Measuring graphical strength within the connectome: A neuroanatomic, parcellation-based study

INTRODUCTION Graph theory is a promising mathematical tool to study the connectome. However, little research has been undertaken to correlate graph metrics to functional properties of the brain. In this study, we report a unique association between the strength of cortical regions and their function. METHODS Eight structural graphs were constructed within DSI Studio using publicly available imaging data derived from the Human Connectome Project. Whole-brain fiber tractography was performed to quantify the strength of each cortical region comprising our atlas. RESULTS Rank-order analysis revealed 27 distinct areas with high average strength, several of which are associated with eloquent cortical functions. Area 4 localizes to the primary motor cortex and is important for fine motor control. Areas 2, 3a and 3b localize to the primary sensory cortex and are involved in primary sensory processing. Areas V1-V4 in the occipital pole are involved in primary visual processing. Several language areas, including area 44, were also found to have high average strength. CONCLUSIONS Regions of average high strength tend to localize to eloquent areas of the brain, such as the primary sensorimotor cortex, primary visual cortex, and Broca's area. Future studies will examine the dynamic effects of neurologic disease on this metric.

[1]  Robert G. Briggs,et al.  A Connectomic Atlas of the Human Cerebrum-Chapter 2: The Lateral Frontal Lobe. , 2018, Operative neurosurgery.

[2]  R. Cameron Craddock,et al.  A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics , 2013, NeuroImage.

[3]  R. Seitz,et al.  Functional anatomy of language processing: Neuroimaging and the problem of individual variability , 1991, Neuropsychologia.

[4]  Distribution and size of GABAergic neurons in area 7b and the retroinsular cortex of the monkey , 1989, Brain Research.

[5]  Juan Ospina,et al.  Algebraic analysis of social networks for bio-surveillance: the cases of SARS-Beijing-2003 and AH1N1 influenza-México-2009. , 2011, Advances in experimental medicine and biology.

[6]  M. Berger,et al.  Frontal operculum gliomas: language outcome following resection. , 2015, Journal of neurosurgery.

[7]  Timothy Edward John Behrens,et al.  Diffusion-Weighted Imaging Tractography-Based Parcellation of the Human Parietal Cortex and Comparison with Human and Macaque Resting-State Functional Connectivity , 2011, The Journal of Neuroscience.

[8]  Robert G. Briggs,et al.  A Connectomic Atlas of the Human Cerebrum-Chapter 1: Introduction, Methods, and Significance. , 2018, Operative neurosurgery.

[9]  B. Wandell,et al.  Visual Field Maps in Human Cortex , 2007, Neuron.

[10]  L. Haberly,et al.  New Features of Connectivity in Piriform Cortex Visualized by Intracellular Injection of Pyramidal Cells Suggest that “Primary” Olfactory Cortex Functions Like “Association” Cortex in Other Sensory Systems , 2000, The Journal of Neuroscience.

[11]  F. Qiu,et al.  Figure and Ground in the Visual Cortex: V2 Combines Stereoscopic Cues with Gestalt Rules , 2005, Neuron.

[12]  K. Grill-Spector,et al.  The human visual cortex. , 2004, Annual review of neuroscience.

[13]  Robert G. Briggs,et al.  A Connectomic Atlas of the Human Cerebrum-Chapter 9: The Occipital Lobe. , 2018, Operative neurosurgery.

[14]  Ivan Toni,et al.  Comparable Mechanisms for Action and Language: Neural Systems Behind Intentions, Goals, and Means , 2006, Cortex.

[15]  Y. Naya.  Declarative association in the perirhinal cortex , 2016, Neuroscience Research.

[16]  Jane E. Joseph,et al.  The changing landscape of functional brain networks for face processing in typical development , 2012, NeuroImage.

[17]  Qin Chen,et al.  Functional connectome assessed using graph theory in drug-naive Parkinson’s disease , 2015, Journal of Neurology.

[18]  Vivek Prabhakaran,et al.  Disrupted Brain Functional Organization in Epilepsy Revealed by Graph Theory Analysis , 2015, Brain Connect..

[19]  D. Heeger,et al.  Two Retinotopic Visual Areas in Human Lateral Occipital Cortex , 2006, The Journal of Neuroscience.

[20]  Effects of an Exhaustive Exercise on Motor Skill Learning and on the Excitability of Primary Motor Cortex and Supplementary Motor Area , 2016, Medicine.

[21]  Robert G. Briggs,et al.  A Connectomic Atlas of the Human Cerebrum-Chapter 3: The Motor, Premotor, and Sensory Cortices. , 2018, Operative neurosurgery.

[22]  Jesper Andersson,et al.  A multi-modal parcellation of human cerebral cortex , 2016, Nature.

[23]  Russell A. Epstein.  Parahippocampal and retrosplenial contributions to human spatial navigation , 2008, Trends in Cognitive Sciences.

[24]  Robert G. Briggs,et al.  A Connectomic Atlas of the Human Cerebrum-Chapter 7: The Lateral Parietal Lobe. , 2018, Operative neurosurgery.

[25]  R. Tootell,et al.  An anterior temporal face patch in human cortex, predicted by macaque maps , 2009, Proceedings of the National Academy of Sciences.

[26]  Keith A. Johnson,et al.  Epicenters of dynamic connectivity in the adaptation of the ventral visual system , 2017, Human brain mapping.

[27]  Robert G. Briggs,et al.  A Connectomic Atlas of the Human Cerebrum-Chapter 8: The Posterior Cingulate Cortex, Medial Parietal Lobe, and Parieto-Occipital Sulcus. , 2018, Operative neurosurgery.

[28]  E. Maguire,et al.  What does the retrosplenial cortex do? , 2009, Nature Reviews Neuroscience.

[29]  Olaf Blanke,et al.  Distinct contributions of Brodmann areas 1 and 2 to body ownership. , 2015, Social cognitive and affective neuroscience.

[30]  David Poeppel,et al.  Functional Anatomic Models of Language: Assembling the Pieces , 2008, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[31]  D. Sharp,et al.  The role of the posterior cingulate cortex in cognition and disease. , 2014, Brain : a journal of neurology.

[32]  Alan C. Evans,et al.  Anatomical mapping of functional activation in stereotactic coordinate space , 1992, NeuroImage.

[33]  Mark Tommerdahl,et al.  Role of primary somatosensory cortex in the coding of pain , 2013, PAIN®.

[34]  Robert G. Briggs,et al.  A Connectomic Atlas of the Human Cerebrum-Chapter 4: The Medial Frontal Lobe, Anterior Cingulate Gyrus, and Orbitofrontal Cortex. , 2018, Operative neurosurgery.

[35]  Oury Monchi,et al.  Function of basal ganglia in bridging cognitive and motor modules to perform an action , 2014, Front. Neurosci..

[36]  J. Winawer,et al.  Human V4 and ventral occipital retinotopic maps , 2015, Visual Neuroscience.

[37]  Michele Furlan,et al.  Global Motion Processing in Human Visual Cortical Areas V2 and V3 , 2016, The Journal of Neuroscience.

[38]  L Krubitzer,et al.  Area 3a: topographic organization and cortical connections in marmoset monkeys. , 2001, Cerebral cortex.

[39]  Mitchel S. Berger,et al.  Analysis of the subcomponents and cortical terminations of the perisylvian superior longitudinal fasciculus: a fiber dissection and DTI tractography study , 2012, Brain Structure and Function.

[40]  Jean-Philippe Thiran,et al.  Graph theory reveals dysconnected hubs in 22q11DS and altered nodal efficiency in patients with hallucinations , 2013, Front. Hum. Neurosci..

[41]  A. Toga,et al.  Mapping the human connectome. , 2012, Neurosurgery.

[42]  Anita E. Bandrowski,et al.  The UCLA multimodal connectivity database: a web-based platform for brain connectivity matrix sharing and analysis , 2012, Front. Neuroinform..

[43]  Philippe A. Chouinard,et al.  The Primary Motor and Premotor Areas of the Human Cerebral Cortex , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[44]  Nadim Joni Shah,et al.  Probabilistic fibre tract analysis of cytoarchitectonically defined human inferior parietal lobule areas reveals similarities to macaques , 2011, NeuroImage.

[45]  Robert G. Briggs,et al.  A Connectomic Atlas of the Human Cerebrum-Chapter 6: The Temporal Lobe. , 2018, Operative neurosurgery.

[46]  Haibo Xu,et al.  Disrupted functional brain connectome in unilateral sudden sensorineural hearing loss , 2016, Hearing Research.

[47]  Aifeng Zhang,et al.  Graph theory analysis of cortical-subcortical networks in late-life depression. , 2014, The American journal of geriatric psychiatry : official journal of the American Association for Geriatric Psychiatry.

[48]  B. Martínez-López,et al.  Social network analysis. Review of general concepts and use in preventive veterinary medicine. , 2009, Transboundary and emerging diseases.

[49]  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.

[50]  J Hyvärinen,et al.  Receptive field integration and submodality convergence in the hand area of the post‐central gyrus of the alert monkey. , 1978, The Journal of physiology.

[51]  H. Freund,et al.  Differential organization of touch and pain in human primary somatosensory cortex. , 2000, Journal of neurophysiology.

[52]  D. Yao,et al.  Diffusion tensor tractography reveals disrupted structural connectivity in childhood absence epilepsy , 2014, Epilepsy Research.

[53]  Doris Y. Tsao,et al.  Comparing face patch systems in macaques and humans , 2008, Proceedings of the National Academy of Sciences.

[54]  Amar Dhand,et al.  Leadership in neurology: A social network analysis , 2014, Annals of neurology.

[55]  Katrin Amunts,et al.  Cortical Folding Patterns and Predicting Cytoarchitecture , 2007, Cerebral cortex.

[56]  P. Rossini,et al.  Human brain networks in physiological aging: a graph theoretical analysis of cortical connectivity from EEG data. , 2014, Journal of Alzheimer's disease : JAD.

[57]  Robert G. Briggs,et al.  A Connectomic Atlas of the Human Cerebrum-Chapter 5: The Insula and Opercular Cortex. , 2018, Operative neurosurgery.

[58]  Tristan A. Chaplin,et al.  Contrasting patterns of cortical input to architectural subdivisions of the area 8 complex: a retrograde tracing study in marmoset monkeys. , 2013, Cerebral cortex.

[59]  Fang-Cheng Yeh,et al.  Generalized ${ q}$-Sampling Imaging , 2010, IEEE Transactions on Medical Imaging.

[60]  Byron Bernal,et al.  How Localized are Language Brain Areas? A Review of Brodmann Areas Involvement in Oral Language. , 2016, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[61]  Danielle S Bassett,et al.  Brain graphs: graphical models of the human brain connectome. , 2011, Annual review of clinical psychology.

[62]  Pan Wang,et al.  Frequency-Dependent Altered Functional Connections of Default Mode Network in Alzheimer’s Disease , 2017, Front. Aging Neurosci..

[63]  Yufeng Zang,et al.  Standardizing the intrinsic brain: Towards robust measurement of inter-individual variation in 1000 functional connectomes , 2013, NeuroImage.

[64]  Troy A Hackett,et al.  Anatomic organization of the auditory cortex. , 2015, Handbook of clinical neurology.

[65]  Richard C Saunders,et al.  The origin of projections from the posterior cingulate and retrosplenial cortices to the anterior, medial dorsal and laterodorsal thalamic nuclei of macaque monkeys , 2013, The European journal of neuroscience.

[66]  Mark Jenkinson,et al.  Correspondences between retinotopic areas and myelin maps in human visual cortex , 2014, NeuroImage.

[67]  Paul J Laurienti,et al.  Graph theory analysis of functional brain networks and mobility disability in older adults. , 2014, The journals of gerontology. Series A, Biological sciences and medical sciences.

[68]  David N. Vaughan,et al.  The Piriform Cortex and Human Focal Epilepsy , 2014, Front. Neurol..