The emergence of age-dependent social cognitive deficits after generalized insult to the developing brain: A longitudinal prospective analysis using susceptibility-weighted imaging

Human Brain Mapping

Volumn 36, Issue 5, 2015, Pages 1677-1691

  Ryan, Nicholas P ^a,b   Catroppa, Cathy ^a,b,c   Cooper, Janine M ^a   Beare, Richard ^a   Ditchfield, Michael ^d,e   Coleman, Lee ^c   Silk, Timothy ^a,f   Crossley, Louise ^a   Beauchamp, Miriam H ^g,h   Anderson, Vicki A ^a,b,c  

^a MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c ROYAL CHILDREN'S HOSPITAL   (Australia)

^d SOUTHERN HEALTH   (Australia)

^e MONASH UNIVERSITY   (Australia)

^f UNIVERSITY OF MELBOURNE   (Australia)

^g UNIVERSITÉ DE MONTRÉAL   (Canada)

^h UNIVERSITY OF MONTREAL   (Canada)

Author keywords

Brain injuries; Child; Magnetic resonance imaging; Neurobiology; Theory of Mind

Indexed keywords

ADOLESCENT; ANTISOCIAL PERSONALITY DISORDER; ARTICLE; BRAIN DAMAGE; BRAIN REGION; CHILD; CHILDHOOD INJURY; COGNITIVE DEFECT; COGNITIVE DEVELOPMENT; CONTROLLED STUDY; FEMALE; GRAY MATTER; HUMAN; INJURY SEVERITY; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; NEUROIMAGING; NEUROPATHOLOGY; PRIORITY JOURNAL; PROSPECTIVE STUDY; SCHOOL CHILD; SOCIAL COGNITION; SOCIAL COGNITIVE IMPAIRMENT; SOCIAL STATUS; STRUCTURE ACTIVITY RELATION; SUSCEPTIBILITY WEIGHTED IMAGING; THEORY OF MIND; TRAUMATIC BRAIN INJURY; WHITE MATTER; BRAIN; BRAIN INJURY; COGNITION DISORDERS; COMPLICATION; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; ONSET AGE; PATHOLOGY; PERCEPTION; PRESCHOOL CHILD; PROCEDURES; PSYCHOLOGY; SEVERITY OF ILLNESS INDEX; TIME;

ADOLESCENT; AGE OF ONSET; BRAIN; BRAIN INJURIES; CHILD; CHILD, PRESCHOOL; COGNITION DISORDERS; FEMALE; HUMANS; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; NEUROPSYCHOLOGICAL TESTS; PROSPECTIVE STUDIES; SEVERITY OF ILLNESS INDEX; SOCIAL PERCEPTION; THEORY OF MIND; TIME FACTORS;

EID: 84927647549     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22729     Document Type: Article

References (85)

1. Adolphs R (2009): The social brain: Neural basis of social knowledge. Annu Rev Psychol 60:693-716.
2. Anderson V, Moore C (1995): Age at injury as a predictor of outcome following pediatric head injury: A longitudinal perspective. Child Neuropsychol 1:187-202.
3. Anderson V, Spencer-Smith M, Leventer R, Coleman L, Anderson P, Williams J, Greenham M, Jacobs R (2010): Childhood brain insult: Can age at insult help us predict outcome? Brain 133:45-56.
4. Anderson V, Spencer-Smith M, Wood A (2011): Do children really recover better? Neurobehavioural plasticity after early brain insult. Brain 134:2197-221.
5. Babikian T, Freier MC, Tong KA, Nickerson JP, Wall CJ, Holshouser BA, Burley T, Riggs ML, Ashwal S (2005): Susceptibility weighted imaging: Neuropsychologic outcome and pediatric head injury. Pediatr Neurol 33:184-94.
6. Beauchamp MH, Anderson V (2010): SOCIAL: An integrative framework for the development of social skills. Psychol Bull 136:39-64.
7. Beauchamp MH, Ditchfield M, Babl FE, Kean M, Catroppa C, Yeates KO, Anderson V (2011a): Detecting traumatic brain lesions in children: CT versus MRI versus susceptibility weighted imaging (SWI). J Neurotrauma 28:915-927.
8. Beauchamp MH, Ditchfield M, Maller JJ, Catroppa C, Godfrey C, Rosenfeld JV, Kean MJ, Anderson VA (2011b): Hippocampus, amygdala and global brain changes 10 years after childhood traumatic brain injury. Int J Dev Neurosci 29:137-143.
9. Beauchamp MH, Beare R, Ditchfield M, Coleman L, Babl FE, Kean M, Crossley L, Catroppa C, Yeates KO, Anderson V (2013): Susceptibility weighted imaging and its relationship to outcome after pediatric traumatic brain injury. Cortex 49:591-598.
10. Belsky J, de Haan M (2011): Annual research review: Parenting and children's brain development: The end of the beginning. J Child Psychol Psychiatry 52:409-428.
11. Blakemore SJ (2008): The social brain in adolescence. Nat Rev Neurosci 9:267-277.
12. Blakemore SJ (2011): Social-cognitive development during adolescence. In: Skuse H, Bruce H, Dowdney L, Mrazek D, editors. Child Psychology and Psychiatry: Frameworks for Practice. Chichester, UK: Wiley. pp 62-66.
13. Blakemore SJ, Choudhury S (2006): Development of the adolescent brain: Implications for executive function and social cognition. J Child Psychol Psychiatry 47:296-312.
14. Chastain CA, Oyoyo UE, Zipperman M, Joo E, Ashwal S, Shutter LA, Tong KA (2009): Predicting outcomes of traumatic brain injury by imaging modality and injury distribution. J Neurotrauma 26:1183-1196.
15. Choudhury S, Blakemore SJ, Charman T (2006): Social cognitive development during adolescence. Soc Cogn Affect Neurosci 1:165-174.
16. Coffey CE, Figiel GS (1991): Neuropsychiatric significance of subcortical encephalomalacia. In: Carrol BJ, Barrett JE, editors. Psychopathology and the Brain. New York: Raven Press. pp 243-264.
17. Cohen J. 1988. Statistical power analysis for the behavioural sciences. San Diego: Academic Press. 567 p.
18. Colbert CA, Holshouser BA, Aaen GS, Sheridan C (2010): Value of cerebral microhemorrhages detected with susceptibility-weighted MR imaging for prediction of long-term outcome in children with nonaccidental trauma. Radiology 256:898-905.
19. Crowe L, Catroppa C, Babl FE, Rosenfeld JV, Anderson VA (2012): Timing of traumatic brain injury in childhood and intellectual outcome. J Pediatr Psychol 37:745-754.
20. Dennis M (1989): Language and the young damaged brain. In: Boll T, Bryant BK, editors. Clinical Neuropsychology and Brain Function: Research, Measurement and Practice. Washington: American Psychological Association. pp 85-124.
21. Dennis M, Barnes MA, Wilkinson M, Humphreys RP (1998): How children with head injury represent real and deceptive emotion in short narratives. Brain Lang 61:450-483.
22. Dennis M, Lockyer L, Lazenby AL (2000): How high-functioning children with autism understand real and deceptive emotion. Autism 4:370-381.
23. Dennis M, Purvis K, Barnes MA, Wilkinson M, Winner E (2001): Understanding of literal truth, ironic criticism, and deceptive praise following childhood head injury. Brain Lang 78:1-16.
24. Dennis M, Simic N, Taylor HG, Bigler ED, Rubin K, Vannatta K, Gerhardt CA, Stancin T, Roncadin C, Yeates KO (2012): Theory of mind in children with traumatic brain injury. J Int Neuropsychol Soc 18:908-916.
25. Dennis M, Agostino A, Taylor HG, Bigler ED, Rubin K, Vannatta K, Gerhardt CA, Stancin T, Yeates KO (2013a): Emotional expression and socially modulated emotive communication in children with traumatic brain injury. J Int Neuropsychol Soc 19:34-43.
26. Dennis M, Simic N, Agostino A, Taylor HG, Bigler ED, Rubin K, Vannatta K, Gerhardt CA, Stancin T, Yeates KO (2013b): Irony and empathy in children with traumatic brain injury. J Int Neuropsychol Soc 19:338-348.
27. Dennis M, Simic N, Bigler ED, Abildskov T, Agostino A, Taylor HG, Rubin K, Vannatta K, Gerhardt CA, Stancin T, Yeates KO (2013c): Cognitive, affective, and conative theory of mind in children with traumatic brain injury. Dev Cogn Neurosci 5:25-39.
28. Dennis M, Spiegler BJ, Simic N, Sinopoli KJ, Wilkinson A, Yeates KO, Taylor HG, Bigler ED, Fletcher JM (2014): Functional plasticity in childhood brain disorders: When, what, how, and whom to assess. Neuropsychol Rev 24:389-408. doi:10.1007/s11065-014-9261-x.
29. Donders J, Warschausky S (2007): Neurobehavioral outcomes after early versus late childhood traumatic brain injury. J Head Trauma Rehabil 22:296-302.
30. Dumontheil I, Apperly IA, Blakemore S-J (2010): Online usage of theory of mind continues to develop in late adolescence. Dev Sci 13:331-338.
31. Follett PL, Roth C, Follett D, Dammann O (2009): White matter damage impairs adaptive recovery more than cortical damage in an in silico model of activity-dependent plasticity. J Child Neurol 24:1205-1211.
32. Geraci A, Surian L, Ferraro M, Cantagallo A (2010): Theory of Mind in patients with ventromedial or dorsolateral prefrontal lesions following traumatic brain injury. BrainInj 24:978-987.
33. Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL (1999): Brain development during childhood and adolescence: A longitudinal MRI study. Nat Neurosci 2:861-863.
34. Giza CC, Prins ML (2006): Is being plastic fantastic? Mechanisms of altered plasticity after developmental traumatic brain injury. Dev Neurosci 28:364-379.
35. Greenham M, Spencer-Smith MM, Anderson PJ, Coleman L, Anderson VA (2010): Social functioning in children with brain insult. Front Hum Neurosci 4:1-10.
36. Haacke EM, Xu Y, Cheng YC, Reichenbach JR (2004): Susceptibility weighted imaging (SWI). Magn Reson Med 52:612-618.
37. Haacke EM, Mittal S, Wu Z, Neelavalli J, Cheng YC (2008): Susceptibility-weighted imaging: Technical aspects and clinical applications, part 1. AJNR Am J Neuroradiol 30:19-30.
38. Hebb D (1942): The effect of early and late brain injury upon test scores, and the nature of normal adult intelligence. Proc Am Phil Soc 85:275-292.
39. Hein G, Singer T (2007): I feel how you feel but not always: The empathic brain and its modulation. Curr Opin Neurobiol 18:153-158.
40. Herbet G, Lafargue G, Bonnetblanc F, Moritz-Gasser S, Duffau H (2013): Is the right frontal cortex really crucial in the mentalizing network? A longitudinal study in patients with a slow-growing lesion. Cortex 49:2711-2727.
41. Herbet G, Lafargue G, Bonnetblanc F, Moritz-Gasser S, de Champfleur NM, Duffau H (2014): Inferring a dual-stream model of mentalizing from associative white matter fibres disconnection. Brain 137:944-959.
42. Hudspeth WJ, Pribram KH (1990): Stages of brain and cognitive maturation. J Educ Psychol 82:881-884.
43. Johnson MH, Griffin R, Csibra G, Halit H, Farroni T, de Haan M, Tucker LA, Baron-Cohen S, Richards J (2005): The emergence of the social brain network: Evidence from typical and atypical development. Dev Psychopathol 17:599-619.
44. Johnson MH (2001): Functional brain development in humans. Nat Rev Neurosci 2:475-483.
45. Kennedy DP, Adolphs R (2012): The social brain in psychiatric and neurological disorders. Trends Cogn Sci 16:559-572.
46. Kinnunen KM, Greenwood R, Powell JH, Leech R, Hawkins PC, Bonnelle V, Patel MC, Counsell SJ, Sharp DJ (2011): White matter damage and cognitive impairment after traumatic brain injury. Brain 134:449-463.
47. Kolb B, Pellis S, Robinson TE (2004): Plasticity and functions of the orbital frontal cortex. Brain Cogn 55:104-115.
48. Kraus MF, Susmaras T, Caughlin BP, Walker CJ, Sweeney JA, Little DM (2007): White matter integrity and cognition in chronic traumatic brain injury: A diffusion tensor imaging study. Brain 130:2508-2519.
49. McMillan J, Beavis A, Jones FL (2009): The AUSEI06: A new socioeconomic index for Australia. J Sociol 45:123-149.
50. Mittal S, Wu Z, Neelavalli J, Haacke EM (2008): Susceptibility-weighted imaging: Technical aspects and clinical applications, part 2. AJNR Am J Neuroradiol 30:232-252.
51. Mosch SC, Max JE, Tranel D (2005): A matched lesion analysis of childhood versus adult-onset brain injury due to unilateral stroke: Another perspective on neural plasticity and recovery of social functioning. Cogn Behav Neurol 18:5-17.
52. Muller F, Simion A, Reviriego E, Galera C, Mazaux JM (2010): Exploring theory of mind after severe traumatic brain injury. Cortex 46:1088-1099.
53. Nelson EE, Leibenluft E, McClure EB, Pine DS (2005): The social re-orientation of adolescence: A neuroscience perspective on the process and its relation to psychopathology. Psychol Med 35:163-174.
54. Paus T (2005): Mapping brain maturation and cognitive development during adolescence. Trends Cogn Sci 9:60-68.
55. Paul A Yushkevich, Joseph Piven, Heather Cody Hazlett, Rachel Gimpel Smith, Sean Ho, James C. Gee, Guido Gerig (2006): User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability. Neuroimage 31:1116-1128.
56. Reichenbach JR, Venkatesan R, Schillinger DJ, Kido DK, Haacke EM (1997): Small vessels in the human brain: MR venography with deoxyhemoglobin as an intrinsic contrast agent. Radiology 204:272-277.
57. Ryan NP, Anderson V, Godfrey C, Eren S, Rosema S, Taylor K, Catroppa C (2013): Social communication mediates the relationship between emotion perception and externalizing behaviors in young adult survivors of pediatric traumatic brain injury (TBI). Int J Dev Neurosci 31:811-819.
58. Ryan NP, Anderson V, Godfrey C, Beauchamp MH, Coleman L, Eren S, Rosema S, Taylor K, Catroppa C (2014): Predictors of very-long-term sociocognitive function after pediatric traumatic brain injury: Evidence for the vulnerability of the immature 'social brain'. J Neurotrauma 31:649-657.
59. Scherf KS, Smyth JM, Delgado MR (2013): The amygdala: An agent of change in adolescent neural networks. Horm Behav 64:298-313.
60. Schmidt AT, Hanten GR, Li X, Orsten KD, Levin HS (2010): Emotion recognition following pediatric traumatic brain injury: Longitudinal analysis of emotional prosody and facial emotion recognition. Neuropsychologia 48:2869-2877.
61. Sehgal V, Delproposto Z, Haacke EM, Tong KA, Wycliffe N, Kido DK, Xu Y, Neelavalli J, Haddar D, Reichenbach JR (2005): Clinical applications of neuroimaging with susceptibility-weighted imaging. J Magn Reson Imaging 22:439-450.
62. Semple BD, Canchola SA, Noble-Haeusslein LJ (2012): Deficits in social behavior emerge during development after pediatric raumatic brain injury in mice. J Neurotrauma 29:2672-2683.
63. Sengpiel F (2007): The critical period. Curr Biol 17:742-743.
64. Shamay-Tsoory SG, Aharon-Peretz J (2007): Dissociable prefrontal networks for cognitive and affective theory of mind: A lesion study. Neuropsychologia 45:3054-3067.
65. Shaw P, Kabani NJ, Lerch JP, Eckstrand K, Lenroot R, Gogtay N, Greenstein D, Clasen L, Evans A, Rapoport JL, Giedd JN, Wise SP (2008): Neurodevelopmental trajectories of the human cerebral cortex. J Neurosci 28:3586-3594.
66. Sigmund GA, Tong KA, Nickerson JP, Wall CJ, Oyoyo U, Ashwal S (2007): Multimodality comparison of neuroimaging in pediatric traumatic brain injury. Pediatr Neurol 36:217-226.
67. Snodgrass C, Knott F (2006): Theory of mind in children with traumatic brain injury. Brain Inj 20:825-833.
68. Sodian B, Thoermer C, Metz U (2007): Now I see it but you don't: 14-month-olds can represent another person's visual perspective. Dev Sci 10:199-204.
69. Spitz G, Maller JJ, Ng A, O'Sullivan R, Ferris NJ, Ponsford JL (2013): Detecting lesions after traumatic brain injury using susceptibility weighted imaging: A comparison with fluid-attenuated inversion recovery and correlation with clinical outcome. J Neurotrauma 30:2038-2050.
70. Surian L, Caldi S, Sperber D (2007): Attribution of beliefs by 13-month-old infants. Psychol Sci 18:580-586.
71. Tabachnick BG, Fidell LS. 2001. Using multivariate statistics. Needham Heights, MA: Allyn and Bacon. 256 p.
72. Tasker RC, Salmond CH, Westland AG, Pena A, Gillard JH, Sahakian BJ, Pickard JD (2005): Head circumference and brain and hippocampal volume after severe traumatic brain injury in childhood. Pediatr Res 58:302-308.
73. Tlustos SJ, Chiu CYP, Walz NC, Taylor HG, Yeates KO, Wade SL (2011): Emotion labeling and socio-emotional outcomes 18 months after early childhood traumatic brain injury. J Int Neuropsychol Soc 17:1132-1142.
74. Tong KA, Ashwal SS, Holshouser BA, Shutter LA, Herigault GG, Haacke EM, et al., (2003): Hemorrhagic shearing lesions in children and adolescents with posttraumatic diffuse axonal injury: Improved detection and initial results. Radiology 227:332-339.
75. Tong KA, Ashwal S, Holshouser BA, Nickerson JP, Wall CJ, Shutter LA, Osterdock RJ, Haacke EM, Kido D (2004): Diffuse axonal injury in children: Clinical correlation with hemorrhagic lesions. Ann Neurol 56:36-50.
76. Tonks J, Williams WH, Frampton I, Yates P, Slater A (2007a): Reading emotions after child brain injury: A comparison between children with brain injury and non-injured controls. Brain Inj 21:731-739.
77. Tonks JJ, Williams WH, Frampton II, Yates PP, Slater AA (2007b): Assessing emotion recognition in 9-15-years olds: Preliminary analysis of abilities in reading emotion from faces, voices and eyes. Brain Inj 21:623-629.
78. van Praag H, Kempermann G, Gage FH (2000): Neural consequences of environmental enrichment. Nat Rev Neurosci 1:191-198.
79. Walz NC, Yeates KO, Taylor HG, Stancin T, Wade SL (2009): First-order theory of mind skills shortly after traumatic brain injury in 3- to 5-year-old children. Dev Neuropsychol 34:507-519.
80. Walz NC, Yeates KO, Taylor HG, Stancin T, Wade SL (2010): Theory of mind skills 1 year after traumatic brain injury in 6- to 8-year-old children. J Neuropsychol 4:181-195.
81. Wellman HM, Cross D, Watson J (2001): Meta-analysis of theory-of-mind development: The truth about false belief. Child Dev 72:655-684.
82. Wilde EA, Hunter JV, Newsome MR, Scheibel RS, Bigler ED, Johnson JL, Fearing MA, Cleavinger HB, Li X, Swank PR, Pedroza C, Roberson GS, Bachevalier J, Levin HS (2005): Frontal and temporal morphometric findings on MRI in children after moderate to severe traumatic brain injury. J Neurotrauma 22:333-344.
83. Wu Z, Li S, Lei J, An D, Haacke EM (2010): Evaluation of traumatic subarachnoid hemorrhage using susceptibility-weighted imaging. AJNR Am J Neuroradiol 31:1302-1310.
84. Yeates KO, Bigler ED, Dennis M, Gerhardt CA, Rubin KH, Stancin T, Taylor HG, Vannatta K (2007): Social outcomes in childhood brain disorder: A heuristic integration of social neuroscience and developmental psychology. Psychol Bull 133:535-556.
85. Yurgelun-Todd D (2006): Emotional and cognitive changes during adolescence. Curr Opin Neurobiol 17:251-257.