Using real-time fMRI to influence effective connectivity in the developing emotion regulation network

NeuroImage

Volumn 125, Issue , 2016, Pages 616-626

  Cohen Kadosh, Kathrin ^a,b   Luo, Qiang ^c,d   de Burca, Calem ^a   Sokunbi, Moses O ^e,f,g   Feng, Jianfeng ^c,d,h   Linden, David E J ^e,f   Lau, Jennifer Y F ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c FUDAN UNIVERSITY   (China)

^d FUDAN UNIVERSITY   (China)

^e CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

^f CARDIFF UNIVERSITY   (United Kingdom)

^g SISSA   (Italy)

^h UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ARTICLE; BRAIN FUNCTION; CHILD; CINGULATE GYRUS; CONNECTOME; DOWN REGULATION; EMOTION REGULATION NETWORK; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INFERIOR PARIETAL LOBULE; INSULA; LONGEVITY; MALE; MENTAL CAPACITY; NERVOUS SYSTEM PARAMETERS; NEUROFEEDBACK; NORMAL HUMAN; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; SCHOOL CHILD; SOCIAL COGNITION; SUPPLEMENTARY MOTOR AREA; UPREGULATION; BRAIN CORTEX; CLINICAL TRIAL; EMOTION; IMAGE PROCESSING; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PROCEDURES;

ADOLESCENT; CEREBRAL CORTEX; CHILD; EMOTIONS; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; NEUROFEEDBACK;

EID: 84946887657     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.09.070     Document Type: Article

References (88)

1. Angold A., Costello E.J., Messer S.C., Pickles A., Winder F., Silver D. The development of a short questionnaire for use in epidemiological studies of depression in children and adolescents. Int. J. Methods Psychiatr. Res. 1995, 5:237-249.
2. Arns M., Heinrich H., Strehl U. Evaluation of neurofeedback in ADHD: the long and winding road. Biol. Psychol. 2014, 95:108-115. 10.1016/j.biopsycho.2013.11.013.
3. Ashburner J., Friston K.J. Rigid body transformation. Human Brain Function 2003, 635-654. Academic Press, Oxford. 2nd ed. R.S. Frakoviak, K.J. Friston, C. Frith, R.J. Dolan, C. Price, S. Zeki, J. Ashburner, W. Penny (Eds.).
4. Ashburner J., Friston K.J. Spatial normalization using basis functions. Human brain function 2003, 655-672. Academic Press, Oxford. 2nd ed. R.S. Frakoviak, K.J. Friston, C. Frith, R.J. Dolan, C. Price, S. Zeki, J. Ashburner, W. Penny (Eds.).
5. Bar-Haim Y. Research review: attention bias modification (ABM): a novel treatment for anxiety disorders. J. Child Psychol. Psychiatry 2010, 51(8):859-870. (JCPP2251 [pii]). 10.1111/j.1469-7610.2010.02251.x.
6. Baur V., Hanggi J., Langer N., Jancke L. Resting-state functional and structural connectivity within an insula-amygdala route specifically index state and trait anxiety. Biol. Psychiatry 2013, 73(1):85-92. 10.1016/j.biopsych.2012.06.003.
7. Bindemann M., Burton A.M., Hooge I.T., Jenkins R., de Haan E.H. Faces retain attention. Psychon. Bull. Rev. 2005, 12(6):1048-1053. (Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/16615327).
8. Blakemore S.-J. The social brain in adolescence. Nat. Rev. Neurosci. 2008, 9:267-277.
9. Blakemore S.J., Mills K.L. Is adolescence a sensitive period for sociocultural processing?. Annu. Rev. Psychol. 2014, 65:187-207. 10.1146/annurev-psych-010213-115202.
10. Burnett S., Sebastian C., Cohen Kadosh K., Blakemore S.-J. The social brain in adolescence: evidence from functional magnetic resonance imaging and behavioural studies. Neurosci. Biobehav. Rev. 2011, 35(8):1654-1564.
11. Caria A., Sitaram R., Veit R., Begliomini C., Birbaumer N. Volitional control of anterior insula activity modulates the response to aversive stimuli. A real-time functional magnetic resonance imaging study. Biol. Psychiatry 2010, 68:425-432.
12. Carlson J.M., Greenberg T., Rubin D., Mujica-Parodi L.R. Feeling anxious: anticipatory amygdalo-insular response predicts the feeling of anxious anticipation. Soc. Cogn. Affect. Neurosci. 2011, 6(1):74-81. 10.1093/Scan/Nsq017.
13. Cohen Kadosh K. Differing processing abilities for specific face properties in mid-childhood and adulthood. Front. Psychol. 2011, 2:400. 10.3389/fpsyg.2011.00400.
14. Cohen Kadosh K., Linden D.E.J., Lau J.Y. Plasticity during childhood and adolescence: innovative approaches to investigating neurocognitive development. Dev. Sci. 2013, 16(4):574-583.
15. Cohen Kadosh K., Heathcote L.C., Lau J.Y. Age-related changes in attentional control across adolescence: how does this impact emotion regulation capacities?. Front. Psychol. 2014.
16. Craig A.D. Interoception: the sense of the physiological condition of the body. Curr. Opin. Neurobiol. 2003, 13(4):500-505. (Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/12965300).
17. Crone E.A. The role of the medial frontal cortex in the development of cognitive and social-affective performance monitoring. Psychophysiology 2014, 51(10):943-950. 10.1111/psyp.12252.
18. Crone E.A., Dahl R.E. Understanding adolescence as a period of social-affective engagement and goal flexibility. Nat. Rev. Neurosci. 2012, 13(9):636-650. 10.1038/nrn3313.
19. deCharms R.C. Reading and controlling human brain activation using real-time functional magnetic resonance imaging. Trends Cogn. Sci. 2007, 11(11):473-481.
20. deCharms R.C., Maeda F., Glover G.H., Ludlow D., Pauly J.M., Soneji D., Mackey S.C. Control over brain activation and pain learned by using real-time functional MRI. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(51):18626-18631.
21. deCharms R.C., Christoff K., Glover G.H., Pauly J.M., Whitfield S., Gabrieli J.D. Learned regulation of spatially localized brain activation using real-time fMRI. NeuroImage 2004, 21(1):436-443. (Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/14741680).
22. Fair D.A., Dosenbach N.U.F., Church J.A., Cohen A.L., Brahmbhatt S., Miezin F.M., Schlaggar B.L. Development of distinct control networks through segregation and integration. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(33):13507-13512.
23. Fair D.A., Cohen A.L., Dosenbach N.U.F., Church J.A., Miezin F.M., Barch D.M., Schlaggar B.L. The maturing architecture of the brain's default network. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(10):4028-4032.
24. Fair D.A., Cohen A.L., Power J.D., Dosenbach N.U., Church J.A., Miezin F.M., Petersen S.E. Functional brain networks develop from a "local to distributed" organization. PLoS Comput. Biol. 2009, 5(5). 10.1371/journal.pcbi.1000381.
25. Friston K.J., Penny W., Philips C., Kiebel S., Hinton G., Ashburner J. Classical and Bayesian inference in neuroimaging: theory. NeuroImage 2002, 16(2):465-483.
26. Ganel T., Goshen-Gottstein Y. Perceptual integrality of sex and identity of faces: further evidence for the single route hypothesis. J. Exp. Psychol. Hum. Percept. Perform. 2002, 28:854-867.
27. Ganel T., Goshen-Gottstein Y. Effects of familiarity on the perceptual integrality of the identity and expression of faces: the parallel-route hypothesis revisited. J. Exp. Psychol. Hum. Percept. Perform. 2004, 30(3):583-597.
28. Garniefski N., Kraaij V., Spinhoven P. Negative life events, cognitive emotion regulation and emotional problems. Personal. Individ. Differ. 2001, 30:1311-1327.
29. Ge T., Feng J., Grabenhorst F., Rolls E. Componential Granger causality, and its application to identifying the source and mechanisms of the top-down biased activation that controls attention to affective vs sensory processing. NeuroImage 2012, 59(2):1846-1858. (Retrieved from citeulike-article-id:9715278). 10.1016/j.neuroimage.2011.08.047.
30. Gee D.G., Humphreys K.L., Flannery J., Goff B., Telzer E.H., Shapiro M., Tottenham N. A developmental shift from positive to negative connectivity in human amygdala-prefrontal circuitry. J. Neurosci. 2013, 33(10):4584-4593. 10.1523/JNEUROSCI.3446-12.2013.
31. Giedd J.N., Blumenthal J., Jeffries N.O., Castellanos F.X., Liu H., Zijdenbos A., Rapoport J.L. Brain development during childhood and adolescence: a longitudinal MRI study. Nat. Neurosci. 1999, 2(10):861-863.
32. Gogtay N., Giedd J.N., Lusk L., Hayashi K.M., Greenstein D., Vaituzis A.C., Thompson P.M. Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(21):8174-8179.
33. Guo S., Wu J., Ding M., Feng J. Uncovering Interactions in the Frequency Domain. PLoS Comput. Biol. 2008, 4(5). (Retrieved from citeulike-article-id:2869965). 10.1371/journal.pcbi.1000087.
34. Guyer A.E., Choate V.R., Pine D.S., Nelson E.E. Neural circuitry underlying affective response to peer feedback in adolescence. Soc. Cogn. Affect. Neurosci. 2012, 7(1):81-92. (nsr043 [pii]). 10.1093/scan/nsr043.
35. Haller S.P.W., Cohen Kadosh K., Lau J.Y.F. A developmental angle to understanding the mechanisms of biased cognition in social anxiety. Front. Hum. Neurosci. 2015, (in press).
36. Haller S.P.W., Cohen Kadosh K., Scerif G., Lau J.Y.F. Social anxiety disorder: a new developmental cognitive neuroscience approach to uncover risk factors during adolescence. Dev. Cogn. Neurosci. 2015, (in press).
37. Hamilton J.P., Chen G., Thomason M.E., Schwartz M.E., Gotlib I.H. Investigating neural primacy in Major Depressive Disorder: multivariate Granger causality analysis of resting-state fMRI time-series data. Mol. Psychiatry 2011, 16(7):763-772. 10.1038/mp.2010.46.
38. Hare T.A., Tottenham N., Galvan A., Voss H.U., Glover G.H., Casey B.J. Biological substrates of emotional reactivity and regulation in adolescence during an emotional go-nogo task. Biol. Psychiatry 2008, 63(10):927-934. 10.1016/j.biopsych.2008.03.015.
39. Harris J.J., Reynell C., Attwell D. The physiology of developmental changes in BOLD functional imaging signals. Dev. Cogn. Neurosci. 2011, 1(3):199-216.
40. Johnson M.H., Grossmann T., Cohen Kadosh K. Mapping functional brain development: building a social brain through Interactive Specialization. Dev. Psychol. 2009, 45:151-159.
41. Johnson M.H., Jones E.J., Gliga T. Brain adaptation and alternative developmental trajectories. Dev. Psychopathol. 2015, 27(2):425-442. 10.1017/S0954579415000073.
42. Johnston S., Boehm S., Healy D., Goebel R., Linden D. Neurofeedback: a promising tool for the self-regulation of emotion networks. NeuroImage 2010, 49:1066-1072.
43. Johnston S., Linden D.E.J., Healy D., Goebel R., Habes I., Boehm S.G. Upregulation of emotion areas through neurofeedback with a focus on positive mood. Cogn. Affect. Behav. Neurosci. 2011, 11:44-51.
44. Kang H.C., Burgund E.D., Lugar H.M., Petersen S.E., Schlaggar B.L. Comparison of functional activation foci in children and adults using a common stereotactic space. NeuroImage 2003, 19:16-28.
45. Keshavan M.S., Giedd J., Lau J.Y.F., Lewis D.A., Paus T. Changes in the adolescent brain and the pathophysiology of psychotic disorders. Lancet Psychiatry 2014, 1(7):549-558.
46. Kessler R.C., Berglund P., Demler O., Jin R., Merikangas K.R., Walters E.E. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch. Gen. Psychiatry 2005, 62(6):593-602. 10.1001/archpsyc.62.6.593.
47. Kohn N., Eickhoff S.B., Scheller M., Laird A.R., Fox P.T., Habel U. Neural network of cognitive emotion regulation-an ALE meta-analysis and MACM analysis. NeuroImage 2014, 87:345-355. 10.1016/j.neuroimage.2013.11.001.
48. Kriegeskorte N., Simmons W.K., Bellgowan P.S., Baker C.I. Circular analysis in systems neuroscience: the dangers of double dipping. Nat. Neurosci. 2009, 12(5):535-540. 10.1038/nn.2303.
49. Lebel C., Beaulieu C. Longitudinal development of human brain wiring continues from childhood to adulthood. J. Neurosci. 2011, 31(30):10937-10947.
50. Linden D.E., Habes I., Johnston S.J., Linden S., Tatineni R., Subramanian L., Goebel R. Real-time self-regulation of emotion networks in patients with depression. PLoS One 2012, 7(6). (PONE-D-11-22815 [pii]). 10.1371/journal.pone.0038115.
51. Luo Q., Ge T., Feng J. Granger causality with signal-dependent noise. NeuroImage 2011, 57(4):1422-1429. 10.1016/j.neuroimage.2011.05.054.
52. Luo Q., Ge T., Grabenhorst F., Feng J., Rolls E.T. Attention-dependent modulation of cortical taste circuits revealed by Granger Causality with signal-dependent noise. PLoS Comput. Biol. 2013, 9(10).
53. Luo Q., Lu W., Cheng W., Valdes-Sosa P.A., Wen X., Ding M., Feng J. Spatio-temporal Granger causality: a new framework. NeuroImage 2013, 79:241-263. (S1053-8119(13)00450-3 [pii]). 10.1016/j.neuroimage.2013.04.091.
54. MacLeod C., Holmes E.A. Cognitive bias modification for children with anxiety disorder: an intervention approach worth attending to. Am. J. Psychiatr. 2011, 169(2):118-120.
55. McRae K., Gross J.J., Weber J., Robertson E.R., Sokol-Hessner P., Ray R.D., Ochsner K.N. The development of emotion regulation: an fMRI study of cognitive reappraisal in children, adolescents and young adults. Soc. Cogn. Affect. Neurosci. 2012, 7(1):11-22. 10.1093/scan/nsr093.
56. Moor B.G., van Leijenhorst L., Rombouts S.A.R.B., Crone E.A., Van der Molen M.W. Do you like me? Neural correlates of social evaluation and developmental trajectories. Soc. Neurosci. 2010, 5(5-6):461-482. (Pii 927980134). 10.1080/17470910903526155.
57. Nelson E.E., Leibenluft E., McClure E.B., Pine D.S. The social re-orientation of adolescence: a neuroscience perspective on the process and its relation to psychopathology. Psychol. Med. 2005, 35(2):163-174. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/15841674.
58. Palaniyappan L., Simmonite M., White T.P., Liddle E.B., Liddle P.F. Neural primacy of the salience processing system in schizophrenia. Neuron 2013, 79(4):814-828. 10.1016/j.neuron.2013.06.027.
59. Paret C., Kluetsch R., Ruf M., Demirakca T., Hoesterey S., Ende G., Schmahl C. Down-regulation of amygdala activation with real-time fMRI neurofeedback in a healthy female sample. Front. Behav. Neurosci. 2014, 8. (Unsp 299). 10.3389/Fnbeh.2014.00299.
60. Park H.-J., Friston K. Structural and functional brain networks: from connections to cognition. Science 2013, 342(6158). 10.1126/science.1238411.
61. Paus T., Keshavan M., Giedd J.N. Why do many psychiatric disorders emerge during adolescence?. Nat. Rev. Neurosci. 2008, 9:947-957.
62. Perlman S.B., Pelphrey K.A. Developing connections for affective regulation: age-related changes in emotional brain connectivity. J. Exp. Child Psychol. 2011, 108(3):607-620. 10.1016/j.jecp.2010.08.006.
63. Petanjek Z., Judas M., Simic G., Rasin M.R., Uylings H.B.M., Rakic P. Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(32):13281-13286.
64. Pfeifer J.H., Allen N.B. Arrested development? Reconsidering dual-systems models of brain function in adolescence and disorders. Trends Cogn. Sci. 2012, (S1364-6613(12)00104-0 [pii]). 10.1016/j.tics.2012.04.011.
65. Phelps E.A., O'Connor K.J., Gatenby J.C., Gore J.C., Grillon C., Davis M. Activation of the left amygdala to a cognitive representation of fear. Nat. Neurosci. 2001, 4(4):437-441. 10.1038/86110.
66. Pitskel N.B., Bolling D.Z., Kaiser M.D., Crowley M.J., Pelphrey K.A. How grossed out are you? The neural bases of emotion regulation from childhood to adolescence. Dev. Cogn. Neurosci. 2011, 1(3):324-337. 10.1016/j.dcn.2011.03.004.
67. Platt B., Cohen Kadosh K., Lau J.Y. The Role of Peer Rejection in Adolescent Depression. Depress Anxiety 2013, 10.1002/da.22120.
68. Rota G., Handjaras G., Sitaram R., Birbaumer N., Dogil G. Reorganization of functional and effective connectivity during real-time fMRI-BCI modulation of prosody processing. Brain Lang. 2011, 117(3):123-132. 10.1016/j.bandl.2010.07.008.
69. Ruiz S., Lee S., Soekadar S.R., Caria A., Veit R., Kircher T., Sitaram R. Acquired self-control of insula cortex modulates emotion recognition and brain network connectivity in schizophrenia. Hum. Brain Mapp. 2013, 34(1):200-212. 10.1002/Hbm.21427.
70. Scherf S.K., Behrmann M., Dahl R. Facing changes & changing faces in adolescence: investigating the neural basis of key developmental shifts in social-information processing. Dev. Cogn. Neurosci. 2012, 2(2):199-219.
71. Scherf K.S., Smyth J.M., Delgado M.R. The amygdala: an agent of change in adolescent neural networks. Horm. Behav. 2013, 64(2):298-313. 10.1016/j.yhbeh.2013.05.011.
72. Sebastian C.L., Tan G.C., Roiser J.P., Viding E., Dumontheil I., Blakemore S.J. Developmental influences on the neural bases of responses to social rejection: implications of social neuroscience for education. NeuroImage 2011, 57(3):686-694. 10.1016/j.neuroimage.2010.09.063.
73. Silvers J.A., McRae K., Gabrieli J.D., Gross J.J., Remy K.A., Ochsner K.N. Age-related differences in emotional reactivity, regulation, and rejection sensitivity in adolescence. Emotion 2012, (2012-13957-001 [pii]). 10.1037/a0028297.
74. Silvers J.A., Buhle J.T., Ochsner K.N. The neuroscience of emotion regulation: basic mechanisms and their role in development, aging and psychopathology. The Oxford Handbook of Cognitive Neuroscience, Vol 2: The cutting edges 2014, vol. 2:53-78. Oxford University Press, New York.
75. Smith S.M., Bandettini P.A., Miller K.L., Behrens T.E., Friston K.J., David O., Nichols T.E. The danger of systematic bias in group-level FMRI-lag-based causality estimation. NeuroImage 2012, 59(2):1228-1229.
76. Subramanian L., Hindle J., Johnston S., Roberts M., Husain M., Goebel R., Linden D.E.J. Real-time fMRI neurofeedback for treatment of Parkinson's disease. J. Neurosci. 2011, 31(45):16309-16317.
77. Tamnes C.K., Walhovd K.B., Dale A.M., Ostby Y., Grydeland H., Richardson G., Alzheimer's Disease Neuroimaging I. Brain development and aging: overlapping and unique patterns of change. NeuroImage 2013, 68:63-74. 10.1016/j.neuroimage.2012.11.039.
78. Thompson-Schill S.L., Ramscar M., Chrysikou E.G. Cognition without control: when a little frontal lobe goes a long way. Curr. Dir. Psychol. Sci. 2009, 18(5):259-263. 10.1111/j.1467-8721.2009.01648.x.
79. 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):274-290.
80. Wager T.D., Feldman-Barrett L. From affect to control: functional specialization of the insula in motivation and regulation 2004, PsycExtra. Retrieved from, retrieved from: http://www.columbia.edu/cu/psychology/tor/.
81. Weiskopf N., Mathias K., Bock S.W., Scharnowski F., Veit R., Grodd W., Birbaumer N. Principles of a brain-computer interface (BCI) based on real-time functional magnetic resonance imaging (fMRI). IEEE Trans. Biomed. Eng. 2004, 51(6):966-970.
82. Weiskopf N., Scharnowski F., Veit R., Goebel R., Birbaumer N., Mathias K. Self-regulation of local brain activity using real-time functional magnetic resonance imaging (fMRI). J. Physiol. Paris 2004, 98:357-373.
83. Wen X., Yao L., Liu Y., Ding M. Causal interactions in attention networks predict behavioral performance. J. Neurosci. 2012, 32(4):1284-1292. 10.1523/JNEUROSCI.2817-11.2012.
84. Wen X., Liu Y., Yao L., Ding M. Top-down regulation of default mode activity in spatial visual attention. J. Neurosci. 2013, 33(15):6444-6453. 10.1523/JNEUROSCI.4939-12.2013.
85. Young K.D., Zotev V., Phillips R., Misaki M., Yuan H., Drevets W.C., Bodurka J. Real-time FMRI neurofeedback training of amygdala activity in patients with major depressive disorder. PLoS One 2014, 9(2). 10.1371/journal.pone.0088785.
86. Yuan H., Young K.D., Phillips R., Zotev V., Misaki M., Bodurka J. Resting-state functional connectivity modulation and sustained changes after real-time functional magnetic resonance imaging neurofeedback training in depression. Brain Connect. 2014, 4(9):690-701. 10.1089/brain.2014.0262.
87. Zotev V., Krueger F., Phillips R., Alvarez R.P., Simmons W.K., Bellgowan P., Bodurka J. Self-regulation of amygdala activation using real-time FMRI neurofeedback. PLoS One 2011, 6(9). (PONE-D-11-06642 [pii]). 10.1371/journal.pone.0024522.
88. Zotev V., Phillips R., Young K.D., Drevets W.C., Bodurka J. Prefrontal control of the amygdala during real-time fMRI neurofeedback training of emotion regulation. PLoS One 2013, 8(11). 10.1371/journal.pone.0079184.