Loss of white matter connections after severe traumatic brain injury (TBI) and its relationship to social cognition
Adults with severe traumatic brain injury (TBI) often suffer poor social cognition. Social cognition is complex, requiring verbal, non-verbal, auditory, visual and affective input and integration. While damage to focal temporal and frontal areas has been implicated in disorders of social cognition after TBI, the role of white matter pathology has not been examined. In this study 17 adults with chronic, severe TBI and 17 control participants underwent structural MRI scans and Diffusion Tensor Imaging. The Awareness of Social Inference Test (TASIT) was used to assess their ability to understand emotional states, thoughts, intentions and conversational meaning in everyday exchanges. Track-based spatial statistics were used to perform voxelwise analysis of Fractional Anisotropy (FA) and Mean Diffusivity (MD) of white matter tracts associated with poor social cognitive performance. FA suggested a wide range of tracts were implicated in poor TASIT performance including tracts known to mediate, auditory localisation (planum temporale) communication between nonverbal and verbal processes in general (corpus callosum) and in memory in particular (fornix) as well as tracts and structures associated with semantics and verbal recall (left temporal lobe and hippocampus), multimodal processing and integration (thalamus, external capsule, cerebellum) and with social cognition (orbitofrontal cortex, frontopolar cortex, right temporal lobe). Even when controlling for non-social cognition, the corpus callosum, fornix, bilateral thalamus, right external capsule and right temporal lobe remained significant contributors to social cognitive performance. This study highlights the importance of loss of white matter connectivity in producing complex social information processing deficits after TBI.
KeywordsTraumatic brain injury White matter Diffuse axonal injury Social cognition
KD was supported by an ARC Discovery Project 15010026. JR was supported by NHMRC Project Grant 1081923. RLR is supported by the ARC Centre of Excellence in Cognition and its Disorders Memory Node (CE11000102) and by the Appenzeller Neuroscience Fellowship in Alzheimer’s Disease. Additional support was provided from the NHMRC Centre of Research Excellence in Brain Recovery and a former ARC DP 1094083.
Compliance with ethical standard
Conflict of interest
SM receives royalties for The Awareness of Social Inference Test. There are no other conflicts to declare.
All procedures performed were in accordance with the ethical standards of the Human Research Ethics Advisory Panel (HREAP approval reference 103,049) at the University of New South Wales and complied with the 1964 Helsinki declaration and its later amendments.
Informed consent was obtained from all individual participants included in the study.
- Baggio, H. C., Segura, B., Ibarretxe-Bilbao, N., Valldeoriola, F., Marti, M. J., Compta, Y., ... Junqué, C. (2012). Structural correlates of facial emotion recognition deficits in Parkinson's disease patients. Neuropsychologia, 50(8), 2121-2128. doi: https://doi.org/10.1016/j.neuropsychologia.2012.05.020
- Burgess, P. W., & Shallice, T. (1997). The Hayling and Brixton Tests. San Antonio: Pearson PsychCorp Assessment.Google Scholar
- Bzdok, D., Schilbach, L., Vogeley, K., Schneider, K., Laird, A. R., Langner, R., & Eickhoff, S. B. (2012). Parsing the neural correlates of moral cognition: ALE meta-analysis on morality, theory of mind, and empathy. Brain Structure & Function, 217(4), 783–796. https://doi.org/10.1007/s00429-012-0380-y.CrossRefGoogle Scholar
- D'Argembeau, A., Ruby, P., Collette, F., Degueldre, C., Balteau, E., Luxen, A., ..., Salmon, E. (2007). Distinct Regions of the Medial Prefrontal Cortex Are Associated with Self-referential Processing and Perspective Taking. Journal of Cognitive Neuroscience, 19(6), 935-944. doi: https://doi.org/10.1162/jocn.2007.19.6.935
- de Sousa, A., McDonald, S., & Rushby, J. (2012). Changes in emotional empathy, affective responsivity and behaviour following severe traumatic brain injury. Journal of Clinical and Experimental Neuropsychology. https://doi.org/10.1080/13803395.2012.66706
- Downey, L. E., Mahoney, C. J., Buckley, A. H., Golden, H. L., Henley, S. M., Schmitz, N., ..., Warren, J. D. (2015). White matter tract signatures of impaired social cognition in frontotemporal lobar degeneration. Neuroimage: Clinical, 8, 640-651. doi: https://doi.org/10.1016/j.nicl.2015.06.005
- Genova, H. M., Rajagopalan, V., Chiaravalloti, N., Binder, A., Deluca, J., & Lengenfelder, J. (2015). Facial affect recognition linked to damage in specific white matter tracts in traumatic brain injury. Social Neuroscience, 10(1), 27–34. https://doi.org/10.1080/17470919.2014.959618.CrossRefPubMedGoogle 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: A Journal of Neurology, 134(2), 449-463. https://doi.org/10.1093/brain/awq347
- Kraus, J. F., Black, M. A., Hessol, N., Ley, P., Rokaw, W., Sullivan, C., ... Marshall, L. (1984). The incidence of acute brain injury and serious impairment in a defined population. American Journal of Epidemiology, 119, 186-201.Google Scholar
- Leigh, R., Oishi, K., Hsu, J., Lindquist, M., Gottesman, R. F., Jarso, S., ... Hillis, A. E. (2013). Acute lesions that impair affective empathy. Brain: A Journal of Neurology, 136, 2539-2549.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), 558-564. https://doi.org/10.1212/WNL.0b013e3181cff5d5
- Martin-Rodriguez, J. F., & Leon-Carrion, J. (2010). Theory of mind deficits in patients with acquired brain injury: A quantitative review. Neuropsychologia, 48, 1181–1191. https://doi.org/10.1016/j.neuropsychologia.2010.02.009.CrossRefPubMedGoogle Scholar
- McDonald, S., Rushby, J., Dalton, K., Landin-Romero, R., & Parkes, N. (2017). The role of the corpus callosum in social cognition deficits after Traumatic Brain Injury. Social Neuroscience, 1-9. https://doi.org/10.1080/17470919.2017.1356370
- Mike, A., Strammer, E., Aradi, M., Orsi, G., Perlaki, G., Hajnal, A., ..., Illes, Z. (2013). Disconnection mechanism and regional cortical atrophy contribute to impaired processing of facial expressions and theory of mind in multiple sclerosis: a structural MRI study. PLoS One, 8(12), e82422. https://doi.org/10.1371/journal.pone.0082422
- Palacios, E. M., Fernandez-Espejo, D., Junque, C., Sanchez-Carrion, R., Roig, T., Tormos, J. M., ..., Vendrell, P. (2011). Diffusion tensor imaging differences relate to memory deficits in diffuse traumatic brain injury. BMC Neurology, 11, 24. https://doi.org/10.1186/1471-2377-11-24
- Perez, A. M., Adler, J., Kulkarni, N., Strain, J. F., Womack, K. B., Diaz-Arrastia, R., & Marquez de la Plata, C. D. (2014). Longitudinal white matter changes after traumatic axonal injury. Journal of Neurotrauma, 31(17), 1478–1485. https://doi.org/10.1089/neu.2013.3216.CrossRefPubMedPubMedCentralGoogle Scholar
- Reitan, R. M. (1992). Trail Making Test. Tuscon: Reitan Neuropsychological Laboratories.Google Scholar
- Rushby, J. A., McDonald, S., Fisher, A. C., Kornfeld, E. J., De Blasio, F. M., Parks, N., & Piguet, O. (2016). Brain volume contributes to arousal and empathy dysregulation following severe traumatic brain injury. Neuroimage: Clinical, 12, 607–614. https://doi.org/10.1016/j.nicl.2016.09.017.CrossRefGoogle Scholar
- Russell, W., & Smith, A. (1961). Post-traumatic amnesia in closed head injury. Archives of Neurology, 5, 16–29. https://doi.org/10.1001/archneur.1961.00450130006002.CrossRefGoogle Scholar
- Sacchetti, B., Scelfo, B., & Strata, P. (2009). Cerebellum and emotional behavior. Neuroscience, 162(3), 756–762. https://doi.org/10.1016/j.neuroscience.2009.01.064.CrossRefPubMedGoogle Scholar
- Sidaros, A., Engberg, A. W., Sidaros, K., Liptrot, M. G., Herning, M., Petersen, P., et al. (2008). Diffusion tensor imaging during recovery from severe traumatic brain injury and relation to clinical outcome: a longitudinal study. Brain, 131(Pt 2), 559–572. https://doi.org/10.1093/brain/awm294.CrossRefPubMedGoogle 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. Neuroimage, 23, S208-S219. https://doi.org/10.1016/j.neuroimage.2004.07.051
- Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C. E., ..., Behrens, T. E. J (2006). Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage, 31(4), 1487-1505. https://doi.org/10.1016/j.neuroimage.2006.02.024
- Veeramuthu, V., Narayanan, V., Kuo, T. L., Delano-Wood, L., Chinna, K., Bondi, M. W., ..., Ramli, N. (2015). Diffusion Tensor Imaging Parameters in Mild Traumatic Brain Injury and Its Correlation with Early Neuropsychological Impairment: A Longitudinal Study. J Neurotrauma, 32 (19), 1497-1509. https://doi.org/10.1089/neu.2014.3750
- Wechsler, D. (1997). Wechsler Adult Intelligence Scale-Third Edition (WAIS-III). San Antonio: The Psychological Corporation.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. https://doi.org/10.1016/j.neuroimage.2014.01.060