Attention reorganizes connectivity across networks in a frequency specific manner

ABSTRACT Attention allows our brain to focus its limited resources on a given task. It does so by selective modulation of neural activity and of functional connectivity (FC) across brain‐wide networks. While there is extensive literature on activity changes, surprisingly few studies examined brain‐wide FC modulations that can be cleanly attributed to attention compared to matched visual processing. In contrast to prior approaches, we used an ultra‐long trial design that avoided transients from trial onsets, included slow fluctuations (<0.1 Hz) that carry important information on FC, and allowed for frequency‐segregated analyses. We found that FC derived from long blocks had a nearly two‐fold higher gain compared to FC derived from traditional (short) block designs. Second, attention enhanced intrinsic (negative or positive) correlations across networks, such as between the default‐mode network (DMN), the dorsal attention network (DAN), and the visual system (VIS). In contrast attention de‐correlated the intrinsically correlated visual regions. Third, the de‐correlation within VIS was driven primarily by high frequencies, whereas the increase in DAN‐VIS predominantly by low frequencies. These results pinpoint two fundamentally distinct effects of attention on connectivity. Information flow increases between distinct large‐scale networks, and de‐correlation within sensory cortex indicates decreased redundancy. HIGHLIGHTSAttention paradigm with ultra‐long trials of 2 min and matched vision control.Ultra‐long trials increased connectivity two‐fold compared to 20 s trials.Attention, compared to matched visual stimulation, de‐correlated visual cortex.Visual de‐correlation mediated by high frequencies, other connections by all bands.Results suggest reorganization of connections by attention is frequency specific.

[1]  Karl J. Friston,et al.  Frontiers in Systems Neuroscience Systems Neuroscience the Temporal Structure of Ongoing Brain Activity , 2022 .

[2]  P. Fries.  Rhythms for Cognition: Communication through Coherence , 2015, Neuron.

[3]  N. Kanwisher,et al.  Visual attention: Insights from brain imaging , 2000, Nature Reviews Neuroscience.

[4]  S. Rombouts,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[5]  I. Fried,et al.  Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex , 2008, Nature Neuroscience.

[6]  Á. Pascual-Leone,et al.  α-Band Electroencephalographic Activity over Occipital Cortex Indexes Visuospatial Attention Bias and Predicts Visual Target Detection , 2006, The Journal of Neuroscience.

[7]  Mark D'Esposito,et al.  Top-down flow of visual spatial attention signals from parietal to occipital cortex. , 2009, Journal of vision.

[8]  R. Malach,et al.  Data-driven clustering reveals a fundamental subdivision of the human cortex into two global systems , 2008, Neuropsychologia.

[9]  Sepideh Sadaghiani,et al.  Ongoing dynamics in large-scale functional connectivity predict perception , 2015, Proceedings of the National Academy of Sciences.

[10]  Yihong Yang,et al.  Frequency specificity of functional connectivity in brain networks , 2008, NeuroImage.

[11]  Peter Dayan,et al.  A Probabilistic Palimpsest Model of Visual Short-term Memory , 2015, PLoS Comput. Biol..

[12]  Christopher J. Fox,et al.  Defining the face processing network: Optimization of the functional localizer in fMRI , 2009, Human brain mapping.

[13]  E. Wojciulik,et al.  Attention increases neural selectivity in the human lateral occipital complex , 2004, Nature Neuroscience.

[14]  Maxime Descoteaux,et al.  Regional variations in vascular density correlate with resting‐state and task‐evoked blood oxygen level‐dependent signal amplitude , 2014, Human brain mapping.

[15]  Jude F. Mitchell,et al.  Spatial Attention Decorrelates Intrinsic Activity Fluctuations in Macaque Area V4 , 2009, Neuron.

[16]  W. Singer,et al.  Hemodynamic Signals Correlate Tightly with Synchronized Gamma Oscillations , 2005, Science.

[17]  Christopher P. Said,et al.  Top-down attention switches coupling between low-level and high-level areas of human visual cortex , 2012, Proceedings of the National Academy of Sciences.

[18]  B T Thomas Yeo,et al.  Reconfigurable task-dependent functional coupling modes cluster around a core functional architecture , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[19]  M. Schölvinck,et al.  Neural basis of global resting-state fMRI activity , 2010, Proceedings of the National Academy of Sciences.

[20]  Leslie G. Ungerleider,et al.  Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. , 1998, Science.

[21]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[22]  Rachel A Robbins,et al.  A Review and Clarification of the Terms “holistic,” “configural,” and “relational” in the Face Perception Literature , 2012, Front. Psychology.

[23]  Hang Joon Jo,et al.  Trouble at Rest: How Correlation Patterns and Group Differences Become Distorted After Global Signal Regression , 2012, Brain Connect..

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

[25]  Jonathan D. Power,et al.  Intrinsic and Task-Evoked Network Architectures of the Human Brain , 2014, Neuron.

[26]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

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

[28]  Edward T. Bullmore,et al.  A simple view of the brain through a frequency-specific functional connectivity measure , 2008, NeuroImage.

[29]  Stefan Treue,et al.  Feature-based attention influences motion processing gain in macaque visual cortex , 1999, Nature.

[30]  S. Dalal,et al.  Prestimulus Oscillatory Phase at 7 Hz Gates Cortical Information Flow and Visual Perception , 2013, Current Biology.

[31]  Keiji Tanaka,et al.  Human Ocular Dominance Columns as Revealed by High-Field Functional Magnetic Resonance Imaging , 2001, Neuron.

[32]  R. Nathan Spreng,et al.  The Fallacy of a “Task-Negative” Network , 2012, Front. Psychology.

[33]  Sharon L. Thompson-Schill,et al.  A Functional Cartography of Cognitive Systems , 2015, PLoS Comput. Biol..

[34]  H. Spitzer,et al.  Increased attention enhances both behavioral and neuronal performance. , 1988, Science.

[35]  Viviana Betti,et al.  Natural Scenes Viewing Alters the Dynamics of Functional Connectivity in the Human Brain , 2013, Neuron.

[36]  Ivan N Pigarev,et al.  Neural Mechanisms of Visual Attention: How Top-Down Feedback Highlights Relevant Locations , 2007, Science.

[37]  V. Haughton,et al.  Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. , 2001, AJNR. American journal of neuroradiology.

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

[39]  N. Logothetis,et al.  Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. , 2003, Cerebral cortex.

[40]  Cleofé Peña-Gómez,et al.  Brain connectivity during resting state and subsequent working memory task predicts behavioural performance , 2012, Cortex.

[41]  Andreas Bartels,et al.  Brain dynamics during natural viewing conditions—A new guide for mapping connectivity in vivo , 2005, NeuroImage.

[42]  J. Pillai.  Functional Connectivity. , 2017, Neuroimaging clinics of North America.

[43]  H. Kennedy,et al.  Visual Areas Exert Feedforward and Feedback Influences through Distinct Frequency Channels , 2014, Neuron.

[44]  Bharat B. Biswal,et al.  Competition between functional brain networks mediates behavioral variability , 2008, NeuroImage.

[45]  Amanda Elton,et al.  Divergent task-dependent functional connectivity of executive control and salience networks , 2014, Cortex.

[46]  K. Kiehl,et al.  Removal of Confounding Effects of Global Signal in Functional MRI Analyses , 2001, NeuroImage.

[47]  Archana Venkataraman,et al.  Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. , 2010, Journal of neurophysiology.

[48]  Laura C. Buchanan,et al.  Tracking ongoing cognition in individuals using brief, whole-brain functional connectivity patterns , 2015, Proceedings of the National Academy of Sciences.

[49]  J. Maunsell,et al.  Attention improves performance primarily by reducing interneuronal correlations , 2009, Nature Neuroscience.

[50]  M. Russell Harter,et al.  Effects of attention and arousal on visually evoked cortical potentials and reaction time in man , 1969 .

[51]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[52]  A. Mizuno,et al.  A change of the leading player in flow Visualization technique , 2006, J. Vis..

[53]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Viviana Betti,et al.  Dynamic reorganization of human resting-state networks during visuospatial attention , 2015, Proceedings of the National Academy of Sciences.

[55]  Louise S. Delicato,et al.  Acetylcholine contributes through muscarinic receptors to attentional modulation in V1 , 2008, Nature.

[56]  Geraint Rees,et al.  Attentional integration between anatomically distinct stimulus representations in early visual cortex. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[57]  R. Oostenveld,et al.  Neuronal Dynamics Underlying High- and Low-Frequency EEG Oscillations Contribute Independently to the Human BOLD Signal , 2011, Neuron.

[58]  Kristina M. Visscher,et al.  The neural bases of momentary lapses in attention , 2006, Nature Neuroscience.

[59]  I. Fried,et al.  Coupling between Neuronal Firing Rate, Gamma LFP, and BOLD fMRI Is Related to Interneuronal Correlations , 2007, Current Biology.

[60]  A. Engel,et al.  Neuronal Synchronization along the Dorsal Visual Pathway Reflects the Focus of Spatial Attention , 2008, Neuron.

[61]  Karl J. Friston,et al.  Attentional modulation of effective connectivity from V2 to V5/MT in humans. , 2000, Proceedings of the National Academy of Sciences of the United States of America.