Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-29T09:50:18.352Z Has data issue: false hasContentIssue false
  • English
  • Français

Functional Magnetic Resonance Imaging of Working Memory and Response Inhibition in Children with Mild Traumatic Brain Injury

Published online by Cambridge University Press:  12 October 2011

Lauren S. Krivitzky ,
Tresa M. Roebuck-Spencer ,
Robert M. Roth ,
Kaitlin Blackstone ,
Chad P. Johnson  and
Gerard Gioia
Lauren S. Krivitzky
Affiliation:
Division of Pediatric Neuropsychology, Department of Psychiatry and Behavioral Sciences, Children's National Medical Center, George Washington University School of Medicine and Health Sciences, Washington, District of Columbia
Tresa M. Roebuck-Spencer
Affiliation:
University of Oklahoma, Norman, Oklahoma
Robert M. Roth
Affiliation:
Brain Imaging Laboratory, Department of Psychiatry, Dartmouth Medical School, Hanover, New Hampshire
Kaitlin Blackstone
Affiliation:
Division of Pediatric Neuropsychology, Department of Psychiatry and Behavioral Sciences, Children's National Medical Center, George Washington University School of Medicine and Health Sciences, Washington, District of Columbia
Chad P. Johnson
Affiliation:
Division of Pediatric Neuropsychology, Department of Psychiatry and Behavioral Sciences, Children's National Medical Center, George Washington University School of Medicine and Health Sciences, Washington, District of Columbia
Gerard Gioia*
Affiliation:
Division of Pediatric Neuropsychology, Department of Psychiatry and Behavioral Sciences, Children's National Medical Center, George Washington University School of Medicine and Health Sciences, Washington, District of Columbia
*
Correspondence and reprint requests to: Gerard Gioia, Children's National Medical Center, 15245 Shady Grove Road, Suite 350, Rockville, MD 20852. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The current pilot study examined functional magnetic resonance imaging (fMRI) activation in children with mild traumatic brain injury (mTBI) during tasks of working memory and inhibitory control, both of which are vulnerable to impairment following mTBI. Thirteen children with symptomatic mTBI and a group of controls completed a version of the Tasks of Executive Control (TEC) during fMRI scanning. Both groups showed greater prefrontal activation in response to increased working memory load. Activation patterns did not differ between groups on the working memory aspects of the task, but children with mTBI showed greater activation in the posterior cerebellum with the addition of a demand for inhibitory control. Children with mTBI showed greater impairment on symptom report and “real world” measures of executive functioning, but not on traditional “paper and pencil” tasks. Likewise, cognitive testing did not correlate significantly with imaging results, whereas increased report of post-concussive symptoms were correlated with increased cerebellar activation. Overall, results provide some evidence for the utility of symptom report as an indicator of recovery and the hypothesis that children with mTBI may experience disrupted neural circuitry during recovery. Limitations of the study included a small sample size, wide age range, and lack of in-scanner accuracy data. (JINS, 2011, 17, 1143–1152)

Keywords

ConcussionBrainInhibitionTraumatic brain injuryCerebellumPrefrontal cortexPost concussive symptoms
Type
Regular Articles
Information
Journal of the International Neuropsychological Society , Volume 17 , Issue 6 , November 2011 , pp. 1143 - 1152
Copyright
Copyright © The International Neuropsychological Society 2011

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

Aron, A.R., Poldrack, R.A. (2005). The cognitive neuroscience of response inhibition: Relevance for genetic research in Attention-Deficit/Hyperactivity Disorder. Biological Psychiatry, 57, 1285–1292.CrossRefGoogle ScholarPubMed
Babikian, T., Asarnow, B. (2009). Neurocognitive outcomes and recovery after pediatric TBI; Meta-analytic review of the literature. Neuropsychology, 23(3), 283–296.CrossRefGoogle ScholarPubMed
Barkley, R. (1997). ADHD and the nature of self-control. New York: The Guilford Press.Google Scholar
Benjamini, Y., Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B-Methodological, 57(1), 289–300.Google Scholar
Brown, J. (1958). Some tests of the decay of immediate memory. Quarterly Journal of Experimental Psychology, 10, 12–21.CrossRefGoogle Scholar
Bunge, S.A., Dudukovic, N.M., Thomason, M.E., Vaidya, C.J., Gabrieli, J.D. (2002). Immature frontal lobe contributions to cognitive control in children: Evidence from fMRI. Neuron, 33(2), 301–311.CrossRefGoogle ScholarPubMed
Capruso, D.X., Levin, H.S. (1992). Cognitive impairment following closed head injury. Neurologic Clinics, 10(4), 879–893.CrossRefGoogle ScholarPubMed
Carroll, L.J., Cassidy, J.D., Peloso, P.M., Borg, J., von Holst, H., Holm, L., Pépin, M. (2004). Prognosis for mild traumatic brain injury: Results of the WHO collaborating centre task force on mild traumatic brain injury. Journal of Rehabilitation Medicine, 43(Suppl.), 84–105.CrossRefGoogle Scholar
Casey, B.J., Cohen, J.D., Jezzard, R.T., Noll, D.C., Trainor, R.J., Giedd, J., Rapoport, J.L. (1995). Activation of prefrontal cortex in children during a nonspatial working memory task with functional MRI. Neuroimage, 2(3), 221–229.CrossRefGoogle ScholarPubMed
Casey, B.J., Trainor, R.J., Orendi, J.L., Schubert, A.B., Nystrom, L.E., Giedd, J.N., Rapoport, J.L. (1997). A developmental functional MRI study of prefrontal activation during performance of a Go-No-Go task. Journal of Cognitive Neuroscience, 9, 835–847.CrossRefGoogle ScholarPubMed
Cassidy, J.D., Carroll, L.J., Peloso, P.M., Borg, J., von Holst, H., Holm, L., Coronado, V.G. (2004). Incidence, risk factors and prevention of mild traumatic brain injury: Results of the WHO ollaborating centre task force on mild traumatic brain injury. Journal of Rehabilitation Medicine, 43(Suppl.), 28–60.CrossRefGoogle Scholar
Delis, D.C., Kaplan, E., Kramer, J.H. (2001). Delis-Kaplan Executive Function System. San Antonio, TX: The Psychological Corporation.Google Scholar
Desmond, J.E., Fiez, J.A. (1998). Neuroimaging studies of the cerebellum: Language, learning, and memory. Trends in Cognitive Sciences, 2(9), 1364–1366.CrossRefGoogle ScholarPubMed
Evans, R.W. (2006). The postconcussion syndrome and the sequelae of mild head injury. In R.W. Evans (Ed.), Neurology and trauma (pp. 815–847). New York: Oxford Press.CrossRefGoogle Scholar
Gagnon, I., Galli, C., Friedman, D., Grilli, L., Iverson, G.L. (2009). Active rehabilitation for children who are slow to recover following sport related concussion. Brain Injury, 23(12), 956–964.CrossRefGoogle ScholarPubMed
Garavan, H., Ross, T.J., Stein, E.A. (1999). Right hemisphere dominance of inhibitory control: An event related functional MRI design. Proceedings of the National Academy of Sciences of the United States of America, 96, 8301–8306.CrossRefGoogle Scholar
Gazzaley, A., Rissman, J., D'Esposito, M. (2004). Functional Connectivity during working memory maintenance. Cognitive, Affective, & Behavioral Neuroscience, 4(4), 580–599.CrossRefGoogle ScholarPubMed
Giza, C.C., Hovda, D.A. (2001). The neurometabolic cascade of concussion. Journal of Athletic Training, 36(3), 228–235.Google ScholarPubMed
Gioia, G., Isquith, P.K., Guy, S., Kenworthy, L. (2000). Behavior rating inventory of executive functioning. Lutz, Fl: Psychological Assessment Resources, Inc.Google Scholar
Gioia, G., Schneider, J.C., Vaughan, C.G., Isquith, P.K. (2009). Which symptom assessment and approaches are most appropriate for paediatric concussion? British Journal of Sports Medicine, 43(Suppl. 1), i13–i22.CrossRefGoogle Scholar
Habas, C., Kamdar, N., Nguyen, D., Prater, K., Beckmann, C.F., Menon, V., Greicius, M.D. (2009). Distinct cerebellar contributions to intrinsic connectivity networks. The Journal of Neuroscience, 29(26), 8586–8594.CrossRefGoogle ScholarPubMed
Isquith, P.K., Roth, R.M., Gioia, G.A. (2010). Tasks of executive control. Lutz, Fl: Psychological Assessment Resources, Inc.Google Scholar
Kelly, A.M., Hester, R., Murphy, K., Javitt, D.C., Foxe, J.J., Garavan, H. (2004). Prefontal-subcortical dissociations underlying inhibitory controlled revealed by event-related fMRI. European Journal of Neuroscience, 19, 3105–3112.CrossRefGoogle Scholar
Kirkwood, M.W., Yeates, K.O., Taylor, H.G., Randolph, C., McCrea, M., Anderson, V.A. (2008). Management of pediatric mild traumatic brain injury: A neuropsychological review from injury through recovery. The Clinical Neuropsychologist, 22, 769–800.CrossRefGoogle ScholarPubMed
Klingberg, T., Vaidya, C.J., Gabrieli, J.D., Moseley, M.E., Hedehus, M. (1999). Myelination and organization of the frontal white matter in children: A diffusion tensor MRI study. Neuroreport, 10, 2817–2821.CrossRefGoogle ScholarPubMed
Konishi, S., Nakajima, K., Uchida, I., Kikyo, H., Kameyama, M., Miyashita, Y. (1999). Common inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. Brain, 122, 981–991.CrossRefGoogle ScholarPubMed
Korkman, M., Kirk, U., Kemp, S. (1997). NEPSY: A developmental neuropsychological assessment. San Antonio, TX: The Psychological Corporation.Google Scholar
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 Neuropsychological Society, 14, 424–435.CrossRefGoogle ScholarPubMed
Kraus, E., Sivak, S., Kucera, P. (1995). Epidemiological features of brain injury in children: Occurrence, children at risk, causes, and manner of injury, severity, and outcomes. In S.H.M. Broman (Ed.), Traumatic head injury in children (pp. 22–39). New York: Oxford Press.Google Scholar
Langlois, J.A., Rutland-Brown, W., Thomas, K.E. (2004). Traumatic brain injury in the United States: Emergency department visits, hospitalizations, and deaths. Atlanta, GA: US Department Health and Human Services, Centers for Disease Control and Prevention, National Center for Injury Prevention and Control.Google Scholar
Levin, H.S., Hanten, G., Chang, C., Zhang, L., Schachar, R., Ewing-Cobbs, L., Max, J.E. (2002). Working memory after traumatic brain injury in children. Annals of Neurology, 52(1), 82–88.CrossRefGoogle ScholarPubMed
Levin, H.S., Mattis, S., Ruff, R.M., Eisenberg, H.M., Marshall, L.F., Tabaddor, K., Frankowski, R.F. (1987). Neurobehavioral outcome following minor head injury: A three-center study. Journal of Neurosugery, 66(2), 234–243.Google ScholarPubMed
Maldjian, J.A., Laurienti, P.J., Kraft, R.A., Burdette, J.H. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage, 19, 1233–1239 (WFU Pickatlas, version 2.4).CrossRefGoogle ScholarPubMed
Matthews, C.G., Klove, K. (1964). Instruction manual for the Adult Neuropsychology Assessment Test Battery. Madison, WI: University of Wisconsin Medical School.Google Scholar
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(6), 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(5), 1004–1012.CrossRefGoogle ScholarPubMed
McCrea, M., Hammeke, T., Olsen, G., Leo, P., Guskiewicz, K. (2004). Unreported concussion in high school football players: Implications for prevention. Clinical Journal or Sports Medicine, 14, 13–17.CrossRefGoogle ScholarPubMed
Miyake, A., Shah, P. (1999). Models of working memory: Mechanisms of active maintenance and executive control. New York: Cambridge University Press.CrossRefGoogle Scholar
Mittenberg, W., Wittner, M.S., Miller, L.J. (1997). Postconcussion syndrome occurs in children. Neuropsychology, 11(3), 447–452.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
O'Hare, E.D., Lu, L.H., Houston, S.M., Bookheimer, S.Y., Sowell, E.R. (2008). Neurodevelopmental changes in verbal working memory load-dependency: An fMRI investigation. Neuroimage, 42(4), 1678–1685.CrossRefGoogle ScholarPubMed
Owen, A.M., McMillan, K.M., Laird, A.R., Bullmore, E. (2005). N-back working memory paradigm: A meta-analysis of normative functional neuroimaging studies. Human Brain Mapping, 25(1), 46–59.CrossRefGoogle ScholarPubMed
Peterson, L.R., Peterson, M.J. (1959). Short-term retention of individual verbal items. Journal of Experimental Psychology, 58, 193–198.CrossRefGoogle ScholarPubMed
Roth, R.M., Randolph, J.J., Koven, N.S., Isquith, P.K. (2006). Neural substrates of executive functions: Insights from functional neuroimaging. In J.R. Dupri (Ed.), Focus on neuropsychology research (pp. 1–36). Hauppauge, NY: Nova Science.Google Scholar
Roth, R.M., Saykin, A.J., Flashman, L.A., Pixley, H.S., West, J.D., Mamourian, A.C. (2007). Event related functional magnetic resonance imaging of response inhibition in obsessive compulsive disorder. Biological Psychiatry, 62, 902–909.CrossRefGoogle ScholarPubMed
Ruff, R.M., Crouch, J.A., Troster, A.I., Marshall, L.F., Buchsbaum, M.S., Lottenberg, S., Somers, L.M. (1994). Selected cases of poor outcome following a minor brain trauma: Comparing neuropsychological and positron emission tomography assessment. Brain Injury, 8(4), 297–308.CrossRefGoogle ScholarPubMed
Satz, P., Zaucha, K., McCleary, C., Light, R., Asarnow, R., Becker, D. (1997). Mild head injury in children and adolescents, A review of studies (1970–1995). Psychological Bulletin, 122(2), 107–131.CrossRefGoogle ScholarPubMed
Signoretti, S., Vagnozzi, R., Tavazzi, B., Lazzarino, G. (2010). Biochemical and neurochemical sequelae following mild traumatic brain injury; summary of experimental data and clinical implications. Neurosurgical Focus, 29(5), E1.CrossRefGoogle ScholarPubMed
Smith, A. (1982). Symbol-Digit Modalities Test (SDMT) Manual-Revised. Los Angeles, CA: Western Psychological Services.Google Scholar
Tamm, L., Menon, V., Ringel, J., Reiss, A.L. (2004). Event-related FMRI evidence of frontotemporal involvement in aberrant response inhibition and task switching in attention-deficit/hyperactivity disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 43(11), 1430–1440.CrossRefGoogle ScholarPubMed
Thomason, M.E., Race, E., Burrows, B., Whitfield-Gabrieli, S., Glover, G.H., Gabrieli, J.D. (2008). Development of spatial and verbal working memory capacity in the human brain. Journal of Cognitive Neuroscience, 21(2), 1–17.Google Scholar
Tiemeier, H., Lenroot, R.K., Greenstein, D.K., Tran, L., Pierson, R., Giedd, J.N. (2010). Cerebellum development during childhood and adolescence: A longitudinal morphometric MRI study. Neuroimage, 49(1), 63–70.CrossRefGoogle ScholarPubMed
Wager, T.D., Smith, E.E. (2003). Neuroimaging studies of working memory: A meta-analysis. Cognitive, Affective & Behavioral Neuroscience, 3(4), 255–274.CrossRefGoogle ScholarPubMed
Wechsler, D. (1999). The Wechsler Abbreviated Scale of Intelligence. San Antonio, TX: The Psychological Corporation.Google Scholar
Wechsler, D. (2004). The Wechsler Intelligence Scale for Children – 4th edition. San Antonio, TX: The Psychological Corporation.Google Scholar
Williamson, I.J., Goodman, D. (2006). Converging evidence for the under-reporting of concussions in youth ice hockey. British Journal of Sports Medicine, 40(2), 128–132.CrossRefGoogle ScholarPubMed
Woodcock, R.W., McGrew, K.S., Mather, N. (2001). Woodcock-Johnson III Tests of Achievement. Itasca, IL: Riverside Publishing.Google Scholar
Yeates, K.O. (2010). Traumatic brain injury. In K.O. Yeates, M.D. Ris, H.G. Taylor, & B. Pennington (Eds.), Pediatric neuropsychology: Research, theory, and practice (2nd ed., pp. 112–146). New York, NY: Guilford Press.Google Scholar
Yeates, K.O., Luria, J., Bartkowski, H., Rusin, J., Martin, L., Bigler, E. (1999). Postconcussive symptoms in children with mild closed head injuries. Journal of Head Trauma Rehabilitation, 14(4), 337–350.CrossRefGoogle ScholarPubMed
Yeates, K.O., Taylor, H.G. (2005). Neurobehavioural outcomes of mild head injury in children and adolescents. Pediatric Rehabilitation, 8, 5–16.Google ScholarPubMed
Yeates, K.O., Taylor, H.G., Rusin, J., Bangert, B., Dietrich, A., Nuss, K., Jones, B.L. (2009). Longitudinal trajectories of post-concussive symptoms in children with mild traumatic brain injuries and their relationship to acute clinical status. Pediatrics, 123, 735–743.CrossRefGoogle ScholarPubMed