Separating neural correlates of allocentric and egocentric neglect: Distinct cortical sites and common white matter disconnections

Insights into the functional nature and neuroanatomy of spatial attention have come from research in neglect patients but to date many conflicting results have been reported. The novelty of the current study is that we used voxel-wise analyses based on information from segmented grey and white matter tissue combined with diffusion tensor imaging to decompose neural substrates of different neglect symptoms. Allocentric neglect was associated with damage to posterior cortical regions (posterior superior temporal sulcus, angular, middle temporal and middle occipital gyri). In contrast, egocentric neglect was associated with more anterior cortical damage (middle frontal, postcentral, supramarginal, and superior temporal gyri) and damage within subcortical structures. Damage to intraparietal sulcus (IPS) and the temporo-parietal junction (TPJ) was associated with both forms of neglect. Importantly, we showed that both disorders were associated with white matter lesions suggesting damage within long association and projection pathways such as the superior longitudinal, superior fronto-occipital, inferior longitudinal, and inferior fronto-occipital fascicule, thalamic radiation, and corona radiata. We conclude that distinct cortical regions control attention (a) across space (using an egocentric frame of reference) and (b) within objects (using an allocentric frame of reference), while common cortical regions (TPJ, IPS) and common white matter pathways support interactions across the different cortical regions.

[1]  G. Humphreys,et al.  Attention, spatial representation, and visual neglect: simulating emergent attention and spatial memory in the selective attention for identification model (SAIM). , 2003, Psychological review.

[2]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

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

[4]  Karl J. Friston,et al.  Statistical parametric mapping , 2013 .

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

[6]  Guy B. Williams,et al.  Diffusion tensor imaging in chronic head injury survivors: correlations with learning and memory indices , 2006, NeuroImage.

[7]  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.

[8]  Lorraine K. Tyler,et al.  Identifying lesions on structural brain images—Validation of the method and application to neuropsychological patients , 2005, Brain and Language.

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

[10]  Glyn W. Humphreys,et al.  Evidence from unilateral visual neglect , 1995 .

[11]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

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

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

[14]  L C Robertson,et al.  The breakdown and rehabilitation of visuospatial dysfunction in brain-injured patients. , 1983, International rehabilitation medicine.

[15]  D. Levine,et al.  UNILATERAL NEGLECT IS MORE SEVERE AND COMMON IN OLDER PATIENTS WITH RIGHT HEMISPHERIC STROKE , 2009, Neurology.

[16]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

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

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

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

[20]  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.

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

[22]  HighWire Press Philosophical Transactions of the Royal Society of London , 1781, The London Medical Journal.

[23]  John C. Marshall,et al.  Toward a principled explanation of unilateral neglect , 1994 .

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

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

[26]  Glyn W. Humphreys,et al.  The effect of cueing on unilateral neglect , 1983, Neuropsychologia.

[27]  Karl J. Friston,et al.  Spatial normalization of lesioned brains: Performance evaluation and impact on fMRI analyses , 2007, NeuroImage.

[28]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[29]  K. Worsley Developments in Random Field Theory , 2003 .

[30]  W. Bank The Human Brain. Surface, Three-Dimensional Sectional Anatomy and MRI , 1993 .

[31]  G. Vallar Extrapersonal Visual Unilateral Spatial Neglect and Its Neuroanatomy , 2001, NeuroImage.

[32]  H. Karnath New insights into the functions of the superior temporal cortex , 2001, Nature Reviews Neuroscience.

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

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

[35]  Dietmar Heinke,et al.  Simulating posterior parietal damage in a biologically plausible framework: Neuropsychological tests of the search over time and space model , 2009, Cognitive neuropsychology.

[36]  Christine Delmaire,et al.  Visualization of disconnection syndromes in humans , 2008, Cortex.

[37]  Galia Avidan,et al.  Reduced structural connectivity in ventral visual cortex in congenital prosopagnosia , 2009, Nature Neuroscience.

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

[39]  P. Gorelick,et al.  The Brain Atlas: A Visual Guide to the Human Central Nervous System, 3rd ed. , 2003, American Journal of Neuroradiology.

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

[41]  Glyn W. Humphreys,et al.  Author ' s personal copy Decomposing the neural mechanisms of visual search through model-based analysis of fMRI : Top-down excitation , active ignoring and the use of saliency by the right TPJ , 2012 .

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

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

[44]  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.

[45]  Glyn W. Humphreys,et al.  “Paradoxical neglect”: spatial representations, hemisphere-specific activation, and spatial cueing , 1995 .

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

[47]  Karl J. Friston,et al.  Distributional Assumptions in Voxel-Based Morphometry , 2002, NeuroImage.

[48]  C. Kennard,et al.  Reply to: Using SPM normalization for lesion analysis in spatial neglect , 2004 .

[49]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[50]  R. Walker,et al.  Object-Based Neglect: An Investigation of the Contributions of Eye Movements and Perceptual Completion , 1996, Cortex.

[51]  G W Humphreys,et al.  Neural representation of objects in space: a dual coding account. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[52]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[53]  Sinisa Pajevic,et al.  Color schemes to represent the orientation of anisotropic tissues from diffusion tensor data: Application to white matter fiber tract mapping in the human brain , 1999, Magnetic resonance in medicine.

[54]  Fabrizio Doricchi,et al.  Implicit Semantic Evaluation of Object Symmetry and Contralesional Visual Denial in A Case of Left Unilateral Neglect with Damage of The Dorsal Paraventricular White Matter , 2000, Cortex.

[55]  Wenya Linda Bi,et al.  The Brain Atlas: A Visual Guide to the Human Central Nervous System , 2002, The Yale Journal of Biology and Medicine.

[56]  G. Vallar,et al.  Neglect syndromes: the role of the parietal cortex. , 2003, Advances in neurology.

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

[58]  Glyn W. Humphreys,et al.  Attention to within-object and between-object spatial representations: multiple sites for visual selection , 1994 .

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

[60]  K. Heilman,et al.  Mechanisms underlying hemispatial neglect , 1979, Annals of neurology.

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

[62]  J. Walker Saccadic Eye Movements in Object-based Neglect , 1996 .

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

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

[65]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[66]  Carl R Olson,et al.  Brain representation of object-centered space in monkeys and humans. , 2003, Annual review of neuroscience.

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

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