Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-27T13:59:18.510Z Has data issue: false hasContentIssue false
  • English
  • Français

Neural Correlates of Interference Control in Adolescents with Traumatic Brain Injury: Functional Magnetic Resonance Imaging Study of the Counting Stroop Task

Published online by Cambridge University Press:  19 November 2010

Sarah J. Tlustos ,
C.-Y. Peter Chiu ,
Nicolay Chertkoff Walz ,
Scott K. Holland ,
Lori Bernard  and
Shari L. Wade
Sarah J. Tlustos
Affiliation:
Department of Psychology, University of Cincinnati, Cincinnati, Ohio
C.-Y. Peter Chiu*
Affiliation:
Department of Psychology, University of Cincinnati, Cincinnati, Ohio Department of Communication Sciences and Disorders, University of Cincinnati, Cincinnati, Ohio
Nicolay Chertkoff Walz
Affiliation:
Division of Behavioral Medicine and Clinical Psychology, Department of Pediatrics, Cincinnati Children’s Hospital Medical Center University of Cincinnati College of Medicine, Cincinnati, Ohio
Scott K. Holland
Affiliation:
University of Cincinnati College of Medicine, Cincinnati, Ohio Cincinnati Children’s Hospital Research Foundation, Department of Radiology, Cincinnati Children’s Hospital Medical Center
Lori Bernard
Affiliation:
Division of Physical Medicine and Rehabilitation, Department of Pediatrics, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio
Shari L. Wade
Affiliation:
University of Cincinnati College of Medicine, Cincinnati, Ohio Division of Physical Medicine and Rehabilitation, Department of Pediatrics, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio
*
Correspondence and reprint requests to: Peter Chiu, Department of Psychology, University of Cincinnati, 101A Dyer Hall, ML 0376, Cincinnati, OH 45221-0376. E-mail: peter.chiu@uc.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Difficulty in inhibition or cognitive control is a common and significant sequela of pediatric traumatic brain injury (TBI). The present study used functional MRI to examine one specific inhibitory function, interference control, in 11 adolescents, aged 12–16 years, (mean age, 15.7 years) with TBI who were at least 1 year postinjury and 11 age-matched typically developing control participants (TC) (mean age, 15.2 years). Participants completed a Counting Stroop task with 2 main conditions: (1) a neutral condition requiring the counting of animal words and (2) an interference condition in which mismatched number words were counted. Both TBI and TC adolescents activated similar networks of brain regions relevant to interference control, but the TBI group showed higher levels of activation relative to the TC group in multiple brain areas within this network, including predominantly right frontal and parietal regions. Findings of greater activation of the relevant neural network in the TBI group are consistent with recent fMRI findings using other interference control paradigms with individuals with a history of TBI. (JINS, 2011, 17, 000–000.)

Keywords

Childhood brain disorderInhibitionExecutive functionsBrain imagingAdolescentHead injury
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 17 , Issue 1 , January 2011 , pp. 181 - 189
Copyright
Copyright © The International Neuropsychological Society 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aarts, E., Roelofs, A., van Turennout, M. (2008). Anticipatory activity in anterior cingulate cortex can be independent of conflict and error likelihood. The Journal of Neuroscience, 28, 4671–4678. doi:10.1523/JNEUROSCI.4400-07.2008CrossRefGoogle ScholarPubMed
Anderson, V., Catroppa, C., Morse, S., Haritou, F., Rosenfeld, J. (2005). Attentional and processing skills following traumatic brain injury in early childhood. Brain Injury, 19, 699–710. doi:10.1080/02699050400025281CrossRefGoogle ScholarPubMed
Anderson, V., Fenwick, T., Manly, T., Robertson, I. (1998). Attentional skills following traumatic brain injury in childhood: A componential analysis. Brain Injury, 12, 937–949. doi:10.1080/026990598121990CrossRefGoogle ScholarPubMed
Bush, G., Frazier, J.A., Rauch, S.L., Seidman, L.J., Whalen, P.J., Jenike, M.A., Biederman, J. (1999). Anterior cingulate cortex dysfunction in attention-deficit/hyperactivity disorder revealed by fMRI and the counting stroop. Biological Psychiatry, 45, 1542–1552.CrossRefGoogle ScholarPubMed
Bush, G., Shin, L.M., Holmes, J., Rosen, B.R., Vogt, B.A. (2003). The multi-source interference task: A validation study with fMRI in individual subjects. Molecular Psychiatry, 8, 60–70. doi:10.1038/sj.mp.4001217CrossRefGoogle ScholarPubMed
Bush, G., Whalen, P.J., Rosen, B.R., Jenike, M.A., McInerney, S.C., Rauch, S.L. (1998). The counting stroop: An interference task specialized for functional neuroimaging – validation study with functional MRI. Human Brain Mapping, 6, 270–282. doi:10.1002/(SICI)1097-0193(1998)6:4<270::AID-HBM6>3.0.CO;2-03.0.CO;2-0>CrossRefGoogle ScholarPubMed
Casey, B.J., Tottenham, N., Liston, C., Durston, S. (2005). Imaging the developing brain: What have we learned about cognitive development? Trends in Cognitive Sciences, 9, 104–110. doi:10.1016/j.tics.2005.01.011CrossRefGoogle ScholarPubMed
Catroppa, C., Anderson, V. (2003). Children’s attentional skills 2 years post-traumatic brain injury. Developmental Neuropsychology, 23, 359–373. doi:10.1207/S15326942DN2303_3CrossRefGoogle ScholarPubMed
Catroppa, C., Anderson, V. (2005). A prospective study of the recovery of attention from acute to 2 years following pediatric traumatic brain injury. Journal of the International Neuropsychological Society, 11, 84–98. doi:10.1017/S1355617705050101CrossRefGoogle ScholarPubMed
Chen, J.K., Johnston, K.M., Collie, A., McCroy, P., Ptito, A. (2007). A validation of the post concussion symptom scale in the assessment of complex concussion using cognitive testing and functional MRI. Journal of Neurology, Neurosurgery, and Psychiatry, 78, 1231–1238. doi:10.1136/jnnp.2006.110395CrossRefGoogle ScholarPubMed
Chen, J.K., Johnston, K.M., Frey, S., Petrides, M., Worsley, K., Ptito, A. (2004). Functional abnormalities in symptomatic concussed athletes: an fMRI study. Neuroimage, 22, 68–82. doi:10.1016/j.neuroimage.2003.12.032CrossRefGoogle ScholarPubMed
Crosnoe, R., Trinitapoli, J. (2008). Shared family activities and the transition from childhood into adolescence. Journal of Research on Adolescence, 18, 23–48. doi:10.1111/j.1532-7795.2008.00549.xCrossRefGoogle Scholar
Delis, D.C., Kaplan, E., Kramer, J.H. (2001). Delis Kaplan Executive Function System (D-KEFS). San Antonio, TX: Psychological Corporation.Google Scholar
Dunn, L.M., Dunn, D.M. (2007). Peabody Picture Vocabulary Test (PPVT4) (4th ed.). Minneapolis, MN: NCS Pearson, Inc.Google Scholar
E-Prime [Computer software]. Sharpsburg, PA: Psychological Software Tools, Inc.Google Scholar
Ewing-Cobbs, L., Prasad, M., Fletcher, J.M., Levin, H.S., Miner, M.E., Eisenberg, H.M. (1998). Attention after pediatric traumatic brain injury: A multidimensional assessment. Child Neuropsychology, 4, 35–48. doi:10.1076/chin.4.1.35.3194CrossRefGoogle Scholar
Ewing-Cobbs, L., Prasad, M.R., Landry, S.H., Kramer, L., DeLeon, R. (2004). Executive functions following traumatic brain injury in young children: A preliminary analysis. Developmental Neuropsychology, 26, 487–512. doi:10.1207/s15326942dn2601_7CrossRefGoogle ScholarPubMed
Fan, J., Flombaum, J.I., McCandliss, B.D., Thomas, K.M., Posner, M.I. (2003). Cognitive and brain consequences of conflict. Neuroimage, 18, 42–57. doi:10.1006/nimg.2002.1319CrossRefGoogle ScholarPubMed
Gioia, G.A., Isquith, P.K., Guy, S.C. (2000). Behavior rating of executive function (BRIEF). Child Neuropsychology, 6, 235–238.CrossRefGoogle Scholar
Guy, S.C., Isquith, P.K., Gioia, G.A. (2004). BRIEF-SR: Behavior rating inventory of executive function--Self-report version. Lutz, FL: Psychological Assessment Resources.Google Scholar
Hu, X., Le, T.H., Parrish, T., Erhard, P. (1995). Retrospective estimation and correction of physiological fluctuation in functional MRI. Magnetic Resonance in Medicine, 34, 201–212. doi:10.1002/mrm.1910340211CrossRefGoogle ScholarPubMed
Keenan, H.T., Bratton, S.L. (2006). Epidemiology and outcomes of pediatric traumatic brain injury. Developmental Neuroscience, 28, 256–263. doi:10.1159/000094152CrossRefGoogle ScholarPubMed
Kramer, M.E., Chiu, C.Y., Shear, P.K., Wade, S.L. (2009). Neural correlates of verbal associative memory and mnemonic strategy use following childhood traumatic brain injury. Journal of Pediatric Rehabilitation Medicine, 2, 255–271. doi:10.3233/PRM-2009-0091CrossRefGoogle ScholarPubMed
Kramer, M.E., Chiu, C.Y., Walz, N.C., Holland, S.K., Yuan, W., Karunanayaka, P., Wade, S.L. (2008). Long-term neural processing of attention following early childhood traumatic brain injury: fMRI and neurobehavioral outcomes. Journal of the International Neuropsychological Society, 14, 424–435. doi:10.1017/S1355617708080545CrossRefGoogle ScholarPubMed
Langlois, J.A., Rutland-Brown, W., Thomas, K.E. (2006). Traumatic brain injury in the United States: Emergency department visits, hospitalizations, and deaths. Atlanta, GA: Centers for Disease Control and Prevention, National Center for Injury Prevention and Control, Retrieved from CDC website: www.cdc.gov/ncipc/pub-res/tbi../tbi%20in%20the%20us_jan_2006.pdfGoogle Scholar
Le, T.H., Hu, X. (1996). Retrospective estimation and correction of physiological artifacts in fMRI by direct extraction of physiological activity from MR data. Magnetic Resonance in Medicine, 35, 290–298.CrossRefGoogle ScholarPubMed
Ledberg, A., Akerman, S., Roland, P.E. (1998). Estimation of the probabilities of 3D clusters in functional brain images. Neuroimage, 8, 113–128. doi:10.1006/nimg.1998.0336CrossRefGoogle ScholarPubMed
Levin, H.S., Hanten, G. (2005). Executive functions after traumatic brain injury in children. Pediatric Neurology, 33, 79–93. doi:10.1016/j.pediatrneurol.2005.02.002CrossRefGoogle ScholarPubMed
Levin, H.S., Hanten, G., Li, X. (2009). The relation of cognitive control to social outcome after paediatric TBI: Implications for intervention. Developmental Neurorehabilitation, 12, 320–329. doi:10.3109/17518420903087673CrossRefGoogle ScholarPubMed
Max, J.E., Manes, F.F., Robertson, B.A.M., Mathews, K., Fox, P.T., Lancaster, J. (2005). Prefrontal and executive attention network lesions and the development of attention-deficit/hyperactivity symptomatology. Journal of the American Academy of Child and Adolescent Psychiatry, 44, 443–450. doi:10.1097/01.chi.0000156661.38576.0fCrossRefGoogle ScholarPubMed
Max, J.E., Schachar, R.J., Levin, H.S., Ewing-Cobbs, L., Chapman, S.B., Dennis, M., Landis, J. (2005a). Predictors of attention-deficit/hyperactivity disorder within 6 months after pediatric traumatic brain injury. Journal of the American Academy of Child & Adolescent Psychiatry, 44, 1032–1040. doi:10.1097/01.chi.0000173293. 05817.b1CrossRefGoogle ScholarPubMed
Max, J.E., Schachar, R.J., Levin, H.S., Ewing-Cobbs, L., Chapman, S.B., Dennis, M., Landis, J. (2005b). Predictors of secondary attention-deficit/hyperactivity disorder in children and adolescents 6 to 24 months after traumatic brain injury. Journal of the American Academy of Child & Adolescent Psychiatry, 44, 1041–1049. doi:10.1097/01.chi.0000173292.05817.f8CrossRefGoogle ScholarPubMed
Mayer, A.R., Mannell, M.V., Ling, J., Elgie, R., Gasparovic, C., Phillips, J.P., Yeo, R.A. (2009). Auditory orienting and inhibition of return in mild traumatic brain injury: A fMRI study. Human Brain Mapping, 30, 4152–4166. doi:10.1002/hbm.20836CrossRefGoogle ScholarPubMed
McAllister, T.W., Saykin, A.J., Flashman, L.A., Sparling, M.B., Johnson, S.C., Guerin, S.J., Yanofsky, N. (1999). Brain activation during working memory 1 month after mild traumatic brain injury: A functional MRI study. Neurology, 53, 1300–1308.CrossRefGoogle ScholarPubMed
McAllister, T.W., Sparling, M.B., Flashman, L.A., Guerin, S.J., Mamourian, A.C., Saykin, A.J. (2001). Differential working memory load effects after mild traumatic brain injury. Neuroimage, 14, 1004–1012. doi:10.1006/nimg.2001.0899CrossRefGoogle ScholarPubMed
Muzik, O., Chugani, D.C. (2000). Statistical parametric mapping: Assessment of application in children. Neuroimage, 12, 538–549. doi:10.1006/nimg.2000.0651CrossRefGoogle ScholarPubMed
Newsome, M.R., Scheibel, R.S., Hunter, J.V., Wang, Z.J., Chu, Z., Li, X., Levin, H.S. (2007). Brain activation during working memory after traumatic brain injury in children. Neurocase, 13, 16–24. doi:10.1080/13554790601186629CrossRefGoogle ScholarPubMed
Newsome, M.R., Scheibel, R.S., Steinberg, J.L., Troyanskaya, M., Sharma, R.G., Rauch, R.A., Levin, H.S. (2007). Working memory brain activation following severe traumatic brain injury. Cortex, 43, 95–111. doi:10.1016/S0010-9452(08)70448-9CrossRefGoogle ScholarPubMed
Newsome, M.R., Steinberg, J.L., Scheibel, R.S., Troyanskaya, M., Chu, Z., Hanten, G., Levin, H.S. (2008). Effects of traumatic brain injury on working memory-related brain activation in adolescents. Neuropsychology, 22, 419–425. doi:10.1037/0894-4105.22.4.419CrossRefGoogle ScholarPubMed
Orme, D.R., Johnstone, B., Hanks, R., Novack, T. (2004). The WRAT-3 reading subtest as a measure of premorbid intelligence among persons with brain injury. Rehabilitation Psychology, 49, 250–253.CrossRefGoogle Scholar
Pennington, B.F. (1994). The working memory function of the prefrontal cortices: Implications for developmental and individual differences in cognition. In M.M. Haith, J. Benson, R.J. Roberts, & B.F. Pennington (Eds.), Future oriented processes in development (pp. 243–289). Chicago: University of Chicago Press.Google Scholar
Posner, M.I., Rothbart, M.K. (2007). Research on attention networks as a model for the integration of psychological science. Annual Review of Psychology, 58, 1–23. doi:10.1146/annurev.psych.58.110405.085516CrossRefGoogle Scholar
Ridderinkhof, K.R., van den Wildenberg, W.P.M., Segalowitz, S.J., Carter, C.S. (2004). Neurocognitive mechanisms of cognitive control: The role of the prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain and Cognition, 56, 129–140. doi:10.1016/j.bandc.2004.09.016CrossRefGoogle ScholarPubMed
Sanchez-Carrion, R., Fernandez-Espejo, D., Junque, C., Falcon, C., Bargallo, N., Roig, T., Vendrell, P. (2008). A longitudinal fMRI study of working memory in severe TBI patients with diffuse axonal injury. Neuroimage, 43, 421–429. doi:10.1016/j.neuroimage.2008.08.003CrossRefGoogle ScholarPubMed
Schachar, R., Levin, H.S., Max, J.E., Purvis, K., Chen, S. (2004). Attention deficit hyperactivity disorder symptoms and response inhibition after closed head injury in children: Do preinjury behavior and injury severity predict outcome? Developmental Neuropsychology, 25, 179–198. doi:10.1207/s15326942dn2501&2_10CrossRefGoogle ScholarPubMed
Scheibel, R.S., Newsome, M.R., Steinberg, J.L., Pearson, D.A., Rauch, R.A., Mao, H., Levin, H.S. (2007). Altered brain activation during cognitive control in patients with moderate to severe traumatic brain injury. Neurorehabilitation and Neural Repair, 21, 36–45. doi:10.1177/1545968306294730CrossRefGoogle ScholarPubMed
Scheibel, R.S., Newsome, M.R., Troyanskaya, M., Steinberg, J.L., Goldstein, F.C., Mao, H., Levin, H.S. (2009). Effects of severity of traumatic brain injury and brain reserve on cognitive-control related brain activation. Journal of Neurotrauma, 26, 1447–1461. doi:10.1089/neu.2008.0736CrossRefGoogle ScholarPubMed
Schmithorst, V.J., Holland, S.K. (2007). Sex differences in the development of neuroanatomical functional connectivity underlying intelligence found using Bayesian connectivity analysis. Neuroimage, 35, 406–419. doi:10.1016/j.neuroimage.2006.11.046CrossRefGoogle ScholarPubMed
Smits, M., Dippel, D.W., Houston, G.C., Wielopolski, P.A., Koudstaal, P.J., Hunink, M.G., van der Lugt, A. (2009). Postconcussion syndrome after minor head injury: Brain activation of working memory and attention. Human Brain Mapping, 30, 2789–2803. doi:10.1002/hbm.20709CrossRefGoogle ScholarPubMed
Talairach, J., Tournoux, P. (1988). Coplanar stereotactic atlas of the human brain. New York, NY: Thieme.Google Scholar
Thevenaz, P., Ruttimann, U.E., Unser, M. (1998). A pyramid approach to subpixel registration based on intensity. IEEE Transactions in Image Processing, 7, 27–41. doi:10.1109/83.650848CrossRefGoogle ScholarPubMed
Wechsler, D. (2003). Wechsler Intelligence Test for Children (WISC-IV) (4th ed.). San Antonio, TX: Psychological Corporation.Google Scholar
Wigfield, A., Eccles, J. (1994). Middle grades schooling and early adolescent development: An introduction. Journal of Early Adolescence, 14, 102–106. doi:0.1177/027243169401400202CrossRefGoogle Scholar
Wilke, M., Schmithorst, V.J., Holland, S.K. (2002). Assessment of spatial normalization of whole-brain magnetic resonance images in children. Human Brain Mapping, 17, 48–60. doi:10.1002/hbm.10053CrossRefGoogle ScholarPubMed
Wilkinson, G.S., Robertson, G.J. (2006). Wide range achievement test (WRAT-4) (4th ed.). Lutz, FL: Psychological Assessment Resources, Inc.Google Scholar
Worsley, K.J., Friston, K.J. (1995). Analysis of fMRI time-series revisited – Again. Neuroimage, 2, 173–181. doi:10.1006/nimg.1995.1023CrossRefGoogle ScholarPubMed
Xiong, J., Gao, J.H., Lancaster, J.L., Fox, P.T. (1995). Clustered pixels analysis for functional MRI activation studies of the human brain. Human Brain Mapping, 3, 287–301. doi:10.1002/hbm.460030404CrossRefGoogle Scholar
Yeates, K.O., Armstrong, K., Janusz, J., Taylor, H.G., Wade, S., Stancin, T., Drotar, D. (2005). Long-term attention problems in children with traumatic brain injury. Journal of the American Academy of Child & Adolescent Psychiatry, 44, 574–584. doi:10.1097/01.chi.0000159947.50523.64CrossRefGoogle ScholarPubMed