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Neural Recruitment after Mild Traumatic Brain Injury Is Task Dependent: A Meta-analysis

Published online by Cambridge University Press:  09 May 2013

E.J. Bryer
Affiliation:
Department of Psychology, The Pennsylvania State University, University Park, Pennsylvania
J.D. Medaglia
Affiliation:
Department of Psychology, The Pennsylvania State University, University Park, Pennsylvania
S. Rostami
Affiliation:
Department of Psychology, The Pennsylvania State University, University Park, Pennsylvania
Frank G. Hillary*
Affiliation:
Department of Psychology, The Pennsylvania State University, University Park, Pennsylvania
*
Correspondence and reprint requests to: Frank G. Hillary, The Pennsylvania State University, Bruce V. Moore Building, Department of Psychology, University Park, PA 16802. E-mail: [email protected]

Abstract

Individuals with mild traumatic brain injury (TBI) often have deficits in processing speed and working memory (WM) and there is a growing literature using functional imaging studies to document these deficits. However, divergent results from these studies revealed both hypoactivation and hyperactivation of neural resources after injury. We hypothesized that at least part of this variance can be explained by distinct demands between WM tasks. Notably, in this literature some WM tasks use discrete periods of encoding, maintenance, and retrieval, whereas others place continuous demands on WM. The purpose of this meta-analysis is to examine the differences in neural recruitment after mTBI to determine if divergent findings can be explained as a function of task demand and cognitive load. A comprehensive literature review revealed 14 studies using functional magnetic resonance imaging to examine brain activity of individuals with mTBI during working memory tasks. Three of the fourteen studies included reported hypoactivity, five reported hyperactivity, and the remaining six reported both hypoactivity and hyperactivity. Studies were grouped according to task type and submitted to GingerALE maximum likelihood meta-analyses to determine the most consistent brain activation patterns. The primary findings from this meta-analysis suggest that the discrepancy in activation patterns is at least partially attributable to the classification of WM task, with hyperactivation being observed in continuous tasks and hypoactivation being observed during discrete tasks. We anticipate that differential task load expressed in continuous and discrete WM tasks contributes to these differences. Implications for the interpretation of fMRI signals in clinical samples are discussed. (JINS, 2013, 19, 1–12)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2013 

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References

ALE meta-analysis: Controlling the false discovery rate and performing statistical contrasts. (2005). Human Brain Mapping, 25, 155164.CrossRefGoogle Scholar
Baddeley, A.D., Hitch, G.J. (1994, October). Developments in the concept of working memory. Neuropsychology, 8(4), 485493.CrossRefGoogle Scholar
Bonnelle, V., Leech, R., Kinnunen, K.M., Ham, T.E., Beckmann, C.F., De Boissezon, X., Sharp, D.J. (2011). Default mode network connectivity predicts sustained attention deficits after traumatic brain injury. J Neurosci, 31(38), 1344213451. doi: 10.1523/jneurosci.1163-11.2011.CrossRefGoogle ScholarPubMed
Caeyenberghs, K., Leemans, A., Heitger, M.H., Leunissen, I., Dhollander, T., Sunaert, S., Dupont, P., Swinnen, S.P. (2012). Graph analysis of functional brain networks for cognitive control of action in traumatic brain injury. Brain, 135(Pt 4), 12931307.CrossRefGoogle ScholarPubMed
Chen, S.H.A., Kareken, D.A., Fastenau, P.S., Trexler, L.E., Hutchins, G.D. (2003). A study of persistent post-concussion symptoms in mild head trauma using positron emission tomography. J Neurol Neurosurg & Psychiatry, 74, 326332.CrossRefGoogle 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, 6882. doi:10.1016/j.neuroimage.2003.12.032.CrossRefGoogle ScholarPubMed
Chen, J.-K., Johnston, K.M., Collie, A., McCrory, 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 & Psychiatry, 78(11), 12311238. doi:10.1136/006.110395.CrossRefGoogle ScholarPubMed
Chen, J.-K., Johnston, K.M., Petrides, M., Ptito, A. (2008). Recovery from mild head injury in sports: Evidence from serial functional magnetic resonance imaging studies in male athletes. Clinical Journal of Sports Medicine, 18(3), 243247.CrossRefGoogle ScholarPubMed
Courtney, S.M. (2004). Attention and cognitive control as emergent properties of information representation in working memory. Cognitive, Affective, and Behavioral Neuroscience, 4(4), 501516.CrossRefGoogle ScholarPubMed
DeLuca, J., Schultheis, M.T., Madigan, N.K., Christodoulou, C., Averill, A. (2000). Acquisition versus retrieval deficits in traumatic brain injury: implications for memory rehabilitation. Arch Phys Med Rehabil, 81, 13271333.CrossRefGoogle ScholarPubMed
Eickhoff, S.B., Laird, A.R., Grefkes, C., Wang, L.E., Zilles, K., Fox, P.T. (2009). Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: A random-effects approach based on empirical estimates of spatial uncertainty. Human Brain Mapping, 30, 29072926.CrossRefGoogle Scholar
Friston, K.J., Price, C.J., Fletcher, P., Moore, C., Frackowiak, R.S., Dolan, R.J. (1996). The trouble with cognitive subtraction. Neuroimage, 4(2), 97104.CrossRefGoogle ScholarPubMed
Goldman-Rakic, P. [S.] (1987). Circuitry of primate prefrontal cortex and regulation of behavior by representational memory.CrossRefGoogle Scholar
Gosselin, N., Bottari, C., Chen, J.-K., Petrides, M., Tinawi, S., de Guise, E., Ptito, A. (2011, March) Electrophysiology and functional MRI in post-acute mild traumatic brain injury. Journal of Neurotrauma, 28, 329341. doi:10.1089/neu.2010.1493.CrossRefGoogle ScholarPubMed
Hillary, F.G. (2008). Neuroimaging of working memory dysfunction and the dilemma with brain reorganization hypotheses. Journal of the International Neuropsychological Society, 14, 526534.CrossRefGoogle ScholarPubMed
Hillary, F.G., Genova, H.M., Chiaravalloti, N.D., Rypma, B., DeLuca, J. (2006). Prefrontal modulation of working memory performance in brain injury and disease. Human Brain Mapping, 27, 837847.CrossRefGoogle ScholarPubMed
Hillary, F.G., Genova, H.M., Medaglia, J.D., Fitzpatrick, N.M., Chiou, K.S., Wardecker, B.M., Wang, J. (2010). The nature of processing speed deficits in traumatic brain injury: Is less brain more? Brain Imaging and Behavior, 4, 141154.CrossRefGoogle ScholarPubMed
Hillary, F.G., Medaglia, J.D., Gates, K., Molenaar, P.C., Slocomb, J., Peechatka, A., Good, D.C. (2011). Examining working memory task acquisition in a disrupted neural network. Brain, 134, 15551570.CrossRefGoogle Scholar
Hillary, F.G., Medaglia, J.D., Gates, K., Molenaar, P., Good, D.C. (2013). Brain connectivity changes after task practice in traumatic brain injury. Brain Imaging and Behavior. PMID: 23138853.Google Scholar
Jantzen, K.J., Anderson, B., Steinberg, F.L., Kelso, J.S. (2004, May). A prospective functional MR imaging study of mild traumatic brain injury in college football players. American Journal of Neuroradiology, 25, 738745.Google ScholarPubMed
Kim, Y.-H., Yoo, W.-K., Ko, M.-H., Park, C.-H., Kim, S.T., Na, D.L. (2009). Plasticity of the attentional network after brain injury and cognitive rehabilitation. Neurorehabilitation and Neural Repair, 23, 468477.CrossRefGoogle ScholarPubMed
Kosslyn, S.M. (1999). If neuroimaging is the answer, what is the question? Philosophical Transactions of the Royal Society of London, 354, 12831294.CrossRefGoogle ScholarPubMed
Lin, A.P., Liao, H.J., Merugumala, S.K., Prabhu, S.P., Meehan, W.P. 3rdRoss, B.D. (2012). Metabolic imaging of mild traumatic brain injury. Brain Imaging Behavior, 6(2), 208223. doi: 10.1007/s11682-012-9181-4.CrossRefGoogle ScholarPubMed
Lovell, M.R., Pardini, J.E., Welling, J., Collins, M.W., Bakal, J., Lazar, N., Eddy, (2007). Functional brain abnormalities are related to clinical recovery and time to return-to-play in athletes. Neurosurgery, 61, 352360. doi:10.1227/01.NEU.0000279985.94168.7F.CrossRefGoogle 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, 41524166. doi:10.1002/hbm.20836.CrossRefGoogle ScholarPubMed
Mayer, A.R., Mannell, M.V., Ling, J., Gasparovic, C., Yeo, R.A. (2011). Functional connectivity in mild traumatic brain injury. Human Brain Mapping, 32(11), 18251835.CrossRefGoogle ScholarPubMed
McAllister, T.W., Flashman, L.A., McDonald, B.C., Saykin, A.J. (2006). Mechanisms of working memory dysfunction after mild and moderate TBI: Evidence from functional MRI and neurogenetics. Journal of Neurotrauma, 23(10), 14501467.CrossRefGoogle ScholarPubMed
McAllister, T.W., Saykin, A., Flashman, L.A., Sparling, M.B., Johnson, S.C., Guerin, S.J., Weaver, J.B. (1999). Brain activation during working memory 1 month after mild traumatic brain injury. Neurology, 53(6).CrossRefGoogle ScholarPubMed
McAllister, T.W., Sparling, M.B., Flashman, L.A., Saykin, A.J. (2001). Neuroimaging findings in mild traumatic brain injuyr. Journal of Clinical and Experimental Neuropsychology, 23(6), 775791.CrossRefGoogle Scholar
McDowell, S., Whyte, J., D'Esposito, M. (1997). Working memory impairments in traumatic brain injury: evidence from a dual-task paradigm. Neuropsychologia, 35, 13411353.CrossRefGoogle ScholarPubMed
Medaglia, J.D., Chiou, K.S., Slocomb, J., Fitzpatrick, N.M., Wardecker, B.M., Ramanathan, D., Good, D.C. (2011, May 17). The less BOLD, the wiser: Support for the latent resource hypothesis after traumatic brain injury. Human Brain Mapping, 33, 979993.CrossRefGoogle ScholarPubMed
Medaglia, J.D., Chiou, K.S., Slocomb, J., Fitzpatrick, N.M., Wardecker, B.M., Ramanathan, D., Hillary, F.G. (2012). The Less BOLD, the Wiser: Support for the latent resource hypothesis after traumatic brain injury. Human Brain Mapping, 33(4), 979993.CrossRefGoogle ScholarPubMed
Miller, E.K., Cohen, J.D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24, 167202.CrossRefGoogle ScholarPubMed
Nakamura, T., Hillary, F.G., Biswal, B.B. (2009). Resting network plasticity following brain injury. PLoS ONE, 4(12).CrossRefGoogle ScholarPubMed
Pardini, J.E., Pardini, D.A., Becker, J.T., Dunfee, K.L., Eddy, W.F., Lovell, M.R., Welling, J.S. (2010). Postconcussive symptoms are associated with compensatory cortical recruitment during a working memory task. Neurosurgery, 67(4), 10201028. doi:10.1227/NEU.0b013e3181ee33e2.CrossRefGoogle ScholarPubMed
Pardo, J.V., Fox, P.T., Raichle, M.E. (1991). Localization of a human system for sustained attention by positron emission tomography. Nature, 349, 6164.CrossRefGoogle ScholarPubMed
Perlstein, W.M., Cole, M.A., Demery, J.A., Seignourel, P.J., Dixit, N.K., Larson, M.J., Briggs, R.W. (2004). Parametric manipulation of working memory load in traumatic brain injury: Behavioral and neural correlates. Journal of the International Neuropsychological Society, 10, 724741.CrossRefGoogle ScholarPubMed
Petrides, M., Alivisatos, B., Meyer, E., Evans, A.C. (1993, February). Functional activation of the human frontal cortex during the performance of verbal working memory tasks. Proceedings of the National Academy of Sciences, 90, 878882.CrossRefGoogle ScholarPubMed
Poldrack, R.A., Fletcher, P.C., Henson, R.N., Worsley, K.J., Brett, M., Nichols, T.E. (2008). Guidelines for reporting an fMRI study. Neuroimage 1, 40(2), 409414.CrossRefGoogle ScholarPubMed
Price, C.J., Crinion, J., Friston, K.J. (2006). Design and analysis of fMRI studies with neurologically impaired patients. Journal of Magnetic Resonance Imaging, 23(6), 816826.CrossRefGoogle ScholarPubMed
Research Imaging Institute, UTHSCSA. (n.d.). Multi-image Analysis GUI (Version 2.6) [Computer program]. Retrieved January 1, 2012, from http://ric.uthscsa.edu/mango/mango.html.Google Scholar
Sanchez-Carrion, R., Fernandez-Espejo, D., Junque, C., Falcon, C., Bargallo, N., Roig, T., Bernabeu, M., Tormos, J.M., Vendrell, P. (2008a). A longitudinal fMRI study of working memory in severe TBI patients with diffuse axonal injury. Neuroimage, 43, 421429.CrossRefGoogle ScholarPubMed
Sanchez-Carrion, R., Gomez, P.V., Junque, C., Fernandez-Espejo, D., Falcon, C., Bargallo, N., Roig-Rovira, T., Enseñat-Cantallops, A., Bernabeu, M. (2008b). Frontal hypoactivation on functional magnetic resonance imaging in working memory after severe diffuse traumatic brain injury. Journal of Neurotrauma, 25(5), 479494.CrossRefGoogle ScholarPubMed
Scheibel, R.S., Pearson, D.A., Faria, L.P., Kotrla, K.J., Aylward, E., Bachevalier, J., Levin, H.S. (2003). An fMRI study of executive functioning after severe diffuse TBI. Brain Injury, 17(11), 919930.CrossRefGoogle 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, 14471461.CrossRefGoogle ScholarPubMed
Scheibel, R.S., Pearson, D.A., Faria, L.P., Kotria, K.J., Aylward, E., Bachevalier, J., Levin, H.S. (2004). An fMRI study of executive functioning after severe diffuse TBI. Brain Injury, 18(2), 919930.CrossRefGoogle Scholar
Sharp, D.J., Beckmann, C.F., Greenwood, R., Kinnunen, K.M., Bonnelle, V., De Boissezon, X., Leech, R. (2011). Default mode network functional and structural connectivity after traumatic brain injury. Brain, 134(Pt 8), 22332247. doi: 10.1093/brain/awr175.CrossRefGoogle ScholarPubMed
Slobounov, S.M., Zhang, K., Pennell, D., Ray, W., Johnson, B., Sebastianelli, W. (2010, April). Functional abnormalities in normally appearing athletes following mild traumatic brain injury: A functional MRI study. Experimental Brain Research, 202(2), 341354. doi:10.1007/09-2141-6.CrossRefGoogle ScholarPubMed
Sweet, L.H., Rao, S.M., Primeau, M., Durgerian, S., Cohen, R.A. (2006). Functional magnetic resonance imaging response to increased verbal working memory demands among patients with multiple sclerosis. Human Brain Mapping, 27, 2836.CrossRefGoogle ScholarPubMed
Teasdale, G., Jennett, B. (1974, July). Assessment of coma and impaired consciousness. A practical scale. Lancet, 2(7872), 8184.CrossRefGoogle ScholarPubMed
Turkeltaub, P.E., Eden, G.F., Jones, K.M., Zeffiro, T.A. (2002). Meta-analysis of the functional neuroanatomy of single-word reading: Method and validation. NeuroImage, 16, 765780.CrossRefGoogle ScholarPubMed
Turkeltaub, P.E., Eickhoff, S.B., Laird, A.R., Fox, M., Wiener, M., Fox, P. (2012). Minimizing within-experiment and within-group effects in Activation Likelihood Estimation meta-analyses. Human Brain Mapping, 33(1), 113. doi: 10.1002/hbm.21186.CrossRefGoogle ScholarPubMed
Turner, G.R., Levine, B. (2008, September 9). Augmented neural activity during executive control processing following diffuse axonal injury. Neurology, 71(11), 812818.CrossRefGoogle ScholarPubMed
Turner, G.R., McIntosh, A.R., Levine, B. (2011, February 24). Prefrontal compensatory engagement in TBI is due to altered functional engagement of existing networks and not functional reorganization. Frontiers in Systems Neuroscience, 5(9), 112.CrossRefGoogle Scholar
Witt, S.T., Lovejoy, D.W., Pearlson, G.D., Stevens, M.C. (2010). Decreased prefrontal cortex activity in mild traumatic brain injury during performance of an auditory oddball task. Brain Imaging and Behavior, 4, 232247. doi:10.1007/s11682-010-9102-3.CrossRefGoogle ScholarPubMed
Zhang, K., Johnson, B., Pennell, D., Ray, W., Sebastianelli, W., Slobounov, S. (2010, July). Are functional deficits in concussed individuals consistent with white matter structural alterations: Combined FMRI & DTI study. Experimental Brain Research, 204(1), 5770. doi:10.1007/s00221-010-2294-3.CrossRefGoogle ScholarPubMed