Using executive control training to suppress amygdala reactivity to aversive information

NeuroImage

Volumn 125, Issue , 2016, Pages 1022-1031

  Cohen, N ^a   Margulies, D S ^b   Ashkenazi, S ^c   Schaefer, A ^b,e   Taubert, M ^b   Henik, A ^a   Villringer, A ^b   Okon Singer, H ^d  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b MAX PLANCK INSTITUTE FOR HUMAN COGNITIVE AND BRAIN SCIENCES   (Germany)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^d UNIVERSITY OF HAIFA   (Israel)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Amygdala; Connectivity; Emotional interference; Executive control; FMRI; Inferior frontal gyrus; Training

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; AVERSION; BRAIN FUNCTION; CONNECTOME; CONTROLLED STUDY; EMOTION; EXECUTIVE FUNCTION; FEMALE; HUMAN; HUMAN EXPERIMENT; INFERIOR FRONTAL GYRUS; MALE; NEUROMODULATION; NORMAL HUMAN; PRIORITY JOURNAL; RESTING STATE NETWORK; TASK PERFORMANCE; AMYGDALA; BEHAVIOR THERAPY; IMAGE PROCESSING; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PREFRONTAL CORTEX; PROCEDURES;

ADULT; AMYGDALA; BEHAVIOR THERAPY; EMOTIONS; EXECUTIVE FUNCTION; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; PREFRONTAL CORTEX;

EID: 84947998331     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.10.069     Document Type: Article

References (91)

1. Aiken L.S., West S.G. Multiple Regression: Testing and Interpreting Interactions (Vol. xi) 1991, Sage Publications, Inc., Thousand Oaks, CA, US.
2. Amaral D.G., Insausti R. Retrograde transport of D-[3H]-aspartate injected into the monkey amygdaloid complex. Exp. Brain Res. 1992, 88:375-388.
3. Aron A.R., Robbins T.W., Poldrack R.A. Inhibition and the right inferior frontal cortex. Trends Cogn. Sci. 2004, 8:170-177.
4. Ashburner J., Friston K.J. Unified segmentation. NeuroImage 2005, 26:839-851.
5. Banich M.T. Executive function the search for an integrated account. Curr. Dir. Psychol. Sci. 2009, 18:89-94.
6. Beck A.T., Steer R.A., Brown G.K. Beck depression inventory manual 1996.
7. Berkman E.T., Burklund L., Lieberman M.D. Inhibitory spillover: intentional motor inhibition produces incidental limbic inhibition via right inferior frontal cortex. NeuroImage 2009, 47:705-712.
8. Bishop S., Duncan J., Brett M., Lawrence A.D. Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli. Nat. Neurosci. 2004, 7:184-188.
9. Biswal B.B., Mennes M., Zuo X.N., Gohel S., Kelly C., Smith SM . . . Milham MP Toward discovery science of human brain function. Proc. Natl. Acad. Sci. 2010, 107:4734-4739.
10. Blair K.S., Smith B.W., Mitchell D.G.V., Morton J., Vythilingam M., Pessoa L . . . Blair RJR Modulation of emotion by cognition and cognition by emotion. NeuroImage 2007, 35:430-440.
11. Braver T.S., Barch D.M., Gray J.R., Molfese D.L., Snyder A. Anterior cingulate cortex and response conflict: effects of frequency, inhibition and errors. Cereb. Cortex 2001, 11:825-836.
12. Buckner R.L., Krienen F.M., Yeo B.T.T. Opportunities and limitations of intrinsic functional connectivity MRI. Nat. Neurosci. 2013, 16:832-837.
13. Buodo G., Sarlo M., Palomba D. Attentional resources measured by reaction times highlight differences within pleasant and unpleasant, high arousing stimuli. Motiv. Emot. 2002, 26:123-138.
14. Calkins A.W., McMorran K.E., Siegle G.J., Otto M.W. The effects of computerized cognitive control training on community adults with depressed mood. Behav. Cogn. Psychother. 2014, 1-12.
15. Carter C.S., Macdonald A.M., Botvinick M., Ross L.L., Stenger V.A., Noll D., Cohen J.D. Parsing executive processes: strategic vs. evaluative functions of the anterior cingulate cortex. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:1944-1948.
16. Cohen N., Henik A. Do irrelevant emotional stimuli impair or improve executive control?. Front Int. Neurosci. 2012, 6.
17. Cohen N., Henik A., Mor N. Can emotion modulate attention? Evidence for reciprocal links in the Attentional Network Test. Exp. Psychol. 2011, 58:171-179.
18. Cohen N., Henik A., Moyal N. Executive control attenuates emotional effects-for high reappraisers only?. Emotion 2012, 12:970-979.
19. Cohen N., Mor N., Henik A. Linking executive control and emotional response: a training procedure to reduce rumination. Clin. Psychol. Sci. 2015, 3:15-25.
20. Cohen N., Moyal N., Lichtenstein-Vidne L., Henik A. Explicit vs. implicit emotional processing: the interaction between processing type and executive control. Cogn. Emot. 2015, 1-15. (ahead-of-print).
21. Cohen N., Moyal N., Henik A. Executive control suppresses pupillary responses to aversive stimuli. Biological psychology 2015, 112:1-11.
22. Cox R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 1996, 29:162-173.
23. Daches S., Mor N. Training ruminators to inhibit negative information: a preliminary report. Cogn. Ther. Res. 2014, 38:160-171.
24. Davelaar E.J., Stevens J. Sequential dependencies in the Eriksen flanker task: a direct comparison of two competing accounts. Psychon. Bull. Rev. 2009, 16:121-126.
25. Dijk K.R.A.V., Hedden T., Venkataraman A., Evans K.C., Lazar S.W., Buckner R.L. Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. J. Neurophysiol. 2010, 103:297-321.
26. Dolcos F., Kragel P., Wang L., McCarthy G. Role of the inferior frontal cortex in coping with distracting emotions. NeuroReport 2006, 17:1591-1594.
27. Erickson K.I., Colcombe S.J., Wadhwa R., Bherer L., Peterson M.S., Scalf P.E., Kramer A.F. Training-induced functional activation changes in dual-task processing: an fMRI study. Cereb. Cortex 2007, 17:192-204.
28. Etkin A., Klemenhagen K.C., Dudman J.T., Rogan M.T., Hen R., Kandel E.R., Hirsch J. Individual differences in trait anxiety predict the response of the basolateral amygdala to unconsciously processed fearful faces. Neuron 2004, 44:1043-1055.
29. Eysenck M.W., Derakshan N., Santos R., Calvo M.G. Anxiety and cognitive performance: attentional control theory. Emotion 2007, 7:336-353.
30. Fan J., McCandliss B.D., Sommer T., Raz A., Posner M.I. Testing the efficiency and independence of attentional networks. J. Cogn. Neurosci. 2002, 14:340-347.
31. Fan J., McCandliss B.D., Fossella J., Flombaum J.I., Posner M.I. The activation of attentional networks. NeuroImage 2005, 26:471-479.
32. Fanselow M., Ledoux J. Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neuron 1999, 23:229-232.
33. Fossati P., Ergis A.M., Allilaire J.F. Executive functioning in unipolar depression: a review. L'Encéphale 2002, 28:97-107.
34. Friedman L., Stern H., Brown G.G., Mathalon D.H., Turner J., Glover G.H., Potkin S.G. Test-retest and between-site reliability in a multicenter fMRI study. Hum. Brain Mapp. 2008, 29:958-972.
35. Friston K.J., Holmes A., Poline J.B., Price C.J., Frith C.D. Detecting activations in PET and fMRI: levels of inference and power. NeuroImage 1996, 4:223-235.
36. Goldin P.R., McRae K., Ramel W., Gross J.J. The neural bases of emotion regulation: reappraisal and suppression of negative emotion. Biol. Psychiatry 2008, 63:577-586.
37. Gratton G.H.G., Donchin E. Optimizing the use of information: strategic control of activation of responses. J. Exp. Psychol. Gen. 1992, 121:480-506.
38. Gratton G.H.G., Sirevaag E.J., Eriksen C.W., Donchin E. Pre- and poststimulus activation of response channels: a psychophysiological analysis. J. Exp. Psychol. Hum. Percept. Perform. 1988, 14:331-344.
39. Gross J.J., John O.P. Individual differences in two emotion regulation processes: Implications for affect, relationships, and well-being. J. Pers. Soc. Psychol. 2003, 85:348-362.
40. Hampshire A., Chamberlain S.R., Monti M.M., Duncan J., Owen A.M. The role of the right inferior frontal gyrus: inhibition and attentional control. NeuroImage 2010, 50:1313-1319.
41. Hariri A.R., Tessitore A., Mattay V.S., Fera F., Weinberger D.R. The amygdala response to emotional stimuli: a comparison of faces and scenes. NeuroImage 2002, 17:317-323.
42. Hartikainen K.M., Ogawa K.H., Knight R.T. Transient interference of right hemispheric function due to automatic emotional processing. Neuropsychologia 2000, 38:1576-1580.
43. Iacoviello B.M., Wu G., Alvarez E., Huryk K., Collins K.A., Murrough J.W., Charney D.S. Cognitive-emotional training as an intervenstion for major depressive disorder. Depression and anxiety 2014, 31:699-706.
44. Iacoviello B.M., Wu G., Alvarez E., Huryk K., Collins K.A., Murrough J.W., Charney D.S. Cognitive-emotional training as an intervention for major depressive disorder. Depress. Anxiety 2014.
45. Iordan A.D., Dolcos S., Dolcos F. Neural signatures of the response to emotional distraction: a review of evidence from brain imaging investigations. Front. Hum. Neurosci. 2013, 7.
46. Jaeggi S.M., Buschkuehl M. Working memory training and transfer: theoretical and practical considerations. Cogn. Affect. Behav. Neurosci. 2014, 14:147-160.
47. Jenkinson M., Beckmann C.F., Behrens T.E.J., Woolrich M.W., Smith S.M. FSL. NeuroImage 2012, 62:782-790.
48. Lancaster J.L., Woldorff M.G., Parsons L.M., Liotti M., Freitas C.S., Rainey L., Fox P.T. Automated Talairach atlas labels for functional brain mapping. Hum. Brain Mapp. 2000, 10:120-131.
49. Lang P., Bradley M.M. The International Affective Picture System (IAPS) in the study of emotion and attention. Handbook of Emotion Elicitation and Assessment 2007, 29.
50. Lang P., Bradley M., Cuthbert B. International Affective Picture System (IAPS): Affective Ratings of Pictures and Instruction Manual 2008.
51. Liberzon I., Martis B. Neuroimaging studies of emotional responses in PTSD. Ann. N. Y. Acad. Sci. 2006, 1071:87-109.
52. MacDonald A.W., Cohen J.D., Stenger V.A., Carter C.S. Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 2000, 288:1835-1838.
53. MacLeod J.W., Lawrence M.A., McConnell M.M., Eskes G.A., Klein R.M., Shore D.I. Appraising the ANT: psychometric and theoretical considerations of the Attention Network Test. Neuropsychology 2010, 24:637-651.
54. Maldjian J.A., Laurienti P.J., Kraft R.A., Burdette J.H. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 2003, 19:1233-1239.
55. Margulies D.S., Böttger J., Long X., Lv Y., Kelly C., Schäfer A., Villringer A. Resting developments: a review of fMRI post-processing methodologies for spontaneous brain activity. MAGMA 2010, 23:289-307.
56. Mazziotta J.C., Toga A.W., Evans A., Fox P., Lancaster J. A probabilistic atlas of the human brain: theory and rationale for its development: the international consortium for brain mapping (ICBM). NeuroImage 1995, 2:89-101.
57. Mennes M., Kelly C., Zuo X.N., Di Martino A., Biswal B.B., Castellanos F.X., Milham M.P. Inter-individual differences in resting-state functional connectivity predict task-induced BOLD activity. NeuroImage 2010, 50:1690-1701.
58. Miller E.K., Cohen J.D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 2001, 24:67-202.
59. Nolen-Hoeksema S., Stice E., Wade E., Bohon C. Reciprocal relations between rumination and bulimic, substance abuse, and depressive symptoms in female adolescents. J. Abnorm. Psychol. 2007, 116:198-207.
60. Norman D.A., Shallice T. Attention to Action: Willed and Automatic Control of Behavior 1980.
61. Ochsner K.N., Gross J.J. Cognitive emotion regulation insights from social cognitive and affective neuroscience. Curr. Dir. Psychol. Sci. 2008, 17:153-158.
62. Ochsner K.N., Bunge S.A., Gross J.J., Gabrieli J.D.E. Rethinking feelings: an fMRI study of the cognitive regulation of emotion. J. Cogn. Neurosci. 2002, 14:1215-1229.
63. Öhman A., Flykt A., Esteves F. Emotion drives attention: detecting the snake in the grass. J. Exp. Psychol. Gen. 2001, 130:466-478.
64. Okon-Singer H., Tzelgov J., Henik A. Distinguishing between automaticity and attention in the processing of emotionally significant stimuli. Emotion 2007, 7:147-157.
65. Okon-Singer H., Lichtenstein-Vidne L., Cohen N. Dynamic modulation of emotional processing. Biol. Psychol. 2013, 92:480-491.
66. Okon-Singer H., Mehnert J., Hoyer J., Hellrung L., Schaare H.L., Dukart J., Villringer A. Neural control of vascular reactions: impact of emotion and attention. The Journal of Neuroscience 2014, 34(12):4251-4259.
67. Okon-Singer H., Hendler T., Pessoa L., Shackman A.J. The neurobiology of emotion-cognition interactions: fundamental questions and strategies for future research. Front. Hum. Neurosci. 2015, 9:58.
68. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
69. Owen A.M., Hampshire A., Grahn J.A., Stenton R., Dajani S., Burns A.S., Ballard C.G. Putting brain training to the test. Nature 2010, 465:775-778.
70. Owens M., Koster E.H., Derakshan N. Improving attention control in dysphoria through cognitive training: transfer effects on working memory capacity and filtering efficiency. Psychophysiology 2013, 50:297-307.
71. Paternoster R., Brame R., Mazerolle P., Piquero A. Using the correct statistical test for the equality of regression coefficients. Criminology 1998, 36:859-866.
72. Quirk G.J., Beer J.S. Prefrontal involvement in the regulation of emotion: convergence of rat and human studies. Curr. Opin. Neurobiol. 2006, 16:723-727.
73. Robinson S., Windischberger C., Rauscher A., Moser E. Optimized 3T EPI of the amygdalae. NeuroImage 2004, 22:203-210.
74. Robinson J.L., Laird A.R., Glahn D.C., Lovallo W.R., Fox P.T. Metaanalytic connectivity modeling: delineating the functional connectivity of the human amygdala. Hum. Brain Mapp. 2010, 31:173-184.
75. Rohr C.S., Okon-Singer H., Craddock R.C., Villringer A., Margulies D.S. Affect and the brain's functional organization: a resting-state connectivity approach. PLoS One 2013, 8(7).
76. Rohr C.S., Dreyer F.R., Aderka I.M., Margulies D.S., Frisch S., Villringer A., Okon-Singer H. Individual differences in common factors of emotional traits and executive functions predict functional connectivity of the amygdala. NeuroImage 2015, 120:154-163.
77. Rosazza C., Minati L. Resting-state brain networks: literature review and clinical applications. Neurol. Sci. 2011, 32:773-785.
78. Roy A.K., Shehzad Z., Margulies D.S., Kelly A.M.C., Uddin L.Q., Gotimer K., Milham M.P. Functional connectivity of the human amygdala using resting state fMRI. NeuroImage 2009, 45:614-626.
79. Sabatinelli D., Fortune E.E., Li Q., Siddiqui A., Krafft C., Oliver W.T., Jeffries J. Emotional perception: meta-analyses of face and natural scene processing. NeuroImage 2011, 54:2524-2533.
80. Sari B.A., Koster E.H., Pourtois G., Derakshan N. Training working memory to improve attentional control in anxiety: A proof-of-principle study using behavioral and electrophysiological measures. Biological Psychology 2015.
81. Schweizer S., Hampshire A., Dalgleish T. Extending brain-training to the affective domain: increasing cognitive and affective executive control through emotional working memory training. PLoS One 2011, 6.
82. Schweizer S., Grahn J., Hampshire A., Mobbs D., Dalgleish T. Training the emotional brain: improving affective control through emotional working memory training. J. Neurosci. 2013, 33:5301-5311.
83. Shehzad Z., Kelly A.C., Reiss P.T., Gee D.G., Gotimer K., Uddin L.Q., Milham M.P. The resting brain: unconstrained yet reliable. Cereb. Cortex 2009, 19:2209-2229.
84. Siegle G.J., Thompson W., Carter C.S., Steinhauer S.R., Thase M.E. Increased amygdala and decreased dorsolateral prefrontal BOLD responses in unipolar depression: related and independent features. Biol. Psychiatry 2007, 61:198-209.
85. Smith S.M., Fox P.T., Miller K.L., Glahn D.C., Fox P.M., Mackay C.E., Beckmann C.F. Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. 2009, 106:13040-13045.
86. Spielberger C.D., Gorsuch R.L., Lushene R.E. Manual for the State-Trait Anxiety Inventory 1970.
87. Tzelgov J., Henik A., Berger J. Controlling Stroop effects by manipulating expectations for color words. Mem. Cogn. 1992, 20:727-735.
88. Van den Heuvel M.P., Hulshoff Pol H.E. Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur. Neuropsychopharmacol. 2010, 20:519-534.
89. Van Dillen L.F., Heslenfeld D.J., Koole S.L. Tuning down the emotional brain: an fMRI study of the effects of cognitive load on the processing of affective images. NeuroImage 2009, 45:1212-1219.
90. Verbruggen F., Logan G.D. Response inhibition in the stop-signal paradigm. Trends Cogn. Sci. 2008, 12:418-424.
91. Woo C.W., Krishnan A., Wager T.D. Cluster-extent based thresholding in fMRI analyses: pitfalls and recommendations. NeuroImage 2014, 91:412-419.