Combining Functional and Anatomical Connectivity Reveals Brain Networks for Auditory Language Comprehension

Cognitive functions are organized in distributed, overlapping, and interacting brain networks. Investigation of those large-scale brain networks is a major task in neuroimaging research. Here, we introduce a novel combination of functional and anatomical connectivity to study the network topology subserving a cognitive function of interest. (i) In a given network, direct interactions between network nodes are identified by analyzing functional MRI time series with the multivariate method of directed partial correlation (dPC). This method provides important improvements over shortcomings that are typical for ordinary (partial) correlation techniques. (ii) For directly interacting pairs of nodes, a region-to-region probabilistic fiber tracking on diffusion tensor imaging data is performed to identify the most probable anatomical white matter fiber tracts mediating the functional interactions. This combined approach is applied to the language domain to investigate the network topology of two levels of auditory comprehension: lower-level speech perception (i.e., phonological processing) and higher-level speech recognition (i.e., semantic processing). For both processing levels, dPC analyses revealed the functional network topology and identified central network nodes by the number of direct interactions with other nodes. Tractography showed that these interactions are mediated by distinct ventral (via the extreme capsule) and dorsal (via the arcuate/superior longitudinal fascicle fiber system) long- and short-distance association tracts as well as commissural fibers. Our findings demonstrate how both processing routines are segregated in the brain on a large-scale network level. Combining dPC with probabilistic tractography is a promising approach to unveil how cognitive functions emerge through interaction of functionally interacting and anatomically interconnected brain regions.

[1]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

[2]  Mingzhou Ding,et al.  Analyzing information flow in brain networks with nonparametric Granger causality , 2008, NeuroImage.

[3]  Matthew H. Davis,et al.  The neural mechanisms of speech comprehension: fMRI studies of semantic ambiguity. , 2005, Cerebral cortex.

[4]  Matthew A. Lambon Ralph,et al.  Lateralization of ventral and dorsal auditory-language pathways in the human brain , 2005, NeuroImage.

[5]  Karl J. Friston,et al.  Dissociating Reading Processes on the Basis of Neuronal Interactions , 2005, Journal of Cognitive Neuroscience.

[6]  L. Aravind,et al.  Integration of Word Meaning and World Knowledge in Language Comprehension , 2022 .

[7]  D. LeBihan,et al.  Phonological Grammar Shapes the Auditory Cortex: A Functional Magnetic Resonance Imaging Study , 2003, The Journal of Neuroscience.

[8]  Michael Eichler,et al.  A graphical approach for evaluating effective connectivity in neural systems , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[9]  Rainer Goebel,et al.  Mapping directed influence over the brain using Granger causality and fMRI , 2005, NeuroImage.

[10]  P. Skudlarski,et al.  Detection of functional connectivity using temporal correlations in MR images , 2002, Human brain mapping.

[11]  Colin Humphries,et al.  Role of left posterior superior temporal gyrus in phonological processing for speech perception and production , 2001, Cogn. Sci..

[12]  Sophie K. Scott,et al.  The functional neuroanatomy of prelexical processing in speech perception , 2004, Cognition.

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

[14]  P. Basser,et al.  Estimation of the effective self-diffusion tensor from the NMR spin echo. , 1994, Journal of magnetic resonance. Series B.

[15]  Volkmar Glauche,et al.  Ventral and dorsal pathways for language , 2008, Proceedings of the National Academy of Sciences.

[16]  Lee M. Miller,et al.  Measuring interregional functional connectivity using coherence and partial coherence analyses of fMRI data , 2004, NeuroImage.

[17]  Hao Huang,et al.  DTI tractography based parcellation of white matter: Application to the mid-sagittal morphology of corpus callosum , 2005, NeuroImage.

[18]  A. Liberman,et al.  On the relation of speech to language , 2000, Trends in Cognitive Sciences.

[19]  S. Bookheimer,et al.  Form and Content Dissociating Syntax and Semantics in Sentence Comprehension , 1999, Neuron.

[20]  P. Lang,et al.  Re‐entrant projections modulate visual cortex in affective perception: Evidence from Granger causality analysis , 2009, Human brain mapping.

[21]  Bernard Mazoyer,et al.  Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing , 2006, NeuroImage.

[22]  M. D’Esposito,et al.  A comparison of Granger causality and coherency in fMRI‐based analysis of the motor system , 2009, Human brain mapping.

[23]  Friedemann Pulvermüller,et al.  Spatiotemporal dynamics of neural language processing: an MEG study using minimum-norm current estimates , 2003, NeuroImage.

[24]  V. Kiselev,et al.  Gibbs tracking: A novel approach for the reconstruction of neuronal pathways , 2008, Magnetic resonance in medicine.

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

[26]  R. Wise,et al.  Temporal lobe regions engaged during normal speech comprehension. , 2003, Brain : a journal of neurology.

[27]  Klaas Enno Stephan,et al.  On the role of general system theory for functional neuroimaging , 2004, Journal of anatomy.

[28]  M Zaitsev,et al.  Point spread function mapping with parallel imaging techniques and high acceleration factors: Fast, robust, and flexible method for echo‐planar imaging distortion correction , 2004, Magnetic resonance in medicine.

[29]  K. Amunts,et al.  Effective connectivity of the left BA 44, BA 45, and inferior temporal gyrus during lexical and phonological decisions identified with DCM , 2009, Human brain mapping.

[30]  D. Poeppel,et al.  Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language , 2004, Cognition.

[31]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[32]  Stephen E. Nadeau,et al.  Phonology: A Review and Proposals from a Connectionist Perspective , 2001, Brain and Language.

[33]  Paul C. Locasto,et al.  A systematic investigation of the functional neuroanatomy of auditory and visual phonological processing , 2005, NeuroImage.

[34]  G. Thierry,et al.  Renewal of the neurophysiology of language: functional neuroimaging. , 2005, Physiological reviews.

[35]  B.W. Kreher,et al.  Connecting and merging fibres: Pathway extraction by combining probability maps , 2008, NeuroImage.

[36]  C. Granger Investigating causal relations by econometric models and cross-spectral methods , 1969 .

[37]  Jennifer S. W. Campbell,et al.  Dissociating the Human Language Pathways with High Angular Resolution Diffusion Fiber Tractography , 2008, The Journal of Neuroscience.

[38]  R. Woods,et al.  Recovery from wernicke's aphasia: A positron emission tomographic study , 1995, Annals of neurology.

[39]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

[40]  C. Weiller,et al.  Dynamics of language reorganization after stroke. , 2006, Brain : a journal of neurology.

[41]  James L. McClelland,et al.  Semantic Cognition: A Parallel Distributed Processing Approach , 2004 .

[42]  Karl J. Friston,et al.  The Cortical Dynamics of Intelligible Speech , 2008, The Journal of Neuroscience.

[43]  James L. McClelland,et al.  The parallel distributed processing approach to semantic cognition , 2003, Nature Reviews Neuroscience.

[44]  Eric E. Smith,et al.  Cerebral White Matter , 2008, Annals of the New York Academy of Sciences.

[45]  Karl J. Friston,et al.  Tractography-based priors for dynamic causal models , 2009, NeuroImage.

[46]  S. Scott,et al.  A physiological change in the homotopic cortex following left posterior temporal lobe infarction , 2002, Annals of neurology.

[47]  M. Mesulam,et al.  Shifts of Effective Connectivity within a Language Network during Rhyming and Spelling , 2005, The Journal of Neuroscience.

[48]  A. Anwander,et al.  The brain differentiates human and non-human grammars: Functional localization and structural connectivity , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Volkmar Glauche,et al.  On the Detection of Direct Directed Information Flow in fMRI , 2008, IEEE Journal of Selected Topics in Signal Processing.

[50]  Luiz A. Baccalá,et al.  Partial directed coherence: a new concept in neural structure determination , 2001, Biological Cybernetics.

[51]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[52]  C. Price,et al.  Right anterior superior temporal activation predicts auditory sentence comprehension following aphasic stroke. , 2005, Brain : a journal of neurology.

[53]  D. Pandya,et al.  Fiber Pathways of the Brain , 2006 .

[54]  C. Granger Investigating Causal Relations by Econometric Models and Cross-Spectral Methods , 1969 .

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

[56]  Geoffrey J M Parker,et al.  A framework for a streamline‐based probabilistic index of connectivity (PICo) using a structural interpretation of MRI diffusion measurements , 2003, Journal of magnetic resonance imaging : JMRI.

[57]  E. Kaan,et al.  The brain circuitry of syntactic comprehension , 2002, Trends in Cognitive Sciences.