Anatomical Substrates of the Alerting, Orienting and Executive Control Components of Attention: Focus on the Posterior Parietal Lobe

Both neuropsychological and functional neuroimaging studies have identified that the posterior parietal lobe (PPL) is critical for the attention function. However, the unique role of distinct parietal cortical subregions and their underlying white matter (WM) remains in question. In this study, we collected both magnetic resonance imaging and diffusion tensor imaging (DTI) data in normal participants, and evaluated their attention performance using attention network test (ANT), which could isolate three different attention components: alerting, orienting and executive control. Cortical thickness, surface area and DTI parameters were extracted from predefined PPL subregions and correlated with behavioural performance. Tract-based spatial statistics (TBSS) was used for the voxel-wise statistical analysis. Results indicated structure-behaviour relationships on multiple levels. First, a link between the cortical thickness and WM integrity of the right inferior parietal regions and orienting performance was observed. Specifically, probabilistic tractography demonstrated that the integrity of WM connectivity between the bilateral inferior parietal lobules mediated the orienting performance. Second, the scores of executive control were significantly associated with the WM diffusion metrics of the right supramarginal gyrus. Finally, TBSS analysis revealed that alerting performance was significant correlated with the fractional anisotropy of local WM connecting the right thalamus and supplementary motor area. We conclude that distinct areas and features within PPL are associated with different components of attention. These findings could yield a more complete understanding of the nature of the PPL contribution to visuospatial attention.

[1]  P. Strick,et al.  Supplementary Motor Area and Presupplementary Motor Area: Targets of Basal Ganglia and Cerebellar Output , 2007, The Journal of Neuroscience.

[2]  S. Kastner,et al.  Mechanisms of Spatial Attention Control in Frontal and Parietal Cortex , 2010, The Journal of Neuroscience.

[3]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[4]  James W Bisley,et al.  The role of the lateral intraparietal area in orienting attention and its implications for visual search , 2011, The European journal of neuroscience.

[5]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[6]  Mark W. Woolrich,et al.  Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? , 2007, NeuroImage.

[7]  L. Westlye,et al.  Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. , 2010, Cerebral cortex.

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

[9]  Timothy Edward John Behrens,et al.  Connection patterns distinguish 3 regions of human parietal cortex. , 2006, Cerebral cortex.

[10]  R. Zahn,et al.  Asymmetries of visual attention after circumscribed subcortical vascular lesions , 2001, Journal of neurology, neurosurgery, and psychiatry.

[11]  George Bush,et al.  Cingulate, Frontal, and Parietal Cortical Dysfunction in Attention-Deficit/Hyperactivity Disorder , 2011, Biological Psychiatry.

[12]  Vincent Walsh,et al.  The perceptual and functional consequences of parietal top-down modulation on the visual cortex. , 2009, Cerebral cortex.

[13]  Hugo D. Critchley,et al.  Brain activity relating to the contingent negative variation: an fMRI investigation , 2004, NeuroImage.

[14]  Alan C. Evans,et al.  A nonparametric method for automatic correction of intensity nonuniformity in MRI data , 1998, IEEE Transactions on Medical Imaging.

[15]  Gereon R Fink,et al.  Cerebral correlates of alerting, orienting and reorienting of visuospatial attention: an event-related fMRI study , 2004, NeuroImage.

[16]  M. Corbetta,et al.  Right Hemisphere Dominance during Spatial Selective Attention and Target Detection Occurs Outside the Dorsal Frontoparietal Network , 2010, The Journal of Neuroscience.

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

[18]  C. Frith,et al.  A fronto-parietal network for rapid visual information processing: a PET study of sustained attention and working memory , 1996, Neuropsychologia.

[19]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[20]  A. Dale,et al.  Distinct genetic influences on cortical surface area and cortical thickness. , 2009, Cerebral cortex.

[21]  Leslie G. Ungerleider,et al.  Posterior parietal cortex and the filtering of distractors , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Alan C. Evans,et al.  Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. , 2009, Cerebral cortex.

[23]  Mert R. Sabuncu,et al.  Measuring and comparing brain cortical surface area and other areal quantities , 2012, NeuroImage.

[24]  K Mathiak,et al.  Effects of a CACNA1C genotype on attention networks in healthy individuals , 2010, Psychological Medicine.

[25]  L. Westlye,et al.  Neuroanatomical correlates of executive functions in children and adolescents: A magnetic resonance imaging (MRI) study of cortical thickness , 2010, Neuropsychologia.

[26]  B. Gulyás,et al.  Activation by Attention of the Human Reticular Formation and Thalamic Intralaminar Nuclei , 1996, Science.

[27]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[28]  C. Eriksen,et al.  Effects of noise letters upon the identification of a target letter in a nonsearch task , 1974 .

[29]  J. Mattingley,et al.  Fast and slow parietal pathways mediate spatial attention , 2004, Nature Neuroscience.

[30]  Bruce D. McCandliss,et al.  Response Anticipation and Response Conflict: An Event-Related Potential and Functional Magnetic Resonance Imaging Study , 2007, The Journal of Neuroscience.

[31]  Caterina Mainero,et al.  fMRI evidence of brain reorganization during attention and memory tasks in multiple sclerosis , 2004, NeuroImage.

[32]  Sami Schiff,et al.  Timing Spatial Conflict within the Parietal Cortex: A TMS Study , 2011, Journal of Cognitive Neuroscience.

[33]  M. Behrmann,et al.  Parietal cortex and attention , 2004, Current Opinion in Neurobiology.

[34]  C. Price,et al.  Phonological decisions require both the left and right supramarginal gyri , 2010, Proceedings of the National Academy of Sciences.

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

[36]  Simon B Eickhoff,et al.  Dissociating bottom-up and top-down processes in a manual stimulus-response compatibility task. , 2010, Journal of neurophysiology.

[37]  K. Willmes,et al.  On the Functional Neuroanatomy of Intrinsic and Phasic Alertness , 2001, NeuroImage.

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

[39]  Hengyi Rao,et al.  The role of human parietal cortex in attention networks. , 2003, Brain : a journal of neurology.

[40]  Alan C. Evans,et al.  Cortical thickness analysis examined through power analysis and a population simulation , 2005, NeuroImage.

[41]  M. Kinsbourne Hemi-neglect and hemisphere rivalry. , 1977, Advances in neurology.

[42]  Michael H. Buonocore,et al.  Integrating Conflict Detection and Attentional Control Mechanisms , 2011, Journal of Cognitive Neuroscience.

[43]  R. Wurtz,et al.  Guarding the gateway to cortex: attention in visual thalamus , 2008, Nature.

[44]  Alan C. Evans,et al.  Automated 3-D extraction and evaluation of the inner and outer cortical surfaces using a Laplacian map and partial volume effect classification , 2005, NeuroImage.

[45]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[46]  M. Husain,et al.  Role of right posterior parietal cortex in maintaining attention to spatial locations over time , 2009, Brain : a journal of neurology.

[47]  L. Westlye,et al.  Associations between regional cortical thickness and attentional networks as measured by the attention network test. , 2011, Cerebral cortex.

[48]  M. Posner,et al.  Mapping the genetic variation of executive attention onto brain activity , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Adam E. Green,et al.  Using genetic data in cognitive neuroscience: from growing pains to genuine insights , 2008, Nature Reviews Neuroscience.

[50]  G. V. Simpson,et al.  Dynamic Activation of Frontal, Parietal, and Sensory Regions Underlying Anticipatory Visual Spatial Attention , 2011, The Journal of Neuroscience.

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

[52]  Sven Bestmann,et al.  Studying the Role of Human Parietal Cortex in Visuospatial Attention with Concurrent TMS–fMRI , 2010, Cerebral cortex.

[53]  Eric Hahn,et al.  Attention network test (ANT) reveals gender-specific alterations of executive function in schizophrenia , 2009, Psychiatry Research.

[54]  Suzanne E. Welcome,et al.  Longitudinal Mapping of Cortical Thickness and Brain Growth in Normal Children , 2022 .

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

[56]  Robert Oostenveld,et al.  Neural Mechanisms of Visual Attention : How Top-Down Feedback Highlights Relevant Locations , 2007 .

[57]  Jeffrey M. Zacks,et al.  Lateral somatotopic organization during imagined and prepared movements. , 2006, Journal of neurophysiology.

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

[59]  Eric Hahn,et al.  Selective anterior cingulate cortex deficit during conflict solution in schizophrenia: an event-related potential study. , 2007, Journal of psychiatric research.

[60]  Alan C. Evans,et al.  Automatic "pipeline" analysis of 3-D MRI data for clinical trials: application to multiple sclerosis , 2002, IEEE Transactions on Medical Imaging.

[61]  B. Bahrami,et al.  Distractibility in Daily Life Is Reflected in the Structure and Function of Human Parietal Cortex , 2011, The Journal of Neuroscience.

[62]  G. Rizzolatti,et al.  Two different streams form the dorsal visual system: anatomy and functions , 2003, Experimental Brain Research.

[63]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[64]  Lingzhong Fan,et al.  Inferior frontal white matter asymmetry correlates with executive control of attention , 2013, Human brain mapping.

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

[66]  M. Posner Measuring Alertness , 2008, Annals of the New York Academy of Sciences.

[67]  M. Goldberg,et al.  Neuronal Activity in the Lateral Intraparietal Area and Spatial Attention , 2003, Science.

[68]  Pratik Mukherjee,et al.  Individual Differences in Distinct Components of Attention are Linked to Anatomical Variations in Distinct White Matter Tracts , 2009, Front. Neuroanat..

[69]  C. Caltagirone,et al.  Asymmetry of Parietal Interhemispheric Connections in Humans , 2011, The Journal of Neuroscience.

[70]  Vinod Menon,et al.  Parietal attentional system aberrations during target detection in adolescents with attention deficit hyperactivity disorder: event-related fMRI evidence. , 2006, The American journal of psychiatry.

[71]  J. P. Mayo Intrathalamic mechanisms of visual attention. , 2009, Journal of neurophysiology.

[72]  N. Sadato,et al.  Neural substrates of phasic alertness: A functional magnetic resonance imaging study , 2010, Neurosciences research.

[73]  Yong He,et al.  Age-related alterations in the modular organization of structural cortical network by using cortical thickness from MRI , 2011, NeuroImage.

[74]  Steven Robbins,et al.  An unbiased iterative group registration template for cortical surface analysis , 2007, NeuroImage.

[75]  Jin Fan,et al.  Selective impairment of attentional networks of orienting and executive control in schizophrenia , 2005, Schizophrenia Research.

[76]  Larson J. Hogstrom,et al.  The structure of the cerebral cortex across adult life: age-related patterns of surface area, thickness, and gyrification. , 2013, Cerebral cortex.

[77]  P. Rakić,et al.  Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[79]  Jun Yoshino,et al.  Demyelination increases radial diffusivity in corpus callosum of mouse brain , 2005, NeuroImage.

[80]  David Badre,et al.  Selection, Integration, and Conflict Monitoring Assessing the Nature and Generality of Prefrontal Cognitive Control Mechanisms , 2004, Neuron.

[81]  Daniel Rueckert,et al.  Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data , 2006, NeuroImage.

[82]  Jack L. Lancaster,et al.  Processing speed is correlated with cerebral health markers in the frontal lobes as quantified by neuroimaging , 2010, NeuroImage.

[83]  J. Buhle,et al.  Typologies of attentional networks , 2006, Nature Reviews Neuroscience.

[84]  Jin Fan,et al.  The activation of attentional networks , 2005, NeuroImage.

[85]  J. Bisley,et al.  A pure salience response in posterior parietal cortex. , 2011, Cerebral cortex.

[86]  P. Haggard,et al.  The role of the right temporoparietal junction in intersensory conflict: detection or resolution? , 2010, Experimental Brain Research.

[87]  Thomas Schenk,et al.  The Involvement of Posterior Parietal Cortex in Feature and Conjunction Visuomotor Search , 2011, Journal of Cognitive Neuroscience.

[88]  N. Andreasen,et al.  Global and regional cortical thinning in first-episode psychosis patients: relationships with clinical and cognitive features , 2010, Psychological Medicine.

[89]  F. Nielsen,et al.  Right temporoparietal cortex activation during visuo-proprioceptive conflict. , 2004, Cerebral Cortex.