Is there a critical lesion site for unilateral spatial neglect? A meta-analysis using activation likelihood estimation

The critical lesion site responsible for the syndrome of unilateral spatial neglect has been debated for more than a decade. Here we performed an activation likelihood estimation (ALE) to provide for the first time an objective quantitative index of the consistency of lesion sites across anatomical group studies of spatial neglect. The analysis revealed several distinct regions in which damage has consistently been associated with spatial neglect symptoms. Lesioned clusters were located in several cortical and subcortical regions of the right hemisphere, including the middle and superior temporal gyrus, inferior parietal lobule, intraparietal sulcus, precuneus, middle occipital gyrus, caudate nucleus, and posterior insula, as well as in the white matter pathway corresponding to the posterior part of the superior longitudinal fasciculus. Further analyses suggested that separate lesion sites are associated with impairments in different behavioral tests, such as line bisection and target cancellation. Similarly, specific subcomponents of the heterogeneous neglect syndrome, such as extinction and allocentric and personal neglect, are associated with distinct lesion sites. Future progress in delineating the neuropathological correlates of spatial neglect will depend upon the development of more refined measures of perceptual and cognitive functions than those currently available in the clinical setting.

[1]  Jon Driver,et al.  Integration of Goal- and Stimulus-Related Visual Signals Revealed by Damage to Human Parietal Cortex , 2010, The Journal of Neuroscience.

[2]  K. Heilman,et al.  Neglect and Related Disorders , 1984, Seminars in neurology.

[3]  John C. Marshall,et al.  Individual variation in line bisection: A study of four patients with right hemisphere damage and normal controls , 1990, Neuropsychologia.

[4]  Ian H. Robertson,et al.  Personal Versus Extrapersonal Neglect: A Group Study of their Dissociation Using a Reliable Clinical Test , 1997, Cortex.

[5]  Katrin Amunts,et al.  White matter fiber tracts of the human brain: Three-dimensional mapping at microscopic resolution, topography and intersubject variability , 2006, NeuroImage.

[6]  Pia Rotshtein,et al.  Separating neural correlates of allocentric and egocentric neglect: Distinct cortical sites and common white matter disconnections , 2010, Cognitive neuropsychology.

[7]  E. De Renzi,et al.  An experimental investigation on the nature of extinction. , 1995, Neuropsychologia.

[8]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

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

[10]  Manfred Fahle,et al.  Dissociation of egocentric and allocentric coding of space in visual search after right middle cerebral artery stroke , 2008, Neuropsychologia.

[11]  P. Good,et al.  A Simple Test , 1994 .

[12]  Chris Rorden,et al.  Improving Lesion-Symptom Mapping , 2007, Journal of Cognitive Neuroscience.

[13]  P. Halligan,et al.  The incidence of neglect phenomena and related disorders in patients with an acute right or left hemisphere stroke. , 1993, Age and ageing.

[14]  M. Catani,et al.  The arcuate fasciculus and the disconnection theme in language and aphasia: History and current state , 2008, Cortex.

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

[16]  K. Zilles,et al.  Line bisection judgments implicate right parietal cortex and cerebellum as assessed by fMRI , 2000, Neurology.

[17]  H. Karnath,et al.  The anatomy of spatial neglect , 2012, Neuropsychologia.

[18]  Jenni A Ogden,et al.  Anterior-posterior interhemispheric differences in the loci of lesions producing visual hemineglect , 1985, Brain and Cognition.

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

[20]  Guinevere F. Eden,et al.  Meta-Analysis of the Functional Neuroanatomy of Single-Word Reading: Method and Validation , 2002, NeuroImage.

[21]  Elizabeth Coulthard,et al.  Visual neglect after right posterior cerebral artery infarction , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[22]  A. Yamadori,et al.  Dissociation of body-centered and stimulus-centered representations in unilateral neglect , 2001, Neurology.

[23]  M. Corbetta,et al.  Spatial neglect and attention networks. , 2011, Annual review of neuroscience.

[24]  J. Marshall,et al.  Unilateral neglect , 1998, Neurology.

[25]  T. Schenkenberg,et al.  Line bisection and unilateral visual neglect in patients with neurologic impairment , 1980, Neurology.

[26]  G Vallar,et al.  Anatomical correlates of visual and tactile extinction in humans: a clinical CT scan study. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[27]  E. Bullmore,et al.  Meta-Analysis of Gray Matter Anomalies in Schizophrenia: Application of Anatomic Likelihood Estimation and Network Analysis , 2008, Biological Psychiatry.

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

[29]  J. Binder,et al.  Distinct syndromes of hemineglect. , 1992, Archives of neurology.

[30]  A. Hillis,et al.  Dissociation between egocentric and allocentric visuospatial and tactile neglect in acute stroke , 2008, Cortex.

[31]  Angela M. Uecker,et al.  ALE meta‐analysis: Controlling the false discovery rate and performing statistical contrasts , 2005, Human brain mapping.

[32]  H. Karnath,et al.  Disturbed line bisection is associated with posterior brain lesions , 2006, Brain Research.

[33]  B H Price,et al.  Dissociated perceptual-sensory and exploratory-motor neglect. , 1992, Journal of neurology, neurosurgery, and psychiatry.

[34]  F. Tomaiuolo,et al.  The anatomy of neglect without hemianopia: a key role for parietal–frontal disconnection? , 2003, Neuroreport.

[35]  Wilhelm Küker,et al.  The cortical substrate of visual extinction , 2003, Neuroreport.

[36]  G. Orban,et al.  Attention Mechanisms in Visual SearchAn fMRI Study , 2000, Journal of Cognitive Neuroscience.

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

[38]  Michael J. Martinez,et al.  Bias between MNI and Talairach coordinates analyzed using the ICBM‐152 brain template , 2007, Human brain mapping.

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

[40]  R. Ptak,et al.  Cortical and subcortical anatomy of chronic spatial neglect following vascular damage , 2008, Behavioral and Brain Functions.

[41]  M. Mesulam,et al.  Remapping attentional priorities: differential contribution of superior parietal lobule and intraparietal sulcus. , 2007, Cerebral cortex.

[42]  H. Karnath,et al.  Personal neglect—A disorder of body representation? , 2011, Neuropsychologia.

[43]  C. Guariglia,et al.  Personal and extrapersonal space: A case of neglect dissociation , 1992, Neuropsychologia.

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

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

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

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

[48]  Maurizio Corbetta,et al.  A Behavioral Analysis of Spatial Neglect and its Recovery After Stroke , 2011, Front. Hum. Neurosci..

[49]  S. Yantis,et al.  Spatially selective representations of voluntary and stimulus-driven attentional priority in human occipital, parietal, and frontal cortex. , 2007, Cerebral cortex.

[50]  C. Oppenheim,et al.  DTI-MR tractography of white matter damage in stroke patients with neglect , 2011, Experimental Brain Research.

[51]  Vijay Kannan,et al.  Neural Substrates of Visuospatial Processing in Distinct Reference Frames: Evidence from Unilateral Spatial Neglect , 2009, Journal of Cognitive Neuroscience.

[52]  J. Marshall,et al.  VISUOSPATIAL NEGLECT: UNDERLYING FACTORS AND TEST SENSITIVITY , 1989, The Lancet.

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

[54]  M. Sale,et al.  Testing for Spatial Neglect with Line Bisection and Target Cancellation: Are Both Tasks Really Unrelated? , 2011, PloS one.

[55]  P. Bartolomeo,et al.  White matter (dis)connections and gray matter (dys)functions in visual neglect: Gaining insights into the brain networks of spatial awareness , 2008, Cortex.

[56]  P. Weiss,et al.  Visual extinction in relation to visuospatial neglect after right-hemispheric stroke: quantitative assessment and statistical lesion-symptom mapping , 2011, Journal of Neurology, Neurosurgery & Psychiatry.

[57]  Argye E. Hillis,et al.  Right hemispatial neglect: Frequency and characterization following acute left hemisphere stroke , 2007, Brain and Cognition.

[58]  Clive H. Y. Wong,et al.  Autistic Disorders and Schizophrenia: Related or Remote? An Anatomical Likelihood Estimation , 2010, PloS one.

[59]  K. Zilles,et al.  Coordinate‐based activation likelihood estimation meta‐analysis of neuroimaging data: A random‐effects approach based on empirical estimates of spatial uncertainty , 2009, Human brain mapping.

[60]  K. Lovblad,et al.  Neuroanatomy of hemispatial neglect and its functional components: a study using voxel-based lesion-symptom mapping. , 2010, Brain : a journal of neurology.

[61]  B. Aouizerate,et al.  Gray Matter Alterations in Obsessive–Compulsive Disorder: An Anatomic Likelihood Estimation Meta-Analysis , 2010, Neuropsychopharmacology.

[62]  Céline R. Gillebert,et al.  Spatial attention deficits in humans: The critical role of superior compared to inferior parietal lesions , 2012, Neuropsychologia.

[63]  G. Busatto,et al.  Neurostructural predictors of Alzheimer's disease: A meta-analysis of VBM studies , 2011, Neurobiology of Aging.

[64]  S. Ferber,et al.  How to Assess Spatial Neglect - Line Bisection or Cancellation Tasks? , 2001, Journal of clinical and experimental neuropsychology.

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

[66]  P. Weiss,et al.  Testing for neglect in right-hemispheric stroke patients using a new assessment battery based upon standardized activities of daily living (ADL) , 2010, Neuropsychologia.

[67]  P Bartolomeo,et al.  Brain networks of spatial awareness: evidence from diffusion tensor imaging tractography , 2007, Journal of Neurology, Neurosurgery, and Psychiatry.

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

[69]  M. Albert A simple test of visual neglect , 1973, Neurology.

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

[71]  Patrick Dupont,et al.  Lesion evidence for the critical role of the intraparietal sulcus in spatial attention. , 2011, Brain : a journal of neurology.

[72]  S. Wakana,et al.  MRI Atlas of Human White Matter , 2005 .

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

[74]  Argye E. Hillis,et al.  Neurobiology of Unilateral Spatial Neglect , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[75]  M. Farah,et al.  Unconscious perception of “extinguished” visual stimuli: Reassessing the evidence , 1991, Neuropsychologia.

[76]  T. Shallice,et al.  Right posterior cortical functions in a tumour patient series , 2010, Cortex.

[77]  R. Cubelli,et al.  Neglect Without Extinction , 1999, Cortex.

[78]  F. Dick,et al.  Voxel-based lesion–symptom mapping , 2003, Nature Neuroscience.

[79]  J. Duncan,et al.  Competitive brain activity in visual attention , 1997, Current Opinion in Neurobiology.

[80]  J. Bogousslavsky,et al.  Stroke Syndromes: Arterial territories of the human brain , 2001 .

[81]  A. Dale,et al.  Functional Parcellation of Attentional Control Regions of the Brain , 2004, Journal of Cognitive Neuroscience.

[82]  Jon Driver,et al.  Revisiting Previously Searched Locations in Visual Neglect: Role of Right Parietal and Frontal Lesions in Misjudging Old Locations as New , 2005, Journal of Cognitive Neuroscience.

[83]  P. Szeszko,et al.  MRI atlas of human white matter , 2006 .

[84]  H. Birch,et al.  Delayed information processing and extinction following cerebral damage. , 1967, Brain : a journal of neurology.

[85]  Leif Johannsen,et al.  The anatomy underlying acute versus chronic spatial neglect: a longitudinal study. , 2011, Brain : a journal of neurology.

[86]  Céline R. Gillebert,et al.  Parcellation of parietal cortex: Convergence between lesion-symptom mapping and mapping of the intact functioning brain , 2009, Behavioural Brain Research.

[87]  Regine Zopf,et al.  Perfusion Imaging of the Right Perisylvian Neural Network in Acute Spatial Neglect , 2009, Front. Hum. Neurosci..

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

[89]  Ronald Peeters,et al.  Convergence between Lesion-Symptom Mapping and Functional Magnetic Resonance Imaging of Spatially Selective Attention in the Intact Brain , 2008, The Journal of Neuroscience.