Perfusion Imaging of the Right Perisylvian Neural Network in Acute Spatial Neglect

Recent studies have suggested a tightly connected perisylvian neural network associated with spatial neglect. Here we investigated whether structural damage in one part of the network typically is accompanied with functional damage in other, structurally intact areas of this network. By combining normalized fluid-attenuated inversion-recovery (FLAIR) imaging, diffusion-weighted imaging (DWI), and perfusion-weighted imaging (PWI) we asked whether or not lesions centering on fronto-temporal regions co-occur with abnormal perfusion in structurally intact parietal cortex. With thresholds applied to delineate behaviourally relevant malperfusion of brain tissue, the analysis of normalized time-to-peak (TTP) and maximal signal reduction (MSR) perfusion maps did not reveal significant changes outside the area of structural damage. In particular, we found no abnormal perfusion in the structurally intact inferior parietal lobule (IPL) and/or the temporo-parietal junction (TPJ). The present results obtained in three consecutively admitted neglect patients with fronto-temporal lesions indicate that structural damage in one part of the right perisylvian network associated with spatial neglect does not necessarily require dysfunction by malperfusion in other, structurally intact parts of the network to provoke spatial neglect. The neural tissue in the fronto-temporal cortex appears to have an original role in processes of spatial orienting and exploration.

[1]  S M Davis,et al.  Prediction of stroke outcome with echoplanar perfusion- and diffusion-weighted MRI , 1998, Neurology.

[2]  Peter B Barker,et al.  Anatomy of Spatial Attention: Insights from Perfusion Imaging and Hemispatial Neglect in Acute Stroke , 2005, The Journal of Neuroscience.

[3]  S. E. Black,et al.  Impaired visual search in patients with unilateral neglect: an oculographic analysis , 1997, Neuropsychologia.

[4]  A E Hillis,et al.  Subcortical aphasia and neglect in acute stroke: the role of cortical hypoperfusion. , 2002, Brain : a journal of neurology.

[5]  Rudolf Graf,et al.  The ischemic penumbra , 1994, Current opinion in neurology.

[6]  A Gregory Sorensen,et al.  Predicting cerebral ischemic infarct volume with diffusion and perfusion MR imaging. , 2002, AJNR. American journal of neuroradiology.

[7]  H. Karnath,et al.  The subcortical anatomy of human spatial neglect: putamen, caudate nucleus and pulvinar. , 2002, Brain : a journal of neurology.

[8]  S. Black,et al.  The Sunnybrook Stroke Study: a prospective study of depressive symptoms and functional outcome. , 1998, Stroke.

[9]  P M Rossini,et al.  Does cerebrovascular disease affect the coupling between neuronal activity and local haemodynamics? , 2004, Brain : a journal of neurology.

[10]  Hans Samuelsson,et al.  Anatomical and Neurological Correlates of Acute and Chronic Visuospatial Neglect Following Right Hemisphere Stroke * * Some of the results of this study were presented at: The 5th Nordic Meeting in Neuropsychology, Uppsala, Sweden, August 17-19, 1995. , 1997, Cortex.

[11]  C. Beaulieu,et al.  Longitudinal magnetic resonance imaging study of perfusion and diffusion in stroke: Evolution of lesion volume and correlation with clinical outcome , 1999, Annals of neurology.

[12]  P. Barker,et al.  Patients with Diffusion‐Perfusion Mismatch on Magnetic Resonance Imaging 48 Hours or More After Stroke Symptom Onset: Clinical and Imaging Features , 2006, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[13]  M. Corbetta,et al.  Neural basis and recovery of spatial attention deficits in spatial neglect , 2005, Nature Neuroscience.

[14]  S. Ferber,et al.  Spatial awareness is a function of the temporal not the posterior parietal lobe , 2001, Nature.

[15]  S. Black,et al.  Brain-behavior correlations in hemispatial neglect using CT and SPECT , 1998, Neurology.

[16]  J. Hopper,et al.  Crossed cerebellar diaschisis and brain recovery after stroke. , 1995, Stroke.

[17]  Fu-Nien Wang,et al.  A Reinvestigation of Maximal Signal Drop in Dynamic Susceptibility Contrast Magnetic Resonance Imaging , 2002, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[18]  M. Mesulam A cortical network for directed attention and unilateral neglect , 1981, Annals of neurology.

[19]  Leif Johannsen,et al.  How Efficient is a Simple Copying Task to Diagnose Spatial Neglect in its Chronic Phase? , 2004, Journal of clinical and experimental neuropsychology.

[20]  Leif Østergaard,et al.  Magnetic Resonance Perfusion-Weighted Imaging of Acute Cerebral Infarction: Effect of the Calculation Methods and Underlying Vasculopathy , 2002, Stroke.

[21]  D Atkinson,et al.  Fluid-attenuated inversion recovery (FLAIR) for assessment of cerebral infarction. Initial clinical experience in 50 patients. , 1996, Stroke.

[22]  S. Weintraub,et al.  Mental state assessment of young and elderly adults in behavioral neurology , 1985 .

[23]  Michael Erb,et al.  Exploring the visual world: The neural substrate of spatial orienting , 2006, NeuroImage.

[24]  L. Gauthier,et al.  The Bells Test: A quantitative and qualitative test for visual neglect. , 1989 .

[25]  B. Siesjö,et al.  Thresholds in cerebral ischemia - the ischemic penumbra. , 1981, Stroke.

[26]  G. Schlaug,et al.  The ischemic penumbra: operationally defined by diffusion and perfusion MRI. , 1999, Neurology.

[27]  김세영 Diffusion and Perfusion weighted MRI , 2010 .

[28]  Chris Rorden,et al.  The anatomy of spatial neglect based on voxelwise statistical analysis: a study of 140 patients. , 2004, Cerebral cortex.

[29]  D G Gadian,et al.  Quantification of Perfusion Using Bolus Tracking Magnetic Resonance Imaging in Stroke: Assumptions, Limitations, and Potential Implications for Clinical Use , 2002, Stroke.

[30]  C. Kennard,et al.  The anatomy of visual neglect. , 2003, Brain : a journal of neurology.

[31]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[32]  Wilhelm Küker,et al.  Using SPM normalization for lesion analysis in spatial neglect. , 2004, Brain : a journal of neurology.

[33]  Leif Johannsen,et al.  Normalized perfusion MRI to identify common areas of dysfunction: patients with basal ganglia neglect. , 2005, Brain : a journal of neurology.

[34]  H. Duffau,et al.  Direct Evidence for a Parietal-Frontal Pathway Subserving Spatial Awareness in Humans , 2005, Science.

[35]  Michael Erb,et al.  Perisylvian white matter connectivity in the human right hemisphere , 2009, BMC Neuroscience.

[36]  D M Reboussin,et al.  A comparison of fast spin-echo, fluid-attenuated inversion-recovery, and diffusion-weighted MR imaging in the first 10 days after cerebral infarction. , 1999, AJNR. American journal of neuroradiology.

[37]  K. Uemura,et al.  MRI of acute cerebral infarction: a comparison of FLAIR and T2-weighted fast spin-echo imaging , 1997, Neuroradiology.

[38]  Hans-Otto Karnath,et al.  Disorders of spatial orientation , 2003 .

[39]  Hans-Otto Karnath,et al.  Spatial Limitation of Eye Movements During Ocular Exploration of Simple Line Drawings in Neglect Syndrome , 1994, Cortex.

[40]  J. Driver,et al.  Task-related modulation of visual neglect in cancellation tasks , 2009, Neuropsychologia.

[41]  G. Mangun,et al.  The neural mechanisms of top-down attentional control , 2000, Nature Neuroscience.

[42]  J W Belliveau,et al.  Functional cerebral imaging by susceptibility‐contrast NMR , 1990, Magnetic resonance in medicine.

[43]  Robert R. Edelman,et al.  Clinical Correlations of Diffusion and Perfusion Lesion Volumes in Acute Ischemic Stroke , 2000, Cerebrovascular Diseases.

[44]  J. Baron,et al.  Perfusion Thresholds in Human Cerebral Ischemia: Historical Perspective and Therapeutic Implications , 2001, Cerebrovascular Diseases.

[45]  H. Karnath,et al.  Spontaneous eye and head position in patients with spatial neglect , 2005, Journal of Neurology.

[46]  Biyu J. He,et al.  Breakdown of Functional Connectivity in Frontoparietal Networks Underlies Behavioral Deficits in Spatial Neglect , 2007, Neuron.

[47]  D. Perani,et al.  The anatomy of unilateral neglect after right-hemisphere stroke lesions. A clinical/CT-scan correlation study in man , 1986, Neuropsychologia.

[48]  H. Karnath A right perisylvian neural network for human spatial orienting , 2010 .

[49]  Chris Rorden,et al.  Spatial Normalization of Brain Images with Focal Lesions Using Cost Function Masking , 2001, NeuroImage.

[50]  H. Ellis stroke , 1997, The Lancet.

[51]  R J Seitz,et al.  Diffusion- and perfusion-weighted MRI: influence of severe carotid artery stenosis on the DWI/PWI mismatch in acute stroke. , 2000, Stroke.

[52]  Roland Bammer,et al.  Influence of Arterial Input Function on Hypoperfusion Volumes Measured With Perfusion-Weighted Imaging , 2003, Stroke.

[53]  Umberto Sabatini,et al.  Neural bases of personal and extrapersonal neglect in humans. , 2007, Brain : a journal of neurology.

[54]  R J Seitz,et al.  Diffusion- and perfusion-weighted MRI. The DWI/PWI mismatch region in acute stroke. , 1999, Stroke.

[55]  Christopher Kennard,et al.  Visual neglect associated with frontal lobe infarction , 1996, Journal of Neurology.

[56]  Bruce T. Volpe,et al.  Classical “parietal” neglect syndrome after subcortical right frontal lobe infarction , 1983, Neurology.

[57]  Irène Buvat,et al.  Detection of inter-hemispheric asymmetries of brain perfusion in SPECT , 2003 .

[58]  P. Bartolomeo,et al.  Left unilateral neglect as a disconnection syndrome. , 2007, Cerebral cortex.

[59]  Chris Rorden,et al.  Damage to white matter fiber tracts in acute spatial neglect. , 2009, Cerebral cortex.

[60]  Derek K. Jones,et al.  Symmetries in human brain language pathways correlate with verbal recall , 2007, Proceedings of the National Academy of Sciences.

[61]  G. Johnson,et al.  Dynamic susceptibility contrast MR imaging: Correlation of signal intensity changes with cerebral blood volume measurements , 2000, Journal of magnetic resonance imaging : JMRI.

[62]  M. E. Moseley,et al.  Correlation of perfusion- and diffusion-weighted MRI with NIHSS score in acute (<6.5 hour) ischemic stroke , 1998, Neurology.

[63]  A. Hillis,et al.  Hypoperfusion of Wernicke's area predicts severity of semantic deficit in acute stroke , 2001, Annals of neurology.

[64]  K M Heilman,et al.  Frontal lobe neglect in man , 1972, Neurology.