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Structural white matter differences underlying heterogeneous learning abilities after TBI

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Abstract

The existence of learning deficits after traumatic brain injury (TBI) is generally accepted; however, our understanding of the structural brain mechanisms underlying learning impairment after TBI is limited. Furthermore, our understanding of learning after TBI is often at risk for overgeneralization, as research often overlooks within sample heterogeneity in learning abilities. The present study examined differences in white matter integrity in a sample of adults with moderate to severe TBI who differed in learning abilities. Adults with moderate to severe TBI were grouped into learners and non-learners based upon achievement of the learning criterion of the open-trial Selective Reminding Test (SRT). Diffusion tensor imaging (DTI) was used to identify white matter differences between the learners and non-learners. Adults with TBI who were able to meet the learning criterion had greater white matter integrity (as indicated by higher fractional anisotropy [FA] values) in the right anterior thalamic radiation, forceps minor, inferior fronto-occipital fasciculus, and forceps minor than non-learners. The results of the study suggest that differences in white matter integrity may explain the observed heterogeneity in learning ability after moderate to severe TBI. This also supports emerging evidence for the involvement of the thalamus in higher order cognition, and the role of thalamo-cortical tracts in connecting functional networks associated with learning.

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References

  • Arenth, P., Russell, K., Scanlon, J., Kessler, L., & Ricker, J. (2012). Encoding and recognition after TBI: neuropsychological and fMRI findings. Journal of Clinical and Experimental Neuropsychology, 34(4), 333–344.

    Article  PubMed  PubMed Central  Google Scholar 

  • Behrens, T., Woolrich, M., Jenkinson, M., Johansen-Berg, H., Nunes, R., Clare, S., & Smith, S. (2003). Characterization and propogation of uncertainty in diffusion-weighted MR imaging. Magnetic Resonance in Medicine, 50(5), 1077–1088.

    Article  CAS  PubMed  Google Scholar 

  • Bigler, E. D. (2003). Neurobiology and neuropathology underlie the neuropsychological deficits associated with traumatic brain injury. Archives of Clinical Neuropsychology, 18(6), 595–621. discussion 623–7.

    Article  PubMed  Google Scholar 

  • Blachstein, H., Vakil, E., & Hoofien, D. (1993). Impaired learning in patients with closed-head injuries: an analysis of components of the acquisition process. Neuropsychology, 7(4), 530–535.

    Article  Google Scholar 

  • Blumenfeld, R. S., & Ranganath, C. (2006). Dorsolateral prefrontal cortex promotes long-term memory formation through its role in working memory organization. The Journal of Neuroscience, 26(3), 916–925.

    Article  CAS  PubMed  Google Scholar 

  • Chiaravalloti, N., Balzano, J., Moore, N., & DeLuca, J. (2009). The open-trial selective reminding test (OT-SRT) as a tool for the assessment of learning and memory. The Clinical Neuropsychologist, 23(2), 231–254.

    Article  PubMed  Google Scholar 

  • Chiaravalloti, N., Sandry, J., Moore, N., & DeLuca, J. (2015). An RCT to treat learning impairment in traumatic brain injury: The TBI-MEM trial. Neurorehabilitation and Neural Repair. Advanced online publication.

  • Chiou, K. S., Sandry, J., & Chiaravalloti, N. D. (2015). Cognitive contributions to differences in learning after moderate to severe traumatic brain injury. Journal of Clinical and Experimental Neuropsychology, 37(10), 1074–1085.

    Article  PubMed  Google Scholar 

  • Christidi, F., Bigler, E. D., McCauley, S. R., Schnelle, K. P., Merkley, T. L., Mors, M. B., & Wilde, E. A. (2011). Diffusion tensor imaging of the perforant pathway zone and its relation to memory function in patients with severe traumatic brain injury. Journal of Neurotrauma, 28(5), 711–725.

    Article  PubMed  Google Scholar 

  • 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. Archives of Physical Medicine and Rehabilitation, 81(10), 1327–33.

    Article  CAS  PubMed  Google Scholar 

  • Dikmen, S., Machamer, J., Fann, J. R., & Temkin, N. R. (2010). Rates of symptom reporting following traumatic brain injury. Journal of the International Neuropsychological Society, 16(3), 401–11.

    Article  PubMed  Google Scholar 

  • Gillis, M. M., & Hampstead, B. M. (2014). A two-part preliminary investigation of encoding-related activation changes after moderate to severe traumatic brain injury: hyperactivation, repetition suppression, and the role of the prefrontal cortex. Brain Imaging and Behavior.

  • Huisman, T. A. G. M., Schwamm, L. H., Schaefer, P. W., Koroshetz, W. J., Shetty-Alva, N., Ozsunar, Y., & Sorensen, A. G. (2004). Diffusion tensor imaging as potential biomarker of white matter injury in diffuse axonal injury. American Journal of Neuroradiology, 25(3), 370–6.

    PubMed  Google Scholar 

  • Jankowski, M. M., Ronnqvist, K. C., Tsanov, M., Vann, S. D., Wright, N. F., Erichsen, J. T., & O’Mara, S. M. (2013). The anterior thalamus provides a subcortical circuit supporting memory and spatial navigation. Frontiers in Systems Neuroscience, 7, 1–12.

    Article  Google Scholar 

  • Jenkinson, M., Beckman, C., Behrens, T., Woolrich, M., & Smith, S. (2012). FSL. NeuroImage, 62, 782–790.

    Article  PubMed  Google Scholar 

  • Kane, M. J., & Engle, R. W. (2000). Working-memory capacity, proactive interference, and divided attention : limits on long-term memory retrieval. Journal of Experimental Psychology: Learning, Memory, and Cognition, 26(2), 336–358.

    CAS  PubMed  Google Scholar 

  • Kinnunen, K. M., Greenwood, R., Powell, J. H., Leech, R., Hawkins, P. C., Bonnelle, V., & Sharp, D. J. (2011). White matter damage and cognitive impairment after traumatic brain injury. Brain, 134(Pt 2), 449–63.

    Article  PubMed  Google Scholar 

  • Kraus, M. F., Susmaras, T., Caughlin, B. P., Walker, C. J., Sweeney, J. A., & Little, D. M. (2007). White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain, 130(Pt 10), 2508–19.

    Article  PubMed  Google Scholar 

  • Larrabee, G., Trahan, D., & Levin, H. (2000). Normative data for a six-trial administration of the Verbal Selective Reminding Test. Clinical Neuropsychology, 14(1), 110–118.

    Article  CAS  Google Scholar 

  • Levin, H., Wilde, E., Troyanskaya, M., Petersen, N., Scheibel, R., Newsome, M., & Li, X. (2010). Diffusion tensor imaging of mild to moderate blast-related. Journal of Neurotrauma, 27(4), 683–694.

    Article  PubMed  Google Scholar 

  • Little, D. M., Kraus, M. F., Joseph, J., Geary, E. K., Susmaras, T., Zhou, X. J., & Gorelick, P. B. (2010). Thalamic integrity underlies executive dysfunction in traumatic brain injury. Neurology, 74(7), 558–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mesulam, M. (1990). Large scale neuro-cognitive networks and distributed processing for attention, language, and memory. Annals of Neurology, 28, 597–613.

    Article  CAS  PubMed  Google Scholar 

  • Millis, S. R., & Ricker, J. H. (1994). Verbal learning patterns in moderate and severe traumatic brain injury. Journal of Clinical and Experimental Neuropsychology, 16, 498–507.

    Article  CAS  PubMed  Google Scholar 

  • Millis, S., Rosenthal, M., Novack, T., Sherer, M., Nick, T., Kruetzer, J., & Ricker, J. (2001). Long term neuropsychological outcome after traumatic brain injury. The Journal of Head Trauma Rehabilitation, 16(4), 343–355.

    Article  CAS  PubMed  Google Scholar 

  • Mori, S., Wakana, S., Nagae-Poetscher, L., & van Zijil, P. (2005). MRI Atlas of Human White Matter. Amsterdam: Elsevier.

    Google Scholar 

  • Petrides, M. (2000). The role of the mid-dorsolateral prefrontal cortext in working memory. In W. Schneider, A. Owen, & J. Duncan (Eds.), Executive Control and the Frontal Lobe: Current Issues (pp. 44–54). Berlin: Springer.

    Chapter  Google Scholar 

  • Povlishock, J. T., & Christman, C. W. (1995). The pathobiology of traumatically induced axonal injury in animals and humans: a review of current thoughts. Journal of Neurotrauma, 12(4), 555–64.

    Article  CAS  PubMed  Google Scholar 

  • Ranganath, C., Cohen, M. X., & Brozinsky, C. J. (2005). Working memory maintenance contributes to long-term memory formation: neural and behavioral evidence. Journal of Cognitive Neuroscience, 17(7), 994–1010.

    Article  PubMed  Google Scholar 

  • Saalmann, Y. B. (2014). Intralaminar and medial thalamic influence on cortical synchrony, information transmission and cognition. Frontiers in Systems Neuroscience, 8, 83.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sallet, J., Mars, R. B., Noonan, M. P., Neubert, F.-X., Jbabdi, S., O’Reilly, J. X., & Rushworth, M. F. (2013). The organization of dorsal frontal cortex in humans and macaques. The Journal of Neuroscience, 33(30), 12255–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharp, D. J., & Ham, T. E. (2011). Investigating white matter injury after mild traumatic brain injury. Current Opinion in Neurology, 24(6), 558–563.

    Article  PubMed  Google 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), 2233–47.

    Article  PubMed  Google Scholar 

  • Smith, S. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17(3), 143–155.

    Article  PubMed  Google Scholar 

  • Smith, S. M., & Nichols, T. E. (2009). Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage, 44(1), 83–98.

    Article  PubMed  Google Scholar 

  • Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E. J., Johansen-berg, H., & Matthews, P. M. (2004). Advances in functional and structural MR image analysis and implementation as FSL technical report TR04SS2. NeuroImage, 23(S1), 208–219.

    Article  Google Scholar 

  • Smith, S. M., Jenkinson, M., Johansen-berg, H., Rueckert, D., Nichols, T., Mackay, C., & Behrens, T. E. J. (2006). Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage, 31, 1487–1505.

    Article  PubMed  Google Scholar 

  • Strangman, G. E., Goldstein, R., O’Neil-Pirozzi, T. M., Kelkar, K., Supelana, C., Burke, D., & Glenn, M. B. (2009). Neurophysiological alterations during strategy-based verbal learning in traumatic brain injury. Neurorehabilitation and Neural Repair, 23(3), 226–236.

    Article  PubMed  Google Scholar 

  • Vakil, E. (2005). The effect of moderate to severe traumatic brain injury (TBI) on different aspects of memory: a selective review. Journal of Clinical and Experimental Neuropsychology, 27(8), 977–1021.

    Article  PubMed  Google Scholar 

  • Vanderploeg, R. D., Curtiss, G., & Belanger, H. G. (2005). Long-term neuropsychological outcomes following mild traumatic brain injury. Journal of the International Neuropsychological Society, 11(3), 228–236.

    Article  PubMed  Google Scholar 

  • Voelbel, G. T., Genova, H. M., Chiaravalotti, N. D., & Hoptman, M. J. (2012). Diffusion tensor imaging of traumatic brain injury review : implications for neurorehabilitation. NeuroRehabilitation, 31, 281–293.

    PubMed  Google Scholar 

  • Whiting, M. D., & Hamm, R. J. (2008). Mechanisms of anterograde and retrograde memory impairment following experimental traumatic brain injury. Brain Research, 1213, 69–77.

    Article  CAS  PubMed  Google Scholar 

  • Winkler, A., Ridgway, G., Webster, M., Smith, S., & Nichols, T. (2014). Permutation inference for the general linear model. NeuroImage, 92, 381–397.

    Article  PubMed  PubMed Central  Google Scholar 

  • Woolrich, M., Jbabdi, S., Patenaude, B., Chappell, M., Makni, S., Behrens, T., & Smith, S. (2009). Bayesian analysis of neuroimaging data in FSL. NeuroImage, 45(S1), 173–186.

    Article  Google Scholar 

  • Wright, M. J., & Schmitter-Edgecombe, M. (2011). The impact of verbal memory encoding and consolidation deficits during recovery from moderate-to-severe traumatic brain injury. The Journal of Head Trauma Rehabilitation, 26(3), 182–91.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Traumatic Brain Injury Research, Kessler Foundation, West Orange, NJ, USA

    Kathy S. Chiou & Nancy D. Chiaravalloti

  2. Neuropsychology and Neuroscience Research, Kessler Foundation, West Orange, NJ, USA

    Helen M. Genova & Nancy D. Chiaravalloti

  3. Department of Physical Medicine & Rehabilitation, Rutgers—New Jersey Medical School, Newark, NJ, USA

    Kathy S. Chiou, Helen M. Genova & Nancy D. Chiaravalloti

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  1. Kathy S. Chiou
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  2. Helen M. Genova
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  3. Nancy D. Chiaravalloti
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Correspondence to Kathy S. Chiou.

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Disclosures

Drs. Chiou, Genova, and Chiaravalloti declare that they have no conflict of interest. The contents of this manuscript were developed under Grant H133A070037 from the Northern NJ TBI Model Systems and a grant from the National Institute on Disability, Independent Living, and Rehabilitation Research (NIDILRR grant number H133P090009). NIDILRR is a Center within the Administration for Community Living (ACL), Department of Health and Human Services (HHS). The contents of this manuscript do not necessarily represent the policy of NIDILRR, ACL, HHS, and you should not assume endorsement by the Federal Government.

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All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation. Informed consent was obtained from all patients for being included in the study.

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Chiou, K.S., Genova, H.M. & Chiaravalloti, N.D. Structural white matter differences underlying heterogeneous learning abilities after TBI. Brain Imaging and Behavior 10, 1274–1279 (2016). https://doi.org/10.1007/s11682-015-9497-y

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