Sensory-biased attention networks in human lateral frontal cortex revealed by intrinsic functional connectivity

&NA; Human frontal cortex is commonly described as being insensitive to sensory modality, however several recent studies cast doubt on this view. Our laboratory previously reported two visual‐biased attention regions interleaved with two auditory‐biased attention regions, bilaterally, within lateral frontal cortex. These regions selectively formed functional networks with posterior visual‐biased and auditory‐biased attention regions. Here, we conducted a series of functional connectivity analyses to validate and expand this analysis to 469 subjects from the Human Connectome Project (HCP). Functional connectivity analyses replicated the original findings and revealed a novel hemispheric connectivity bias. We also subdivided lateral frontal cortex into 21 thin‐slice ROIs and observed bilateral patterns of spatially alternating visual‐biased and auditory‐biased attention network connectivity. Finally, we performed a correlation difference analysis that revealed five additional bilateral lateral frontal regions differentially connected to either the visual‐biased or auditory‐biased attention networks. These findings leverage the HCP dataset to demonstrate that sensory‐biased attention networks may have widespread influence in lateral frontal cortical organization. Graphical abstract Figure. No caption available. HighlightsSensory‐biased attention networks extend into human lateral frontal cortex (LFC).Small N dataset used to mine Human Connectome Project dataset (N = 469).RS‐functional connectivity confirms 4 sensory‐biased LFC regions bilaterally.5 new putative sensory‐biased attention regions observed bilaterally in LFC.

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

[2]  Martin I. Sereno,et al.  Spatial maps in frontal and prefrontal cortex , 2006, NeuroImage.

[3]  E. DeYoe,et al.  Mapping striate and extrastriate visual areas in human cerebral cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[4]  V Menon,et al.  Modality effects in verbal working memory: differential prefrontal and parietal responses to auditory and visual stimuli , 2004, NeuroImage.

[5]  Susan M. Courtney,et al.  Functional topography of working memory for face or voice identity , 2005, NeuroImage.

[6]  Timothy O. Laumann,et al.  Evaluation of Denoising Strategies to Address Motion-Correlated Artifacts in Resting-State Functional Magnetic Resonance Imaging Data from the Human Connectome Project , 2016, Brain Connect..

[7]  Kathleen A. Hansen,et al.  Topographic Organization in and near Human Visual Area V4 , 2007, The Journal of Neuroscience.

[8]  R. Buckner,et al.  Parcellating Cortical Functional Networks in Individuals , 2015, Nature Neuroscience.

[9]  D. Pandya,et al.  The cortical connectivity of the prefrontal cortex in the monkey brain , 2012, Cortex.

[10]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[11]  René Marois,et al.  Mapping the pathways of information processing from sensation to action in four distinct sensorimotor tasks , 2009, Human brain mapping.

[12]  Lotfi B Merabet,et al.  Visual Topography of Human Intraparietal Sulcus , 2007, The Journal of Neuroscience.

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

[14]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[15]  David Badre,et al.  Cognitive control, hierarchy, and the rostro–caudal organization of the frontal lobes , 2008, Trends in Cognitive Sciences.

[16]  Russell A. Poldrack,et al.  Scanning the Horizon: Towards transparent and reproducible neuroimaging research , 2016 .

[17]  Ludovica Griffanti,et al.  Automatic denoising of functional MRI data: Combining independent component analysis and hierarchical fusion of classifiers , 2014, NeuroImage.

[18]  Christopher L. Asplund,et al.  A Unified attentional bottleneck in the human brain , 2011, Proceedings of the National Academy of Sciences.

[19]  H. Barbas,et al.  Organization of afferent input to subdivisions of area 8 in the rhesus monkey , 1981, The Journal of comparative neurology.

[20]  David J. Sharp,et al.  Separable networks for top-down attention to auditory non-spatial and visuospatial modalities , 2013, NeuroImage.

[21]  Clayton E. Curtis,et al.  Persistent neural activity during the maintenance of spatial position in working memory , 2008, NeuroImage.

[22]  E. DeYoe,et al.  A comparison of visual and auditory motion processing in human cerebral cortex. , 2000, Cerebral cortex.

[23]  F. Hanlon,et al.  Look Hear! The Prefrontal Cortex is Stratified by Modality of Sensory Input During Multisensory Cognitive Control , 2016, Cerebral cortex.

[24]  Juha Salmi,et al.  Orienting and maintenance of spatial attention in audition and vision: multimodal and modality-specific brain activations , 2007, Brain Structure and Function.

[25]  Jean-Baptiste Poline,et al.  Analysis of a large fMRI cohort: Statistical and methodological issues for group analyses , 2007, NeuroImage.

[26]  A. Dale,et al.  Functional Analysis of V3A and Related Areas in Human Visual Cortex , 1997, The Journal of Neuroscience.

[27]  M. Chun,et al.  Functional connectome fingerprinting: Identifying individuals based on patterns of brain connectivity , 2015, Nature Neuroscience.

[28]  Clayton E. Curtis,et al.  Persistent neural activity in the human frontal cortex when maintaining space that is “off the map” , 2009, Nature Neuroscience.

[29]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[30]  Jakob Heinzle,et al.  Topographically specific functional connectivity between visual field maps in the human brain , 2011, NeuroImage.

[31]  Örjan Blom,et al.  The dorsal auditory pathway is involved in performance of both visual and auditory rhythms , 2009, NeuroImage.

[32]  J. Duncan The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour , 2010, Trends in Cognitive Sciences.

[33]  Matthew F. Glasser,et al.  Trends and Properties of Human Cerebral Cortex: Correlations with Cortical Myelin Content Introduction and Review , 2022 .

[34]  Mark W. Woolrich,et al.  Resting-state fMRI in the Human Connectome Project , 2013, NeuroImage.

[35]  J. Rothwell,et al.  Cortical Connectivity , 2012, Springer Berlin Heidelberg.

[36]  Barbara G. Shinn-Cunningham,et al.  Short-Term Memory for Space and Time Flexibly Recruit Complementary Sensory-Biased Frontal Lobe Attention Networks , 2015, Neuron.

[37]  Steen Moeller,et al.  ICA-based artefact removal and accelerated fMRI acquisition for improved resting state network imaging , 2014, NeuroImage.

[38]  Essa Yacoub,et al.  The WU-Minn Human Connectome Project: An overview , 2013, NeuroImage.

[39]  Asaid Khateb,et al.  Group analysis and the subject factor in functional magnetic resonance imaging: Analysis of fifty right‐handed healthy subjects in a semantic language task , 2008, Human brain mapping.

[40]  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.

[41]  Mark Jenkinson,et al.  The minimal preprocessing pipelines for the Human Connectome Project , 2013, NeuroImage.

[42]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[43]  Timothy O. Laumann,et al.  Methods to detect, characterize, and remove motion artifact in resting state fMRI , 2014, NeuroImage.

[44]  M. Chun,et al.  Functional connectome fingerprinting: Identifying individuals based on patterns of brain connectivity , 2015, Nature Neuroscience.

[45]  Rodrigo M. Braga,et al.  Auditory and visual connectivity gradients in frontoparietal cortex , 2016, Human brain mapping.

[46]  E. Koechlin,et al.  The Architecture of Cognitive Control in the Human Prefrontal Cortex , 2003, Science.

[47]  D. H. Warren,et al.  Immediate perceptual response to intersensory discrepancy. , 1980, Psychological bulletin.

[48]  Stephen M. Smith,et al.  Multi-level block permutation , 2015, NeuroImage.

[49]  Robert J. Zatorre,et al.  Neural substrates for dividing and focusing attention between simultaneous auditory and visual events , 2006, NeuroImage.

[50]  Nancy Kanwisher,et al.  Broad domain generality in focal regions of frontal and parietal cortex , 2013, Proceedings of the National Academy of Sciences.

[51]  M. Fox,et al.  Individual Variability in Functional Connectivity Architecture of the Human Brain , 2013, Neuron.

[52]  Lizabeth M Romanski,et al.  Representation and integration of auditory and visual stimuli in the primate ventral lateral prefrontal cortex. , 2007, Cerebral cortex.

[53]  Abraham Z. Snyder,et al.  Function in the human connectome: Task-fMRI and individual differences in behavior , 2013, NeuroImage.

[54]  James A. Brissenden,et al.  Functional Evidence for a Cerebellar Node of the Dorsal Attention Network , 2016, The Journal of Neuroscience.

[55]  M. D’Esposito,et al.  Is the rostro-caudal axis of the frontal lobe hierarchical? , 2009, Nature Reviews Neuroscience.

[56]  Christopher L Asplund,et al.  Amodal Processing in Human Prefrontal Cortex , 2013, The Journal of Neuroscience.

[57]  P. Goldman-Rakic,et al.  An auditory domain in primate prefrontal cortex , 2002, Nature Neuroscience.

[58]  Stephen M. Smith,et al.  Permutation inference for the general linear model , 2014, NeuroImage.

[59]  L. Romanski Integration of faces and vocalizations in ventral prefrontal cortex: Implications for the evolution of audiovisual speech , 2012, Proceedings of the National Academy of Sciences.

[60]  Steen Moeller,et al.  Advances in diffusion MRI acquisition and processing in the Human Connectome Project , 2013, NeuroImage.

[61]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[62]  D. V. van Essen,et al.  Mapping Human Cortical Areas In Vivo Based on Myelin Content as Revealed by T1- and T2-Weighted MRI , 2011, The Journal of Neuroscience.

[63]  Fred L. Steinberg,et al.  Functional MRI reveals the existence of modality and coordination-dependent timing networks , 2005, NeuroImage.

[64]  Evelina Fedorenko The role of domain-general cognitive control in language comprehension , 2014, Front. Psychol..