Big Words, Halved Brains and Small Worlds: Complex Brain Networks of Figurative Language Comprehension

Language comprehension is a complex task that involves a wide network of brain regions. We used topological measures to qualify and quantify the functional connectivity of the networks used under various comprehension conditions. To that aim we developed a technique to represent functional networks based on EEG recordings, taking advantage of their excellent time resolution in order to capture the fast processes that occur during language comprehension. Networks were created by searching for a specific causal relation between areas, the negative feedback loop, which is ubiquitous in many systems. This method is a simple way to construct directed graphs using event-related activity, which can then be analyzed topologically. Brain activity was recorded while subjects read expressions of various types and indicated whether they found them meaningful. Slightly different functional networks were obtained for event-related activity evoked by each expression type. The differences reflect the special contribution of specific regions in each condition and the balance of hemispheric activity involved in comprehending different types of expressions and are consistent with the literature in the field. Our results indicate that representing event-related brain activity as a network using a simple temporal relation, such as the negative feedback loop, to indicate directional connectivity is a viable option for investigation which also derives new information about aspects not reflected in the classical methods for investigating brain activity.

[1]  Sandeep Krishna,et al.  Oscillation patterns in negative feedback loops , 2006, Proceedings of the National Academy of Sciences.

[2]  C. J. Stam,et al.  Functional connectivity patterns of human magnetoencephalographic recordings: a ‘small-world’ network? , 2004, Neuroscience Letters.

[3]  Karl J. Friston,et al.  Dynamic causal modeling , 2010, Scholarpedia.

[4]  Abraham Goldstein,et al.  Dynamics of hemispheric activity during metaphor comprehension: Electrophysiological measures , 2007, NeuroImage.

[5]  S. Bressler,et al.  Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Richard S. J. Frackowiak,et al.  The anatomy of phonological and semantic processing in normal subjects. , 1992, Brain : a journal of neurology.

[7]  K. Sneppen,et al.  Minimal model of spiky oscillations in NF-κB signaling , 2006 .

[8]  M. Jung-Beeman Bilateral brain processes for comprehending natural language , 2005, Trends in Cognitive Sciences.

[9]  Martin Suter,et al.  Small World , 2002 .

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

[11]  G Tononi,et al.  Theoretical neuroanatomy: relating anatomical and functional connectivity in graphs and cortical connection matrices. , 2000, Cerebral cortex.

[12]  Stanley Wasserman,et al.  Social Network Analysis: Methods and Applications , 1994, Structural analysis in the social sciences.

[13]  D. Lehmann,et al.  Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[14]  Edward T. Bullmore,et al.  Efficiency and Cost of Economical Brain Functional Networks , 2007, PLoS Comput. Biol..

[15]  Albert-László Barabási,et al.  Statistical mechanics of complex networks , 2001, ArXiv.

[16]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[17]  A. Goldstein,et al.  Brainwaves are stethoscopes: ERP correlates of novel metaphor comprehension , 2007, Brain Research.

[18]  Evelyn C. Ferstl,et al.  The extended language network: A meta‐analysis of neuroimaging studies on text comprehension , 2008, Human brain mapping.

[19]  Roberto D. Pascual-Marqui,et al.  Functional imaging with low resolution brain electromagnetic tomography (LORETA) : review, new comparisons, and new validation , 2002 .

[20]  Yoram Louzoun,et al.  Self-emergence of knowledge trees: extraction of the Wikipedia hierarchies. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[21]  D. Fell,et al.  The small world inside large metabolic networks , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[22]  Katherine P. Rankin,et al.  Detecting sarcasm from paralinguistic cues: Anatomic and cognitive correlates in neurodegenerative disease , 2009, NeuroImage.

[23]  Frank Harary,et al.  Graph Theory , 2016 .

[24]  B. Horwitz,et al.  Functional connectivity of the angular gyrus in normal reading and dyslexia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[26]  V. Ramachandran A Brief Tour of Human Consciousness: From Impostor Poodles to Purple Numbers , 2004 .

[27]  E. Ross,et al.  Neurology of affective prosody and its functional–anatomic organization in right hemisphere , 2008, Brain and Language.

[28]  M. Kutas,et al.  Semantic integration in reading: engagement of the right hemisphere during discourse processing. , 1999, Brain : a journal of neurology.

[29]  O. Sporns,et al.  Organization, development and function of complex brain networks , 2004, Trends in Cognitive Sciences.

[30]  T. Hendler,et al.  An fMRI investigation of the neural correlates underlying the processing of novel metaphoric expressions , 2007, Brain and Language.

[31]  G. Chartrand,et al.  Graphs & Digraphs , 1986 .

[32]  David Luck,et al.  The right parahippocampal gyrus contributes to the formation and maintenance of bound information in working memory , 2010, Brain and Cognition.

[33]  Karl Magnus Petersson,et al.  The role of precuneus and left inferior frontal cortex during source memory episodic retrieval , 2005, NeuroImage.

[34]  Remco J. Renken,et al.  Semantic ambiguity processing in sentence context: Evidence from event-related fMRI , 2007, NeuroImage.

[35]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[36]  El Houssine Snoussi Necessary Conditions for Multistationarity and Stable Periodicity , 1998 .

[37]  T. Hendler,et al.  The role of the right hemisphere in processing nonsalient metaphorical meanings: Application of Principal Components Analysis to fMRI data , 2005, Neuropsychologia.

[38]  Colin M. Brown,et al.  The Neural Circuitry Involved in the Reading of German Words and Pseudowords: A PET Study , 1999, Journal of Cognitive Neuroscience.

[39]  A. Goldbeter,et al.  Modeling the mammalian circadian clock: sensitivity analysis and multiplicity of oscillatory mechanisms. , 2004, Journal of Theoretical Biology.

[40]  Carol A. Seger,et al.  Neural correlates of metaphor processing: The roles of figurativeness, familiarity and difficulty , 2009, Brain and Cognition.

[41]  R. Pascual-Marqui Review of methods for solving the EEG inverse problem , 1999 .

[42]  E. Bullmore,et al.  A Resilient, Low-Frequency, Small-World Human Brain Functional Network with Highly Connected Association Cortical Hubs , 2006, The Journal of Neuroscience.

[43]  Danielle Smith Bassett,et al.  Small-World Brain Networks , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[44]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[45]  Kim Sneppen,et al.  Minimal model of spiky oscillations in NF-kappaB signaling. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Xin-She Yang,et al.  Small‐world networks in geophysics , 2001, 1003.4886.