The development of human amygdala functional connectivity at rest from 4 to 23years: A cross-sectional study

NeuroImage

Volumn 95, Issue , 2014, Pages 193-207

  Gabard Durnam, Laurel J ^a   Flannery, Jessica ^a   Goff, Bonnie ^a   Gee, Dylan G ^a   Humphreys, Kathryn L ^a   Telzer, Eva ^b   Hare, Todd ^c   Tottenham, Nim ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Amygdala; Amygdala subnuclei; Development; Medial pre frontal cortex; Resting state

Indexed keywords

ADOLESCENCE; ADOLESCENT; ADULT; AGE DISTRIBUTION; AMYGDALOID NUCLEUS; ARTICLE; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN RADIOGRAPHY; BRAIN REGION; CHILD; CHILDHOOD; CROSS-SECTIONAL STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INSULA; LIMBIC CORTEX; MALE; NEUROIMAGING; NEWBORN; NORMAL HUMAN; PARAHIPPOCAMPAL GYRUS; POSTERIOR CINGULATE; PRIORITY JOURNAL; RESTING STATE NETWORK; SUPERIOR TEMPORAL SULCUS; BRAIN MAPPING; GROWTH, DEVELOPMENT AND AGING; IMAGE PROCESSING; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PRESCHOOL CHILD; REST; YOUNG ADULT;

ADOLESCENT; AMYGDALA; BRAIN MAPPING; CHILD; CHILD, PRESCHOOL; CROSS-SECTIONAL STUDIES; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; REST; YOUNG ADULT;

EID: 84899684216     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.03.038     Document Type: Article

References (86)

1. Adolphs R., Spezio M. Role of the amygdala in processing visual social stimuli. Prog. Brain Res. 2006, 156:363-378.
2. Amaral D.G., Price J.L., Pitkanen A., Carmichael S.T. Anatomical organization of the primate amygdaloid complex. The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction 1992, 1-66. Wiley-Liss, New York. J.P. Aggleton (Ed.).
3. Amunts K., Kedo O., Kindler M., Pieperhoff P., Mohlberg H., Shah N.J., Habel U., Schneider F., Zilles K. Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps. Anat. Embryol. 2005, 210:343-352.
4. Anand A., Li Y., Wang Y., Wu J., Gao S., Bukhari L., Mathews V.P., Kalnin A., Lowe M.J. Activity and connectivity of brain mood regulating circuit in depression: a functional magnetic resonance study. Biol. Psychiatry 2005, 57:1079-1088.
5. Ball T., Rahm B., Eickhoff S.B., Schulze-Bonhage A., Speck O., Mutschler I. Response properties of human amygdala subregions: evidence based on functional MRI combined with probabilistic anatomical maps. PLoS One 2007, 2:e307.
6. Banks S.J., Eddy K.T., Angstadt M., Nathan P.J., Phan K.L. Amygdala-frontal connectivity during emotion regulation. Soc. Cogn. Affect. Neurosci. 2007, 2:303-312.
7. Baseler H.A., Harris R.J., Young A.W., Andrews T.J. Neural responses to expression and gaze in the posterior superior temporal sulcus interact with facial identity. Cereb. Cortex 2012, 24:737-744.
8. Berking M., Wupperman P. Emotion regulation and mental health: recent findings, current challenges, and future directions. Curr. Opin. Psychiatry 2012, 25:128-134.
9. Bunge S.A., Dudukovic N.M., Thomason M.E., Vaidya C.J., Gabrielli J.D. Immature frontal lobe contributions to cognitive control in children: evidence from fMRI. Neuron 2002, 33:301-311.
10. Cabral J., Hugues E., Sporns O., Deco G. Role of local network oscillations in resting-state functional connectivity. NeuroImage 2011, 57:130-139.
11. Casey B.J., Trainor R., Giedd J., Vauss Y., Vaituzis C.K., Hamburger S., Kozuch P., Rapoport J.L. The role of the anterior cingulate in automatic and controlled processes: a developmental neuroanatomical study. Dev. Psychobiol. 1997, 30:61-69.
12. Casey B.J., Giedd J.N., Thomas K.M. Structural and functional brain development and its relation to cognitive development. Biol. Psychol. 2000, 54:241-257.
13. Chai X.J., Ofen N., Gabrieli J.D.E., Whitfield-Gabrieli S. Selective development of anticorrelated networks in the intrinsic functional organization of the human brain. J. Cogn. Neurosci. 2014, 26:501-513.
14. Chang C., Glover G.H. Effects of model-based physiological noise correction on default mode network anti-correlations and correlations. NeuroImage 2009, 47:1448-1459.
15. Chen G., Chen G., Xie C., Ward B.D., Li W., Antuono P., Li S.J. A method to determine the necessity for global signal regression in resting-state fMRI studies. Magn. Reson. Med. 2012, 68:1828-1835.
16. Cisler J.M., Olatunji B.O. Emotion regulation and anxiety disorders. Curr. Psychiatry Rep. 2012, 14:182-187.
17. Cox R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 1996, 29:162-173.
18. Das P., Kemp A.H., Flynn G., Harris A.W., Liddell B.J., Whitford T.J., Peduto A., Gordon E., Williams L.M. Functional disconnections in the direct and indirect amygdala pathways for fear processing in schizophrenia. Schizophr. Res. 2007, 90:284-294.
19. Davis K.D., Talor S.J., Crawley A.P., Wood M.L., Mikulis D.J. Functional MRI of pain- and attention-related activations in the human cingulate cortex. J. Neurophysiol. 1997, 77:3370-3380.
20. Davis F.C., Johnstone T., Mazzulla E.C., Oler J.A., Whalen P.J. Regional response differences across the human amygdaloid complex during social conditioning. Cereb. Cortex 2010, 20:612-621.
21. Etkin A., Egner T., Peraza D.M., Kandel E.R., Hirsch J. Resolving emotional conflict: a role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron 2006, 51:871-882.
22. Etkin A., Egner T., Kalisch R. Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn. Sci. 2011, 15:85-93.
23. Fair D.A., Cohen A.L., Power J.D., Dosenbach N.U.F., Church J.A., Miezin F.M., Schlaggar B.L., Petersen S.E. Functional brain networks develop from a "local to distributed" organization. PLoS Comput. Biol. 2009, 5:e1000381.
24. Fisher P.M., Meltzer C.C., Price J.C., Coleman R.L., Ziolko S.K., Becker C., Moses-Kolko E.L., Berga S.L., Hariri A.R. Medial prefrontal cortex 5-HT(2A) density is correlated with amygdala reactivity, response habituation, and functional coupling. Cereb. Cortex 2009, 19:2499-2507.
25. Fox M.D., Zhang D., Snyder A.Z., Raichle M.E. The global signal and observed anticorrelated resting state brain networks. J. Neurophysiol. 2009, 101:3270-3283.
26. Gee D.G., Humphreys K.L., Flannery J., Goff B., Telzer E.H., Shapiro M., Hare T.A., Bookheimer S.Y., Tottenham N. A developmental shift from positive to negative connectivity in human amygdala-prefrontal circuitry. J. Neurosci. 2013, 33:4584-4593.
27. Giedd J.N., Vaituzis A.C., Hamburger S.D., Lange N., Rajapakse J.C., Kaysen D., Vauss Y.C., Rapoport J.L. Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: ages 4-18years. J. Comp. Neurol. 1996, 366:223-230.
28. Gilmore J.H., Shi F., Woolson S.L., Knickmeyer R.C., Short S.J., Lin W., Zhu H., Hamer R.M., Styner M., Shen D. Longitudinal development of cortical and subcortical gray matter from birth to 2years. Cereb. Cortex 2012, 22:2478-2485.
29. Gogtay N., Giedd J.N., Lusk L., Hayashi K.M., Greenstein D., Vaituzis A.C., Nugent T.F., Herman D.H., Clasen L.S., Toga A.W., Rapoport J.L., Thompson P.M. Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:8174-8179.
30. 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.
31. Hallquist M.N., Hwang K., Luna B. The nuisance of nuisance regression: spectral misspecification in a common approach to resting-state fMRI preprocessing reintroduces noise and obscures functional connectivity. NeuroImage 2013, 82:208-225.
32. Hampson M., Driesen N., Roth J.K., Gore J.C., Constable R.T. Functional connectivity between task-positive and task-negative brain areas and its relation to working memory performance. Magn. Reson. Imaging 2010, 28:1051-1057.
33. 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, 63:927-934.
34. Hariri A.R., Mattay V.S., Tessitore A., Fera F., Weinberger D.R., James W. Neocortical modulation of the amygdala response to fearful stimuli. Biol. Psychiatry 2003, 53:494-501.
35. He H., Liu T.T. A geometric view of global signal confounds in resting-state functional MRI. NeuroImage 2012, 59:2339-2348.
36. Henry J.D., Rendell P.G., Green M.J., McDonald S., O'Donnell M. Emotion regulation in schizophrenia: affective, social, and clinical correlates of suppression and reappraisal. J. Abnorm. Psychol. 2008, 117:473-478.
37. Huttenlocher P.R. Morphometric study of human cerebral cortex development. Neuropsychologia 1990, 28:517-527.
38. Khundrakpam B.S., Reid A., Brauer J., Carbonell F., Lewis J., Ameis S., et al. Developmental changes in organization of structural brain networks. Cereb. Cortex 2013, 23:2072-2085.
39. Killgore W.D., Yurgelun-Todd D.A. Sex-related developmental differences in the lateralized activation of the prefrontal cortex and amygdala during perception of facial affect. Percept. Mot. Skills 2004, 99:371-391.
40. Kim M.J., Loucks R.A., Palmer A.L., Brown A.C., Solomon K.M., Marchante A.N., Whalen P.J. The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety. Behav. Brain Res. 2011, 223:403-410.
41. Kim M.J., Gee D.G., Loucks R.A., Davis F.C., Whalen P.J. Anxiety dissociates dorsal and ventral medial prefrontal cortex functional connectivity with the amygdala at rest. Cereb. Cortex 2011, 21:1667-1673.
42. LeDoux J. The emotional brain, fear, and the amygdala. Cell. Mol. Neurobiol. 2003, 23:727-738.
43. Lee H., Heller A.S., van Reekum C.M., Nelson B., Davidson R.J. Amygdala-prefrontal coupling underlies individual differences in emotion regulation. NeuroImage 2012, 62:1575-1581.
44. Linnman C., Zeidan M.A., Furtak S.C., Pitman R.K., Quirk G.J., Milad M.R. Resting amygdala and medial prefrontal metabolism predicts functional activation of the fear extinction circuit. Am. J. Psychiatry 2012, 169:415-423.
45. Lou H.C., Luber B., Crupain M., Keenan J.P., Nowak M., Kjaer T.W., Sackeim H.A., Lisanby S.H. Parietal cortex and representation of the mental self. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6827-6832.
46. Luna B., Thulborn K.R., Munoz D.P., Merriam E.P., Garver K.E., Minshew N.J., Keshavan M.S., Genovese C.R., Eddy W.F., Sweeney J.A. Maturation of widely distributed brain function subserves cognitive development. NeuroImage 2001, 13:786-793.
47. Maddock R.J., Garrett A.S., Buonocore M.H. Posterior cingulate cortex activation by emotional words: fMRI evidence from a valence decision task. Hum. Brain Mapp. 2003, 18:30-41.
48. McRae K., Gross J.J., Weber J., Robertson E.R., Sokol-Hessner P., Ray R.D., Gabrieli J.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, 7:11-22.
49. Murphy K., Birn R.M., Handwerker D.A., Jones T.B., Bandettini P.A. The impact of global signal regression on resting state correlations: are anti-correlated networks introduced?. NeuroImage 2009, 44:893-905.
50. Ochsner K.N., Silvers J.A., Buhle J.T. Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion. Ann. N. Y. Acad. Sci. 2012, 1251:E1-E24.
51. Perlman S.B., Pelphrey K.A. Developing connections for affective regulation: age-related changes in emotional brain connectivity. J. Exp. Child Psychol. 2011, 108:607-620.
52. Pessoa L., Adolphs R. Emotion processing and the amygdala: from a "low road" to "many roads" of evaluating biological significance. Nat. Rev. Neurosci. 2010, 11:773-783.
53. Petersen A.C., Crockett L., Richards M., Boxer A. A self-report measure of pubertal status: reliability, validity, and initial norms. J. Youth Adolesc. 1988, 17:117-133.
54. Phan K.L., Fitzgerald D.A., Nathan P.J., Moore G.J., Uhde T.W., Tancer M.E. Neural substrates for voluntary suppression of negative affect: a functional magnetic resonance imaging study. Biol. Psychiatry 2005, 57:210-219.
55. 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, 4:437-441.
56. Phillips M.L., Drevets W.C., Rauch S.L., Lane R. Neurobiology of emotion perception I: the neural basis of normal emotion perception. Biol. Psychiatry 2003, 54:504-514.
57. Pitkänen A. Connectivity of the rat amygdaloid complex. The amygdala: a functional analysis 2000, 2:31-115.
58. Pizoli C.E., Shah M.N., Snyder A.Z., Shimony J.S., Limbrick D.D., Raichle M.E., Schlaggar B.L., Smyth M.D. Resting-state activity in development and maintenance of normal brain function. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:11638-11643.
59. Power J.D., Barnes K.A., Snyder A.Z., Schlaggar B.L., Petersen S.E. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage 2012, 59:2142-2154.
60. Price J.L. Comparative aspects of amygdala connectivity. Ann. N. Y. Acad. Sci. 2003, 985:50-58.
61. Qin S., Young C.B., Supekar K., Uddin L.Q., Menon V. Immature integration and segregation of emotion-related brain circuitry in young children. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:7941-7946.
62. Raichle M.E. Two views of brain function. Trends Cogn. Sci. 2010, 14:180-190.
63. Roy A.K., Shehzad Z., Margulies D.S., Kelly A.M., Uddin L.Q., Gotimer K., Biswal B.B., Castellanos F.X., Milham M.P. Functional connectivity of the human amygdala using resting state fMRI. NeuroImage 2009, 45:614-626.
64. Saad Z.S., Gotts S.J., Murphy K., Chen G., Jo H.J., Martin A., Cox R.W. Trouble at rest: how correlation patterns and group differences become distorted after global signal regression. Brain Connect. 2012, 2:25-32.
65. Sarkheil P., Goebel R., Schneider F., Mathiak K. Emotion unfolded by motion: a role for parietal lobe in decoding dynamic facial expressions. Soc. Cogn. Affect. Neurosci. 2012, 8:950-957.
66. Satterthwaite T.D., Wolf D.H., Loughead J., Ruparel K., Elliott M.A., Hakonarson H., Gur R.C., Gur R.E. Impact of in-scanner head motion on multiple measures of functional connectivity: relevance for studies of neurodevelopment in youth. NeuroImage 2012, 60:623-632.
67. Sowell E.R., Trauner D.A., Gamst A., Jernigan T.L. Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study. Dev. Med. Child Neurol. 2007, 44:4-16.
68. Sporns O., Zwi J.D. The small world of the cerebral cortex. Neuroinformatics 2004, 2:145-162.
69. Supekar K., Musen M., Menon V. Development of large-scale functional brain networks in children. PLoS Biol. 2009, 7:e1000157.
70. Swartz J.R., Carrasco M., Wiggins J.L., Thomason M.E., Monk C.S. Age-related changes in the structure and function of prefrontal cortex-amygdala circuitry in children and adolescents: a multimodal imaging study. NeuroImage 2014, 86:212-220.
71. Talairach J., Tournoux P. Co-planar stereotaxic atlas of the human brain 1988, Theime, Germany, Stuttgart.
72. Thomas K.M., Drevets W.C., Whalen P.J., Eccard C.H., Dahl R.E., Ryan N.D., Casey B.J. Amygdala response to facial expressions in children and adults. Biol. Psychiatry 2001, 49:309-316.
73. Tomasi D., Wang G.J., Volkow N.D. Energetic cost of brain functional connectivity. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:13642-13647.
74. Tottenham N., Sheridan M.A. A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing. Front. Hum. Neurosci. 2009, 3:68.
75. Uddin L.Q., Supekar K., Menon V. Typical and atypical development of functional human brain networks: insights from resting-state FMRI. Front. Syst. Neurosci. 2010, 4:21.
76. Ulfig N., Setzer M., Bohl J. Ontogeny of the human amygdala. Ann. N. Y. Acad. Sci. 2003, 985:22-33.
77. 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.
78. Van Dijk K.R., 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.
79. Van Dijk K.R., Sabuncu M.R., Buckner R.L. The influence of head motion on intrinsic functional connectivity MRI. NeuroImage 2012, 59:431-438.
80. Wang F., Kalmar J.H., He Y., Jackowski M., Chepenik L.G., Edmiston E.E., Tie K., Gong G., Shah M.P., Jones M., Uderman J., Constable R.T., Blumberg H.P. Functional and structural connectivity between the perigenual anterior cingulate and amygdala in bipolar disorder. Biol. Psychiatry 2009, 66:516-521.
81. Wang D.-Y., Han X.-J., Li S.-F., Liu D.-Q., Yan C.-G., Zuo X.-N., Zhu C.-Z., He Y., Kiviniemi V., Zang Y.-F. Effects of Apolipoprotein E genotype on the off-line memory consolidation. PLoS One 2012, 7:e51617.
82. Weissenbacher A., Kasess C., Gerstl F., Lanzenberger R., Moser E., Windischberger C. Correlations and anticorrelations in resting-state functional connectivity MRI: a quantitative comparison of preprocessing strategies. NeuroImage 2009, 47:1408-1416.
83. Yan C.G., Cheung B., Kelly C., Colcombe S., Craddock R.C., Di Martino A., Li Q., Zuo X.N., Castellanos F.X., Milham M.P. A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. NeuroImage 2013, 76:183-201.
84. Zhang S., Li C.R. Functional connectivity mapping of the human precuneus by resting state fMRI. NeuroImage 2012, 59:3548-3562.
85. Zhang S., Li C.-S.R. Functional clustering of the human inferior parietal lobule by whole brain connectivity mapping of resting state fMRI signals. Brain Connect. 2013, 10.1089/brain.2013.0191.
86. Zhang S., Hu S., Chao H.H., Ide J.S., Luo X., Farr O.M., Li C.-S.R. Ventromedial prefrontal cortex and the regulation of physiological arousal. Soc. Cogn. Affect. Neurosci. 2013, 10.1093/scan/nst064.