosclerotic cardiovascular disease risk to neural activity evoked by the cognitive regulation of emotion. Biol Psychiatry. 2014; 75(9):738-45. doi: 10. 1016/j. biopsych. 2013. 10. 012 PMID: 24267410
80. Op de Beeck HP. Against hyperacuity in brain reading: spatial smoothing does not hurt multivariate fMRI analyses? Neuroimage. 2010; 49(3):1943-8. doi: 10. 1016/j. neuroimage. 2009. 02. 047 PMID: 19285144
81. Bartoshuk LM. Comparing sensory experiences across individuals: recent psychophysical advances illuminate genetic variation in taste perception. Chem Senses. 2000; 25(4):447-60. PMID: 10944509
82. Green BG, Dalton P, Cowart B, Shaffer G, Rankin K, Higgins J. Evaluating the 'Labeled Magnitude Scale' for measuring sensations of taste and smell. Chem Senses. 1996; 21(3):323-34. PMID: 8670711
83. Atlas LY, Bolger N, Lindquist MA, Wager TD. Brain mediators of predictive cue effects on perceived pain. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2010; 30 (39):12964-77. doi: 10. 1523/JNEUROSCI. 0057-10. 2010 PMID: 20881115
84. Pereira F, Mitchell T, Botvinick M. Machine learning classifiers and fMRI: a tutorial overview. Neuroimage. 2009; 45(1 Suppl):S199-209. doi: 10. 1016/j. neuroimage. 2008. 11. 007 PMID: 19070668
85. Hastie T, Tibshirani R, Friedman J. The elements of statistical learning: Data mining, inference, and prediction. 2nd ed. New York: Springer; 2009. doi: 10. 1016/j. neunet. 2009. 04. 005 PMID: 19443179
86. Kohavi R, editor A study of cross-validation and bootstrap for accuracy estimation and model selection. International Joint Conference on Aartificial Intelligence; 1995; Montreal, Quebec.
87. Efron B, Tibshirani R. An introduction to the bootstrap. New York: Springer; 1993.
88. Campbell DT, Fiske DW. Convergent and Discriminant Validation by the Multitrait-Multimethod Matrix. Psychological Bulletin. 1959; 56(2):81-105. PMID: 13634291
89. Haxby JV, Guntupalli JS, Connolly AC, Halchenko YO, Conroy BR, Gobbini MI, et al. A common, highdimensional model of the representational space in human ventral temporal cortex. Neuron. 2011; 72 (2):404-16. doi: 10. 1016/j. neuron. 2011. 08. 026 PMID: 22017997
90. Brodersen KH, Ong CS, Stephan KE, Buhmann JM, editors. The balanced accuracy and its posterior distribution. International Conference on Pattern Recognition; 2010; Istanbul, Turkey.
91. Macmillan NA, Creelman CD. Detection theory: A user's guide: Psychology Press; 2005.
92. Agresti A. Categorical Data Analysis. Hoboken, NJ: John Wiley & Sons, Inc.; 2012.
93. Shepard RN. Multidimensional scaling, tree-fitting, and clustering. Science. 1980; 210(4468):390-8. PMID: 17837406
94. Rissman J, Gazzaley A, D'Esposito M. Measuring functional connectivity during distinct stages of a cognitive task. Neuroimage. 2004; 23(2):752-63. PMID: 15488425