Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-26T00:09:02.079Z Has data issue: false hasContentIssue false
  • English
  • Français

Frontal and Temporal Structural Connectivity Is Associated with Social Communication Impairment Following Traumatic Brain Injury

Published online by Cambridge University Press:  13 July 2016

Arianna Rigon ,
Michelle W. Voss ,
Lyn S. Turkstra ,
Bilge Mutlu  and
Melissa C. Duff
Arianna Rigon*
Affiliation:
Interdisciplinary Neuroscience Program, The University of Iowa, Iowa City, Iowa
Michelle W. Voss
Affiliation:
Interdisciplinary Neuroscience Program, The University of Iowa, Iowa City, Iowa Department of Psychological & Brain Sciences, The University of Iowa, Iowa City, Iowa
Lyn S. Turkstra
Affiliation:
Department of Communication Sciences and Disorders, The University of Wisconsin – Madison, Wisconsin Interdisciplinary Program in Neuroscience, The University of Wisconsin – Madison, Wisconsin
Bilge Mutlu
Affiliation:
Department of Computer Sciences, The University of Wisconsin – Madison, Wisconsin
Melissa C. Duff
Affiliation:
Interdisciplinary Neuroscience Program, The University of Iowa, Iowa City, Iowa Department of Communication Sciences and Disorders, The University of Iowa, Iowa City, Iowa Department of Neurology, The University of Iowa, Iowa City, Iowa
*
Correspondence and reprint requests to: Arianna Rigon, 420-I Seashore Hall, 328 Iowa Ave, Iowa City, IA 52242. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Objectives: Although it has been well documented that traumatic brain injury (TBI) can result in communication impairment, little work to date has examined the relationship between social communication skills and structural brain integrity in patients with TBI. The aim of the current study was to investigate the association between self- and other-perceived communication problems and white matter integrity in patients with mild to severe TBI. Methods: Forty-four individuals (TBI=24) and people with whom they frequently communicate, as well as demographically matched normal healthy comparisons (NC) and their frequent communication partners, were administered, respectively, the La-Trobe Communication Questionnaire Self form (LCQ-SELF) and Other form (LCQ-OTHER). In addition, diffusion tensor imaging data were collected, and fractional anisotropy (FA) measures were extracted for each lobe in both hemispheres. Results: Within the TBI group, but not within the NC group, participants who were perceived by their close others as having more communication problems had lower FA in the left frontal and temporal lobes (p<.01), but not in other brain regions. Conclusions: Frontotemporal white matter microstructural integrity is associated with social communication abilities in adults with TBI. This finding contributes to our understanding of the mechanisms leading to communication impairment following TBI and can inform the development of new neuromodulation therapies as well as diagnostic tools. (JINS, 2016, 22, 705–716)

Keywords

White matterCommunicationDiffusion tensor imagingFractional anisotropyFrontal lobeTemporal lobe
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 22 , Issue 7 , August 2016 , pp. 705 - 716
Copyright
Copyright © The International Neuropsychological Society 2016 

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

Adams, J.H., Doyle, D., Graham, D.I., Lawrence, A.E., & McLellan, D.R. (1984). Diffuse axonal injury in head injuries caused by a fall. Lancet, 2(8417-8418), 1420–1422.CrossRefGoogle ScholarPubMed
Adams, J.H., Graham, D.I., & Jennett, B. (2001). The structural basis of moderate disability after traumatic brain damage. Journal of Neurology, Neurosurgery, and Psychiatry, 71(4), 521–524.Google Scholar
Adolphs, R. (2003). Cognitive neuroscience of human social behaviour. Nature Reviews. Neuroscience, 4(3), 165–178.CrossRefGoogle ScholarPubMed
Ahles, T.A., Saykin, A.J., Noll, W.W., Furstenberg, C.T., Guerin, S., Cole, B., && Mott, L.A. (2003). The relationship of APOE genotype to neuropsychological performance in long-term cancer survivors treated with standard dose chemotherapy. Psychooncology, 12(6), 612–619.CrossRefGoogle ScholarPubMed
Andersson, J.L.R., Jenkinson, M., & Smith, S. (2007a). Non-linear optimisation. FMRIB technical report TR07JA1. Retrieved from http://www.fmrib.ox.ac.uk/analysis/techrep Google Scholar
Andersson, J.L.R., Jenkinson, M., & Smith, S. (2007b). Non-linear registration, aka Spatial normalisation FMRIB technical report TR07JA2. Retrieved from http://www.fmrib.ox.ac.uk/analysis/techrep Google Scholar
Aron, A., Aron, E.N., & Smollan, D. (1992). Inclusion of other in the self scale and the structure of interpersonal closeness. Journal of Personality and Social Psychology, 63(4), 596–612.Google Scholar
Basser, P.J. (1995). Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR in Biomedicine, 8(7-8), 333–344.Google Scholar
Beauchamp, M.S. (2015). The social mysteries of the superior temporal sulcus. Trends in Cognitive Sciences, 19(9), 489–490.Google Scholar
Beaulieu, C. (2002). The basis of anisotropic water diffusion in the nervous system - A technical review. NMR in Biomedicine, 15(7–8), 435–455.Google Scholar
Bechara, A., Tranel, D., & Damasio, H. (2000). Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. Brain, 123(Pt 11), 2189–2202.Google Scholar
Behrens, T.E., Woolrich, M.W., Jenkinson, M., Johansen-Berg, H., Nunes, R.G., Clare, S., & Smith, S.M. (2003). Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magnetic Resonance in Medicine, 50(5), 1077–1088.Google Scholar
Bernicot, J., & Dardier, V. (2001). Communication deficits: Assessment of subjects with frontal lobe damage in an interview setting. International Journal of Language & Communication Disorders/Royal College of Speech & Language Therapists, 36(2), 245–263.Google Scholar
Bond, F., & Godfrey, H.P. (1997). Conversation with traumatically brain-injured individuals: A controlled study of behavioural changes and their impact. Brain Injury, 11(5), 319–329.Google Scholar
Bornhofen, C., & McDonald, S. (2008). Emotion perception deficits following traumatic brain injury: A review of the evidence and rationale for intervention. Journal of the International Neuropsychological Society, 14(4), 511–525.Google Scholar
Bosco, F.M., Angeleri, R., Sacco, K., & Bara, B.G. (2015). Explaining pragmatic performance in traumatic brain injury: A process perspective on communicative errors. International Journal of Language & Communication Disorders/Royal College of Speech & Language Therapists, 50(1), 63–83.CrossRefGoogle ScholarPubMed
Champagne-Lavau, M., Stip, E., & Joanette, Y. (2007). Language functions in right-hemisphere damage and schizophrenia: Apparently similar pragmatic deficits may hide profound differences. Brain, 130(Pt 2), e67. author reply e68.Google Scholar
Ciaramelli, E., Braghittoni, D., & di Pellegrino, G. (2012). It is the outcome that counts! Damage to the ventromedial prefrontal cortex disrupts the integration of outcome and belief information for moral judgment. Journal of the International Neuropsychological Society, 18(6), 962–971.Google Scholar
Coelho, C.A., DeRuyter, F., & Stein, M. (1996). Treatment efficacy: Cognitive-communicative disorders resulting from traumatic brain injury in adults. Journal of Speech and Hearing Research, 39(5), S5–S17.Google Scholar
Coelho, C.A., Liles, B.Z., & Duffy, R.J. (1995). Impairments of discourse abilities and executive functions in traumatically brain-injured adults. Brain Injury, 9(5), 471–477.Google Scholar
Costa, P.J. (2014). Truncated outlier filtering. Journal of Biopharmaceutical Statistics, 24(5), 1115–1129.Google Scholar
Crewe-Brown, S.J., Stipinovich, A.M., & Zsilavecz, U. (2011). Communication after mild traumatic brain injury--A spouse’s perspective. The South African Journal of Communication Disorders=Die Suid-Afrikaanse tydskrif vir Kommunikasieafwykings, 58, 48–55.Google ScholarPubMed
Cubon, V.A., Putukian, M., Boyer, C., & Dettwiler, A. (2011). A diffusion tensor imaging study on the white matter skeleton in individuals with sports-related concussion. Journal of Neurotrauma, 28(2), 189–201.Google Scholar
Cummings, L. (2007). Pragmatics and adult language disorders: Past achievements and future directions. Seminars in Speech and Language, 28(2), 96–110.Google Scholar
Dardier, V., Bernicot, J., Delanoe, A., Vanberten, M., Fayada, C., Chevignard, M., & Dubois, B. (2011). Severe traumatic brain injury, frontal lesions, and social aspects of language use: A study of French-speaking adults. Journal of Communication Disorders, 44(3), 359–378.Google Scholar
Delis, D.C., Freeland, J., Kramer, J.H., & Kaplan, E. (1988). Integrating clinical assessment with cognitive neuroscience: Construct validation of the California Verbal Learning Test. Journal of Consulting and Clinical Psychology, 56(1), 123–130.CrossRefGoogle ScholarPubMed
Despins, E.H., Turkstra, L.S., Struchen, M.A., & Clark, A.N. (2016). Sex-based differences in perceived pragmatic communication ability of adults with traumatic brain injury. Archives of Physical Medicine and Rehabilitation, 97(Suppl.), S26–S32.CrossRefGoogle ScholarPubMed
Docking, K., Murdoch, B.E., & Jordan, F.M. (2000). Interpretation and comprehension of linguistic humour by adolescents with head injury: A group analysis. Brain Injury, 14(1), 89–108.Google Scholar
Douglas, J.M. (2010). Relation of executive functioning to pragmatic outcome following severe traumatic brain injury. Journal of Speech, Language, and Hearing Research, 53(2), 365–382.Google Scholar
Douglas, J.M., Bracy, C.A., & Snow, P.C. (2007). Measuring perceived communicative ability after traumatic brain injury: Reliability and validity of the La Trobe Communication Questionnaire. The Journal of Head Trauma Rehabilitation, 22(1), 31–38.Google Scholar
Duff, M.C., & Brown-Schmidt, S. (2012). The hippocampus and the flexible use and processing of language. Frontiers in Human Neuroscience, 6, 69.CrossRefGoogle ScholarPubMed
Duncan, J., & Owen, A.M. (2000). Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends in Neurosciences, 23(10), 475–483.Google Scholar
Edwards-Lee, T., Miller, B.L., Benson, D.F., Cummings, J.L., Russell, G.L., Boone, K., && Mena, I. (1997). The temporal variant of frontotemporal dementia. Brain, 120(Pt 6), 1027–1040.Google Scholar
Engberg, A.W., & Teasdale, T.W. (2004). Psychosocial outcome following traumatic brain injury in adults: A long-term population-based follow-up. Brain injury, 18(6), 533–545.Google Scholar
Fontaine, A., Azouvi, P., Remy, P., Bussel, B., & Samson, Y. (1999). Functional anatomy of neuropsychological deficits after severe traumatic brain injury. Neurology, 53(9), 1963–1968.Google Scholar
Gaetz, M. (2004). The neurophysiology of brain injury. Clinical Neurophysiology, 115(1), 4–18.Google Scholar
Garcia-Molina, A., Ensenat-Cantallops, A., Sanchez-Carrion, R., Rodriguez, P., Tormos, J.M., & Roig-Rovira, T. (2013). [Interindividual variability in recovery after traumatic brain injury: Effect of cognitive reserve]. Medicina Clinica, 140(12), 527–531.Google Scholar
Gordon, R.G., Rigon, A., & Duff, M.C. (2015). Conversational synchrony in the communicative interactions of individuals with traumatic brain injury. Brain Injury, 29(11), 1300–1308.CrossRefGoogle ScholarPubMed
Gordon, N.G. (1972). The Trail Making Test in neuropsychological diagnosis. Journal of Clinical Psychology, 28(2), 167–169.3.0.CO;2-X>CrossRefGoogle ScholarPubMed
Gordon, R.G., Tranel, D., & Duff, M.C. (2014). The physiological basis of synchronizing conversational rhythms: The role of the ventromedial prefrontal cortex. Neuropsychology, 28(4), 624–630.Google Scholar
Hayes, J.P., Bigler, E.D., & Verfaellie, M. (2016). Traumatic Brain Injury as a Disorder of Brain Connectivity. Journal of the International Neuropsychological Society, 22(2), 120–137.Google Scholar
Head, D., Buckner, R.L., Shimony, J.S., Williams, L.E., Akbudak, E., Conturo, T.E., & Snyder, A.Z. (2004). Differential vulnerability of anterior white matter in nondemented aging with minimal acceleration in dementia of the Alzheimer type: Evidence from diffusion tensor imaging. Cerebral Cortex, 14(4), 410–423.Google Scholar
Holdnack, J.A., Xiaobin, Z., Larrabee, G.J., Millis, S.R., & Salthouse, T.A. (2011). Confirmatory factor analysis of the WAIS-IV/WMS-IV. Assessment, 18(2), 178–191.Google Scholar
Hornak, J., Rolls, E.T., & Wade, D. (1996). Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage. Neuropsychologia, 34(4), 247–261.Google Scholar
Hua, K., Zhang, J., Wakana, S., Jiang, H., Li, X., Reich, D.S., & Mori, S. (2008). Tract probability maps in stereotaxic spaces: Analyses of white matter anatomy and tract-specific quantification. Neuroimage, 39(1), 336–347.Google Scholar
Hulkower, M.B., Poliak, D.B., Rosenbaum, S.B., Zimmerman, M.E., & Lipton, M.L. (2013). A decade of DTI in traumatic brain injury: 10 years and 100 articles later. AJNR. American Journal of Neuroradiology, 34(11), 2064–2074.Google Scholar
Johnstone, B., Callahan, C.D., Kapila, C.J., & Bouman, D.E. (1996). The comparability of the WRAT-R reading test and NAART as estimates of premorbid intelligence in neurologically impaired patients. Archives of Clinical Neuropsychology, 11(6), 513–519.Google Scholar
Kennedy, M.R., Wozniak, J.R., Muetzel, R.L., Mueller, B.A., Chiou, H.H., Pantekoek, K., && Lim, K.O. (2009). White matter and neurocognitive changes in adults with chronic traumatic brain injury. Journal of the International Neuropsychological Society, 15(1), 130–136.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), 449–463.Google Scholar
Knox, L., & Douglas, J. (2009). Long-term ability to interpret facial expression after traumatic brain injury and its relation to social integration. Brain and Cognition, 69(2), 442–449.CrossRefGoogle ScholarPubMed
Koenigs, M., & Tranel, D. (2007). Irrational economic decision-making after ventromedial prefrontal damage: Evidence from the Ultimatum Game. The Journal of Neuroscience, 27(4), 951–956.Google Scholar
Koenigs, M., Young, L., Adolphs, R., Tranel, D., Cushman, F., Hauser, M., && Damasio, A. (2007). Damage to the prefrontal cortex increases utilitarian moral judgements. Nature, 446(7138), 908–911.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), 2508–2519.Google Scholar
Kumar, R., Husain, M., Gupta, R.K., Hasan, K.M., Haris, M., Agarwal, A.K., & Narayana, P.A. (2009). Serial changes in the white matter diffusion tensor imaging metrics in moderate traumatic brain injury and correlation with neuro-cognitive function. Journal of Neurotrauma, 26(4), 481–495.Google Scholar
Levin, H.S. (1992). Head injury and its rehabilitation. Current Opinion in Neurology and Neurosurgery, 5(5), 673–676.Google Scholar
Malec, J.F., Brown, A.W., Leibson, C.L., Flaada, J.T., Mandrekar, J.N., Diehl, N.N., &&Perkins, P.K. (2007). The mayo classification system for traumatic brain injury severity. Journal of Neurotrauma, 24(9), 1417–1424.Google Scholar
McDonald, S., & Pearce, S. (1998). Requests that overcome listener reluctance: Impairment associated with executive dysfunction in brain injury. Brain and Language, 61(1), 88–104.Google Scholar
McDonald, S., Tate, R., Togher, L., Bornhofen, C., Long, E., Gertler, P., && Bowen, R. (2008). Social skills treatment for people with severe, chronic acquired brain injuries: A multicenter trial. Archives of Physical Medicine and Rehabilitation, 89(9), 1648–1659.Google Scholar
Pagulayan, K.F., Temkin, N.R., Machamer, J., & Dikmen, S.S. (2006). A longitudinal study of health-related quality of life after traumatic brain injury. Archives of Physical Medicine and Rehabilitation, 87(5), 611–618.CrossRefGoogle ScholarPubMed
Pettersen, L. (1991). Sensitivity to emotional cues and social behavior in children and adolescents after head injury. Perceptual and Motor Skills, 73(3 Pt 2), 1139–1150.Google Scholar
Roozenbeek, B., Maas, A.I., & Menon, D.K. (2013). Changing patterns in the epidemiology of traumatic brain injury. Nature Reviews. Neurology, 9(4), 231–236.Google Scholar
Rosenberg, H., McDonald, S., Dethier, M., Kessels, R.P., & Westbrook, R.F. (2014). Facial emotion recognition deficits following moderate-severe Traumatic Brain Injury (TBI): Re-examining the valence effect and the role of emotion intensity. Journal of the International Neuropsychological Society, 20(10), 994–1003.Google Scholar
Rousseaux, M., Verigneaux, C., & Kozlowski, O. (2010). An analysis of communication in conversation after severe traumatic brain injury. European Journal of Neurology, 17(7), 922–929.Google Scholar
Ryan, N.P., Catroppa, C., Beare, R., Coleman, L., Ditchfield, M., Crossley, L., & Anderson, V.A. (2015). Predictors of longitudinal outcome and recovery of pragmatic language and its relation to externalizing behaviour after pediatric traumatic brain injury. Brain and Language, 142, 86–95.Google Scholar
Saxe, R. (2006). Uniquely human social cognition. Current Opinion in Neurobiology, 16(2), 235–239.CrossRefGoogle ScholarPubMed
Sen, P.N., & Basser, P.J. (2005). A model for diffusion in white matter in the brain. Biophysical Journal, 89(5), 2927–2938.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), 2233–2247.Google Scholar
Sharp, D.J., Scott, G., & Leech, R. (2014). Network dysfunction after traumatic brain injury. Nature Reviews. Neurology, 10(3), 156–166.CrossRefGoogle ScholarPubMed
Shewan, C.M., & Kertesz, A. (1980). Reliability and validity characteristics of the Western Aphasia Battery (WAB). The Journal of Speech and Hearing Disorders, 45(3), 308–324.Google Scholar
Smith, S.M. (2002). Fast robust automated brain extraction. Human brain mapping, 17(3), 143–155.Google Scholar
Smith, S.M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T.E., Mackay, C.E., & Behrens, T.E. (2006). Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. Neuroimage, 31(4), 1487–1505.Google Scholar
Smith, S.M., Jenkinson, M., Woolrich, M.W., Beckmann, C.F., Behrens, T.E., Johansen-Berg, H., & Matthews, P.M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage, 23(Suppl. 1), S208–S219.Google Scholar
Snow, P., Douglas, J., & Ponsford, J. (1998). Conversational discourse abilities following severe traumatic brain injury: A follow-up study. Brain Injury, 12(11), 911–935.Google Scholar
Stolk, A., D’Imperio, D., di Pellegrino, G., & Toni, I. (2015). Altered communicative decisions following ventromedial prefrontal lesions. Current Biology, 25(11), 1469–1474.Google Scholar
Struchen, M.A., Clark, A.N., Sander, A.M., Mills, M.R., Evans, G., & Kurtz, D. (2008). Relation of executive functioning and social communication measures to functional outcomes following traumatic brain injury. Neurorehabilitation, 23(2), 185–198.Google Scholar
Struchen, M.A., Pappadis, M.R., Mazzei, D.K., Clark, A.N., Davis, L.C., & Sander, A.M. (2008). Perceptions of communication abilities for persons with traumatic brain injury: Validity of the La Trobe Communication Questionnaire. Brain Injury, 22(12), 940–951.Google Scholar
Tompkins, C.A., Lehman, M.T., Wyatt, A.D., & Schulz, R. (1998). Functional outcome assessment of adults with right hemisphere brain damage. Seminars in Speech and Language, 19(3), 303–321.Google Scholar
Vigneau, M., Beaucousin, V., Herve, P.Y., Duffau, H., Crivello, F., Houde, O., & Tzourio-Mazoyer, N. (2006). Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing. Neuroimage, 30(4), 1414–1432.Google Scholar
Voss, M.W., Heo, S., Prakash, R.S., Erickson, K.I., Alves, H., Chaddock, L., & Kramer, A.F. (2013). The influence of aerobic fitness on cerebral white matter integrity and cognitive function in older adults: Results of a one-year exercise intervention. Human Brain Mapping, 34(11), 2972–2985.Google Scholar
Wakana, S., Caprihan, A., Panzenboeck, M.M., Fallon, J.H., Perry, M., Gollub, R.L., & Mori, S. (2007). Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage, 36(3), 630–644.Google Scholar
Werring, D.J., Clark, C.A., Barker, G.J., Thompson, A.J., & Miller, D.H. (1999). Diffusion tensor imaging of lesions and normal-appearing white matter in multiple sclerosis. Neurology, 52(8), 1626–1632.Google Scholar
Whelan, B.M., Murdoch, B.E., & Bellamy, N. (2007). Delineating communication impairments associated with mild traumatic brain injury: A case report. The Journal of Head Trauma Rehabilitation, 22(3), 192–197.CrossRefGoogle ScholarPubMed
Wilkinson, G.S., & Robertson, G.J. (2006). Wide Range Achievement Test 4 professional manual. Lutz, FL: Psychological Assessment Resources.Google Scholar
Winkler, A.M., Ridgway, G.R., Webster, M.A., Smith, S.M., & Nichols, T.E. (2014). Permutation inference for the general linear model. Neuroimage, 92, 381–397.Google Scholar
Zappala, G., Thiebaut de Schotten, M., & Eslinger, P.J. (2012). Traumatic brain injury and the frontal lobes: What can we gain with diffusion tensor imaging? Cortex, 48(2), 156–165.Google Scholar
Supplementary material: File

Rigon supplementary material S1

Rigon supplementary material

Download Rigon supplementary material S1(File)
File 128.5 KB
Supplementary material: File

Rigon supplementary material S2

Rigon supplementary material

Download Rigon supplementary material S2(File)
File 83.6 KB