The global landscape of cognition: hierarchical aggregation as an organizational principle of human cortical networks and functions

Though widely hypothesized, limited evidence exists that human brain functions organize in global gradients of abstraction starting from sensory cortical inputs. Hierarchical representation is accepted in computational networks, and tentatively in visual neuroscience, yet no direct holistic demonstrations exist in vivo. Our methods developed network models enriched with tiered directionality, by including input locations, a critical feature for localizing representation in networks generally. Grouped primary sensory cortices defined network inputs, displaying global connectivity to fused inputs. Depth-oriented networks guided analyses of fMRI databases (~17,000 experiments;~1/4 of fMRI literature). Formally, we tested whether network depth predicted localization of abstract versus concrete behaviors over the whole set of studied brain regions. For our results, new cortical graph metrics, termed network-depth, ranked all databased cognitive function activations by network-depth. Thus, we objectively sorted stratified landscapes of cognition, starting from grouped sensory inputs in parallel, progressing deeper into cortex. This exposed escalating amalgamation of function or abstraction with increasing network-depth, globally. Nearly 500 new participants confirmed our results. In conclusion, data-driven analyses defined a hierarchically ordered connectome, revealing a related continuum of cognitive function. Progressive functional abstraction over network depth may be a fundamental feature of brains, and is observed in artificial networks.

[1]  David J. C. MacKay,et al.  Information Theory, Inference, and Learning Algorithms , 2004, IEEE Transactions on Information Theory.

[2]  Danilo Bzdok,et al.  The BrainMap strategy for standardization, sharing, and meta-analysis of neuroimaging data , 2011, BMC Research Notes.

[3]  Janina Seubert,et al.  Statistical localization of human olfactory cortex , 2013, NeuroImage.

[4]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[5]  Angela R. Laird,et al.  Comparison of the disparity between Talairach and MNI coordinates in functional neuroimaging data: Validation of the Lancaster transform , 2010, NeuroImage.

[6]  Simon B. Eickhoff,et al.  Meta-analytical definition and functional connectivity of the human vestibular cortex , 2012, NeuroImage.

[7]  A. Treisman,et al.  A feature-integration theory of attention , 1980, Cognitive Psychology.

[8]  Johan N Lundström,et al.  Identification of human gustatory cortex by activation likelihood estimation , 2011, Human brain mapping.

[9]  Honglak Lee,et al.  Convolutional deep belief networks for scalable unsupervised learning of hierarchical representations , 2009, ICML '09.

[10]  T. Brandt,et al.  Dominance for vestibular cortical function in the non-dominant hemisphere. , 2003, Cerebral cortex.

[11]  Russell A. Poldrack,et al.  Large-scale automated synthesis of human functional neuroimaging data , 2011, Nature Methods.

[12]  Shlomo Bentin,et al.  Local or Global? , 2010, Psychological science.

[13]  Karl J. Friston,et al.  Anterior insular cortex and emotional awareness , 2013, The Journal of comparative neurology.

[14]  Timothy E. J. Behrens,et al.  What is the most interesting part of the brain? , 2013, Trends in Cognitive Sciences.

[15]  David H. Zald,et al.  On the scent of human olfactory orbitofrontal cortex: Meta-analysis and comparison to non-human primates , 2005, Brain Research Reviews.

[16]  J C Mazziotta,et al.  Automated labeling of the human brain: A preliminary report on the development and evaluation of a forward‐transform method , 1997, Human brain mapping.

[17]  F. Pulvermüller How neurons make meaning: brain mechanisms for embodied and abstract-symbolic semantics , 2013, Trends in Cognitive Sciences.

[18]  Edward T. Bullmore,et al.  Neuroinformatics Original Research Article , 2022 .

[19]  Bernard J. Baars,et al.  Global Workspace Dynamics: Cortical “Binding and Propagation” Enables Conscious Contents , 2013, Front. Psychol..

[20]  B. T. Thomas Yeo,et al.  The Organization of Local and Distant Functional Connectivity in the Human Brain , 2010, PLoS Comput. Biol..

[21]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

[22]  S. Hochstein,et al.  View from the Top Hierarchies and Reverse Hierarchies in the Visual System , 2002, Neuron.

[23]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[24]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[25]  Michael J. Martinez,et al.  Bias between MNI and Talairach coordinates analyzed using the ICBM‐152 brain template , 2007, Human brain mapping.

[26]  G. Deco,et al.  A hierarchical neural system with attentional top–down enhancement of the spatial resolution for object recognition , 2000, Vision Research.

[27]  Jessica A. Turner,et al.  Behavioral Interpretations of Intrinsic Connectivity Networks , 2011, Journal of Cognitive Neuroscience.

[28]  S. Dehaene,et al.  A Hierarchy of Responses to Auditory Regularities in the Macaque Brain , 2014, The Journal of Neuroscience.

[29]  Thomas Serre,et al.  A quantitative theory of immediate visual recognition. , 2007, Progress in brain research.

[30]  César A. Hidalgo,et al.  The Product Space Conditions the Development of Nations , 2007, Science.

[31]  Heiko Wersing,et al.  Learning Optimized Features for Hierarchical Models of Invariant Object Recognition , 2003, Neural Computation.

[32]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[33]  R Cameron Craddock,et al.  A whole brain fMRI atlas generated via spatially constrained spectral clustering , 2012, Human brain mapping.

[34]  O. Sporns,et al.  Rich-Club Organization of the Human Connectome , 2011, The Journal of Neuroscience.

[35]  R. W. Stowe,et al.  Context availability and lexical decisions for abstract and concrete words , 1988 .

[36]  P. Fox,et al.  Mapping context and content: the BrainMap model , 2002, Nature Reviews Neuroscience.

[37]  Margaret D. King,et al.  The NKI-Rockland Sample: A Model for Accelerating the Pace of Discovery Science in Psychiatry , 2012, Front. Neurosci..

[38]  Michael Wilson MRC Psycholinguistic Database , 2001 .

[39]  Yaroslav O. Halchenko,et al.  Open is Not Enough. Let's Take the Next Step: An Integrated, Community-Driven Computing Platform for Neuroscience , 2012, Front. Neuroinform..

[40]  Timothy O. Laumann,et al.  Informatics and Data Mining Tools and Strategies for the Human Connectome Project , 2011, Front. Neuroinform..

[41]  P. Schlindwein,et al.  Neural correlates of hemispheric dominance and ipsilaterality within the vestibularsystem , 2008, NeuroImage.

[42]  Keith A. Johnson,et al.  Cortical Hubs Revealed by Intrinsic Functional Connectivity: Mapping, Assessment of Stability, and Relation to Alzheimer's Disease , 2009, The Journal of Neuroscience.

[43]  G. Westbrook,et al.  Hierarchical excitatory synaptic connectivity in mouse olfactory cortex , 2013, Proceedings of the National Academy of Sciences.

[44]  Timothée Masquelier,et al.  Unsupervised Learning of Visual Features through Spike Timing Dependent Plasticity , 2007, PLoS Comput. Biol..

[45]  Tatsu Kobayakawa,et al.  Laterality of human primary gustatory cortex studied by MEG. , 2005, Chemical senses.

[46]  Nobuyuki Sakai,et al.  Location of the primary gustatory area in humans and its properties, studied by magnetoencephalography. , 2005, Chemical senses.

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

[48]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[49]  E. Rolls,et al.  A Neurodynamical cortical model of visual attention and invariant object recognition , 2004, Vision Research.

[50]  Hans-Jochen Heinze,et al.  The Neural Site of Attention Matches the Spatial Scale of Perception , 2006, The Journal of Neuroscience.

[51]  Angela R Laird,et al.  Brainmap taxonomy of experimental design: Description and evaluation , 2005, Human brain mapping.

[52]  Fabrice Bartolomei,et al.  Electrical stimulation of a small brain area reversibly disrupts consciousness , 2014, Epilepsy & Behavior.

[53]  Geoffrey E. Hinton Learning multiple layers of representation , 2007, Trends in Cognitive Sciences.

[54]  Mark A. Chevillet,et al.  Functional Correlates of the Anterolateral Processing Hierarchy in Human Auditory Cortex , 2011, The Journal of Neuroscience.

[55]  Timothy S. Coalson,et al.  Parcellations and hemispheric asymmetries of human cerebral cortex analyzed on surface-based atlases. , 2012, Cerebral cortex.

[56]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[57]  G. Edelman,et al.  Biology of Consciousness , 2010, Front. Psychology.

[58]  Amy Beth Warriner,et al.  Concreteness ratings for 40 thousand generally known English word lemmas , 2014, Behavior research methods.

[59]  Cedric E. Ginestet,et al.  Cognitive relevance of the community structure of the human brain functional coactivation network , 2013, Proceedings of the National Academy of Sciences.

[60]  Angela R. Laird,et al.  BrainMap , 2007, Neuroinformatics.

[61]  T. Poggio,et al.  Cognitive neuroscience: Neural mechanisms for the recognition of biological movements , 2003, Nature Reviews Neuroscience.

[62]  F. Mast,et al.  The human vestibular cortex revealed by coordinate-based activation likelihood estimation meta-analysis , 2012, Neuroscience.

[63]  K. Zilles,et al.  A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis , 2010, Brain Structure and Function.

[64]  M. V. D. Heuvel,et al.  Exploring the brain network: A review on resting-state fMRI functional connectivity , 2010, European Neuropsychopharmacology.

[65]  C. Koch,et al.  Invariant visual representation by single neurons in the human brain , 2005, Nature.

[66]  CM Bennett,et al.  Neural correlates of interspecies perspective taking in the post-mortem Atlantic Salmon: an argument for multiple comparisons correction , 2009, NeuroImage.

[67]  P. Haggard,et al.  Neural signatures of body ownership: a sensory network for bodily self-consciousness. , 2007, Cerebral cortex.

[68]  Gustavo Deco,et al.  A Neurodynamical Model of Visual Attention: Feedback Enhancement of Spatial Resolution in a Hierarchical System , 2001, Journal of Computational Neuroscience.

[69]  S. Ullman Object recognition and segmentation by a fragment-based hierarchy , 2007, Trends in Cognitive Sciences.

[70]  C. Koch,et al.  What is the function of the claustrum? , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.