Visual Tracking Synchronization as a Metric for Concussion Screening

Our goal was to determine whether performance variability during predictive visual tracking can provide a screening measure for mild traumatic brain injury (mTBI). Seventeen subjects with chronic postconcussive syndrome and 9 healthy control subjects were included in this study. Eye movements were recorded with video-oculography as the subject visually tracked a target that moved through a circular trajectory. We compared the variability of gaze positional errors relative to the target with the microstructural integrity of white matter tracts as measured by the fractional anisotropy (FA) parameter of diffusion tensor imaging. Gaze error variability was significantly correlated with the mean FA values of the right anterior corona radiata (ACR) and the left superior cerebellar peduncle, tracts that support spatial processing and sustenance of attention, and the genu of the corpus callosum. Because the ACR and the genu are among the most frequently damaged white matter tracts in mTBI, the correlations imply that gaze error variability during visual tracking may provide a useful screening tool for mTBI. Gaze error variability was also significantly correlated with attention and working memory measures in neurocognitive testing; thus, measurement of visual tracking performance is promising as a fast and practical screening tool for mTBI.

[1]  Justin L. Vincent,et al.  Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Ken Nakayama,et al.  Visual and cognitive control of attention in smooth pursuit. , 2002, Progress in brain research.

[3]  Alain Ptito,et al.  Contributions of functional magnetic resonance imaging (fMRI) to sport concussion evaluation. , 2007, NeuroRehabilitation.

[4]  Joan Machamer,et al.  Neuropsychological outcome at 1-year post head injury. , 1995 .

[5]  D Kushner,et al.  Mild traumatic brain injury: toward understanding manifestations and treatment. , 1998, Archives of internal medicine.

[6]  A. Ropper,et al.  Clinical practice. Concussion. , 2007, The New England journal of medicine.

[7]  Jeremy D. Schmahmann,et al.  Functional topography in the human cerebellum: A meta-analysis of neuroimaging studies , 2009, NeuroImage.

[8]  K. Lim,et al.  Diffusion Tensor Imaging in Psychiatric Disorders , 2008, Topics in magnetic resonance imaging : TMRI.

[9]  Y. Assaf,et al.  Diffusion Tensor Imaging (DTI)-based White Matter Mapping in Brain Research: A Review , 2007, Journal of Molecular Neuroscience.

[10]  Donald T. Stuss,et al.  Frontal dysfunction' after traumatic brain injury , 1992 .

[11]  W. Peh,et al.  Diffuse axonal injury: detection of changes in anisotropy of water diffusion by diffusion-weighted imaging , 2002, Neuroradiology.

[12]  Pratik Mukherjee,et al.  Structural dissociation of attentional control and memory in adults with and without mild traumatic brain injury. , 2008, Brain : a journal of neurology.

[13]  Thomas Ptak,et al.  Cerebral fractional anisotropy score in trauma patients: a new indicator of white matter injury after trauma. , 2003, AJR. American journal of roentgenology.

[14]  A. Gean,et al.  Neuroimaging of traumatic brain injury. , 2009, The Mount Sinai journal of medicine, New York.

[15]  Erin D Bigler,et al.  Neuropsychology and clinical neuroscience of persistent post-concussive syndrome , 2007, Journal of the International Neuropsychological Society.

[16]  Craig A Branch,et al.  Diffusion-tensor imaging implicates prefrontal axonal injury in executive function impairment following very mild traumatic brain injury. , 2009, Radiology.

[17]  D R Rutgers,et al.  White Matter Abnormalities in Mild Traumatic Brain Injury: A Diffusion Tensor Imaging Study , 2008, American Journal of Neuroradiology.

[18]  J. Adams,et al.  Diffuse axonal injury in head injury: Definition, diagnosis and grading , 1989, Histopathology.

[19]  E. Courchesne,et al.  Attentional Activation of the Cerebellum Independent of Motor Involvement , 1997, Science.

[20]  B. Thompson,et al.  MR imaging of head trauma: review of the distribution and radiopathologic features of traumatic lesions. , 1988, AJR. American journal of roentgenology.

[21]  M. Mesulam.  Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[22]  Michael H. Buonocore,et al.  Cognitive Control and White Matter Callosal Microstructure in Methamphetamine-Dependent Subjects: A Diffusion Tensor Imaging Study , 2009, Biological Psychiatry.

[23]  Richard B Ivry,et al.  The Predictive Brain State: Asynchrony in Disorders of Attention? , 2009, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[24]  Leslie G. Ungerleider,et al.  Fiber pathways of cortical areas mediating smooth pursuit eye movements in monkeys , 1988, Annals of neurology.

[25]  Guy Madison,et al.  Intelligence and Variability in a Simple Timing Task Share Neural Substrates in the Prefrontal White Matter , 2008, The Journal of Neuroscience.

[26]  R. Engle,et al.  The nature of individual differences in working memory capacity: active maintenance in primary memory and controlled search from secondary memory. , 2007, Psychological review.

[27]  Edward E. Smith,et al.  Spatial working memory in humans as revealed by PET , 1993, Nature.

[28]  N. Nakayama,et al.  Evidence for white matter disruption in traumatic brain injury without macroscopic lesions , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[29]  M. Alexander.  Mild traumatic brain injury , 1995, Neurology.

[30]  M. Posner,et al.  The attention system of the human brain. , 1990, Annual review of neuroscience.

[31]  P. Basser,et al.  Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. , 1996, Journal of magnetic resonance. Series B.

[32]  I. Robertson,et al.  `Oops!': Performance correlates of everyday attentional failures in traumatic brain injured and normal subjects , 1997, Neuropsychologia.

[33]  D. V. von Cramon,et al.  Cognitive sequelae of diffuse axonal injury. , 2006, Archives of neurology.

[34]  D. Stuss,et al.  Reaction time after head injury: fatigue, divided and focused attention, and consistency of performance. , 1989, Journal of neurology, neurosurgery, and psychiatry.

[35]  P. Strick,et al.  Cerebellar Loops with Motor Cortex and Prefrontal Cortex of a Nonhuman Primate , 2003, The Journal of Neuroscience.

[36]  D. Lykken,et al.  Electro-oculographic recording and scoring of smooth pursuit and saccadic eye tracking: a parametric study using monozygotic twins. , 1979, Psychophysiology.

[37]  Craig A Branch,et al.  Multifocal white matter ultrastructural abnormalities in mild traumatic brain injury with cognitive disability: a voxel-wise analysis of diffusion tensor imaging. , 2008, Journal of neurotrauma.

[38]  V. Haughton,et al.  Diffusion tensor MR imaging in diffuse axonal injury. , 2002, AJNR. American journal of neuroradiology.

[39]  A. Ebert,et al.  Neuropsychological sequelae of diffuse traumatic brain injury , 2005, Brain injury.

[40]  T A Gennarelli,et al.  Prevalence of MR evidence of diffuse axonal injury in patients with mild head injury and normal head CT findings. , 1994, AJNR. American journal of neuroradiology.

[41]  H S Markus,et al.  Characterization of white matter damage in ischemic leukoaraiosis with diffusion tensor MRI. , 1999, Stroke.

[42]  A. Sorensen,et al.  Diffusion tensor imaging as potential biomarker of white matter injury in diffuse axonal injury. , 2004, AJNR. American journal of neuroradiology.

[43]  J. Donders,et al.  Criterion validity of the California Verbal Learning Test-Second Edition (CVLT-II) after traumatic brain injury. , 2007, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[44]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[45]  D. Meaney,et al.  Diffuse Axonal Injury in Head Trauma , 2003, The Journal of head trauma rehabilitation.

[46]  H. Collewijn,et al.  A comparison of oculomotor pursuit of a target in circular real, beta or sigma motion , 1983, Vision Research.

[47]  J. Sweeney,et al.  White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. , 2007, Brain : a journal of neurology.

[48]  S. Lebedev,et al.  Saccades in pursuit eye tracking reflect motor attention processes. , 1990, Comprehensive psychiatry.

[49]  Bruce D. McCandliss,et al.  Extent of Microstructural White Matter Injury in Postconcussive Syndrome Correlates with Impaired Cognitive Reaction Time: A 3T Diffusion Tensor Imaging Study of Mild Traumatic Brain Injury , 2008, American Journal of Neuroradiology.

[50]  Peter Boesiger,et al.  Attention and Interhemispheric Transfer: A Behavioral and fMRI Study , 2005, Journal of Cognitive Neuroscience.

[51]  R. Krauzlis.  The Control of Voluntary Eye Movements: New Perspectives , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[52]  P V Bayly,et al.  Deformation of the human brain induced by mild acceleration. , 2005, Journal of neurotrauma.

[53]  Harald Schrader,et al.  Magnetic resonance imaging after most common form of concussion , 2009, BMC Medical Imaging.

[54]  G. Barnes,et al.  Cognitive processes involved in smooth pursuit eye movements , 2008, Brain and Cognition.

[55]  H. Levin,et al.  Cognitive Outcome Following Traumatic Brain Injury , 2009, The Journal of head trauma rehabilitation.

[56]  Richard D. Jones,et al.  Impaired eye movements in post-concussion syndrome indicate suboptimal brain function beyond the influence of depression, malingering or intellectual ability. , 2009, Brain : a journal of neurology.

[57]  Bruce D. McCandliss,et al.  Testing the Efficiency and Independence of Attentional Networks , 2002, Journal of Cognitive Neuroscience.

[58]  Andrew J. Saykin,et al.  Differential Working Memory Load Effects after Mild Traumatic Brain Injury , 2001, NeuroImage.

[59]  Jean-Jacques Orban de Xivry,et al.  Saccades and pursuit: two outcomes of a single sensorimotor process , 2007, The Journal of physiology.

[60]  D. Pandya,et al.  Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns , 1999, The European journal of neuroscience.

[61]  T A Gennarelli,et al.  Diffuse axonal injury in non-missile head injury. , 1991, Journal of neurology, neurosurgery, and psychiatry.

[62]  A. Holbourn.  MECHANICS OF HEAD INJURIES , 1943 .

[63]  D. Pandya,et al.  Topography of commissural fibers of the prefrontal cortex in the rhesus monkey , 2004, Experimental Brain Research.

[64]  E. J. Morris,et al.  Visual motion processing and sensory-motor integration for smooth pursuit eye movements. , 1987, Annual review of neuroscience.

[65]  N. Nevin.  NEUROPATHOLOGICAL CHANGES IN THE WHITE MATTER FOLLOWING HEAD INJURY , 1967, Journal of neuropathology and experimental neurology.

[66]  T Mäkelä,et al.  [Mechanics of head injuries]. , 1965, Suomen laakarilehti. Finlands lakartidning.

[67]  Hangyi Jiang,et al.  DtiStudio: Resource program for diffusion tensor computation and fiber bundle tracking , 2006, Comput. Methods Programs Biomed..

[68]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[69]  G J Barker,et al.  Diffusion imaging shows abnormalities after blunt head trauma when conventional magnetic resonance imaging is normal , 2001, Journal of neurology, neurosurgery, and psychiatry.

[70]  A. D. de Crespigny,et al.  Compromised white matter tract integrity in schizophrenia inferred from diffusion tensor imaging. , 1999, Archives of general psychiatry.

[71]  K. Lim,et al.  Age‐related decline in brain white matter anisotropy measured with spatially corrected echo‐planar diffusion tensor imaging , 2000, Magnetic resonance in medicine.

[72]  M. Raichle,et al.  Localization of a human system for sustained attention by positron emission tomography , 1991, Nature.

[73]  L. Binder,et al.  A review of mild head trauma. Part II: Clinical implications. , 1997, Journal of clinical and experimental neuropsychology.

[74]  P. Sachdev,et al.  Diffusion tensor imaging in mild cognitive impairment and Alzheimer's disease: a review , 2008, Current opinion in neurology.