Personal experience with narrated events modulates functional connectivity within visual and motor systems during story comprehension

Past experience of everyday life activities, which forms the basis of our knowledge about the world, greatly affects how we understand stories. Yet, little is known about how this influence is instantiated in the human brain. Here, we used functional magnetic resonance imaging to investigate how past experience facilitates functional connectivity during the comprehension of stories rich in perceptual and motor details. We found that comprehenders' past experience with the scenes and actions described in the narratives selectively modulated functional connectivity between lower‐ and higher‐level areas within the neural systems for visual and motor processing, respectively. These intramodal interactions may play an important role in integrating personal knowledge about a narrated situation with an evolving discourse representation. This study provides empirical evidence consistent with the idea that regions related to visual and motor processing are involved in the reenactment of experience as proposed by theories of embodied cognition. Hum Brain Mapp 36:1494–1505, 2015. © 2014 Wiley Periodicals, Inc.

[1]  Melanie C. Green,et al.  Transportation Into Narrative Worlds: The Role of Prior Knowledge and Perceived Realism , 2004 .

[2]  P. Broek,et al.  The effects of prior knowledge and text structure on comprehension processes during reading of scientific texts , 2007, Memory & cognition.

[3]  F. Bartlett,et al.  Remembering: A Study in Experimental and Social Psychology , 1932 .

[4]  Rolf A. Zwaan,et al.  Situation models in language comprehension and memory. , 1998, Psychological bulletin.

[5]  Jeffrey M. Zacks,et al.  Reading Stories Activates Neural Representations of Visual and Motor Experiences , 2009, Psychological science.

[6]  Marcia K. Johnson,et al.  Contextual prerequisites for understanding: Some investigations of comprehension and recall , 1972 .

[7]  W. Kintsch.  Text comprehension, memory, and learning. , 1994, The American psychologist.

[8]  M. Corbetta,et al.  Learning sculpts the spontaneous activity of the resting human brain , 2009, Proceedings of the National Academy of Sciences.

[9]  Daniel Casasanto,et al.  Neural Dissociations between Action Verb Understanding and Motor Imagery , 2010, Journal of Cognitive Neuroscience.

[10]  C. Keysers,et al.  The Observation and Execution of Actions Share Motor and Somatosensory Voxels in all Tested Subjects: Single-Subject Analyses of Unsmoothed fMRI Data , 2008, Cerebral cortex.

[11]  L. Barsalou.  Situated simulation in the human conceptual system , 2003 .

[12]  Tülay Adali,et al.  Estimating the number of independent components for functional magnetic resonance imaging data , 2007, Human brain mapping.

[13]  Carson C. Chow,et al.  Repetition priming and repetition suppression: A case for enhanced efficiency through neural synchronization , 2012, Cognitive neuroscience.

[14]  Guido Gainotti,et al.  Mental representation of normal subjects about the sources of knowledge in different semantic categories and unique entities. , 2009, Neuropsychology.

[15]  Danielle S. McNamara,et al.  Learning from texts: Effects of prior knowledge and text coherence , 1996 .

[16]  E. Maguire,et al.  The functional neuroanatomy of comprehension and memory: the importance of prior knowledge. , 1999, Brain : a journal of neurology.

[17]  I. Johnsrude,et al.  Somatotopic Representation of Action Words in Human Motor and Premotor Cortex , 2004, Neuron.

[18]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[19]  Christine D. Wilson,et al.  Grounding conceptual knowledge in modality-specific systems , 2003, Trends in Cognitive Sciences.

[20]  Bradford Z. Mahon,et al.  CONSTRAINING QUESTIONS ABOUT THE ORGANISATION AND REPRESENTATION OF CONCEPTUAL KNOWLEDGE , 2003, Cognitive neuropsychology.

[21]  Daniel D. Dilks,et al.  Resting-State Neural Activity across Face-Selective Cortical Regions Is Behaviorally Relevant , 2011, The Journal of Neuroscience.

[22]  Leonardo Fogassi,et al.  Motor functions of the parietal lobe , 2005, Current Opinion in Neurobiology.

[23]  B. Bahrami,et al.  Coming of age: A review of embodiment and the neuroscience of semantics , 2012, Cortex.

[24]  Sian L. Beilock,et al.  The role of personal experience in the neural processing of action-related language , 2010, Brain and Language.

[25]  L. Barsalou.  Grounded cognition. , 2008, Annual review of psychology.

[26]  Paul van den Broek,et al.  Using Texts in Science Education: Cognitive Processes and Knowledge Representation , 2010 .

[27]  P. Johnson-Laird.  Mental models , 1989 .

[28]  K. Grill-Spector,et al.  The human visual cortex. , 2004, Annual review of neuroscience.

[29]  Clinton L. Johns,et al.  The importance of knowledge in vivid text memory: An individual-differences investigation of recollection and familiarity , 2008, Psychonomic bulletin & review.

[30]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[31]  T. Trabasso,et al.  Constructing inferences during narrative text comprehension. , 1994, Psychological review.

[32]  Allen R. Braun,et al.  Denoising the speaking brain: Toward a robust technique for correcting artifact-contaminated fMRI data under severe motion , 2014, NeuroImage.

[33]  C. Miniussi,et al.  The Functional Importance of Rhythmic Activity in the Brain , 2012, Current Biology.

[34]  Vittorio Gallese,et al.  Listening to Action-related Sentences Activates Fronto-parietal Motor Circuits , 2005, Journal of Cognitive Neuroscience.

[35]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[36]  Alfonso Caramazza,et al.  All Talk and No Action: A Transcranial Magnetic Stimulation Study of Motor Cortex Activation during Action Word Production , 2004, Journal of Cognitive Neuroscience.

[37]  Iris van Rooij,et al.  Hierarchies in Action and Motor Control , 2012, Journal of Cognitive Neuroscience.

[38]  Evelyn C. Ferstl,et al.  Emotional and Temporal Aspects of Situation Model Processing during Text Comprehension: An Event-Related fMRI Study , 2005, Journal of Cognitive Neuroscience.

[39]  Allen R. Braun,et al.  Neural correlates and network connectivity underlying narrative production and comprehension: A combined fMRI and PET study , 2014, Cortex.

[40]  A. Damasio.  Time-locked multiregional retroactivation: A systems-level proposal for the neural substrates of recall and recognition , 1989, Cognition.

[41]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[42]  Lynn C. Robertson,et al.  Functional Plasticity in Ventral Temporal Cortex following Cognitive Rehabilitation of a Congenital Prosopagnosic , 2007, Journal of Cognitive Neuroscience.

[43]  Thomas D Albright,et al.  On the Perception of Probable Things: Neural Substrates of Associative Memory, Imagery, and Perception , 2012, Neuron.

[44]  C. Caltagirone,et al.  The influence of rTMS over prefrontal and motor areas in a morphological task: Grammatical vs. semantic effects , 2008, Neuropsychologia.

[45]  P. Fries.  Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

[46]  Gereon R. Fink,et al.  Stimulus properties matter more than perspective: An fMRI study of mental imagery and silent reading of action phrases , 2007, NeuroImage.

[47]  Mark S. Seidenberg,et al.  Activation of sensory-motor areas in sentence comprehension. , 2010, Cerebral cortex.

[48]  Peter Hagoort,et al.  Beyond the sentence given , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[49]  Karl J. Friston.  Functional integration and inference in the brain , 2002, Progress in Neurobiology.

[50]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[51]  Russell A. Epstein.  Parahippocampal and retrosplenial contributions to human spatial navigation , 2008, Trends in Cognitive Sciences.

[52]  S. Larsen,et al.  Personal remindings while reading literature , 1988 .

[53]  K. McGraw,et al.  Forming inferences about some intraclass correlation coefficients. , 1996 .

[54]  S Makeig,et al.  Analysis of fMRI data by blind separation into independent spatial components , 1998, Human brain mapping.

[55]  W. Kintsch.  The role of knowledge in discourse comprehension: a construction-integration model. , 1988, Psychological review.

[56]  G. Riva,et al.  The effects of rTMS over the primary motor cortex: The link between action and language , 2013, Neuropsychologia.

[57]  Sian L. Beilock,et al.  Sports experience changes the neural processing of action language , 2008, Proceedings of the National Academy of Sciences.

[58]  J. R. Landis,et al.  The measurement of observer agreement for categorical data. , 1977, Biometrics.

[59]  Frank Van Overwalle,et al.  Understanding others' actions and goals by mirror and mentalizing systems: A meta-analysis , 2009, NeuroImage.

[60]  W. Schneider,et al.  Perceptual Knowledge Retrieval Activates Sensory Brain Regions , 2006, The Journal of Neuroscience.

[61]  J. Decety,et al.  Functional anatomy of execution, mental simulation, observation, and verb generation of actions: A meta‐analysis , 2001, Human brain mapping.

[62]  Dwight J. Kravitz,et al.  A new neural framework for visuospatial processing , 2011, Nature Reviews Neuroscience.

[63]  Xi-Nian Zuo,et al.  Resting-State Functional Connectivity Indexes Reading Competence in Children and Adults , 2011, The Journal of Neuroscience.

[64]  Siyuan Liu,et al.  Embodied Comprehension of Stories: Interactions between Language Regions and Modality-specific Neural Systems , 2014, Journal of Cognitive Neuroscience.

[65]  M. Corbetta,et al.  Individual variability in functional connectivity predicts performance of a perceptual task , 2012, Proceedings of the National Academy of Sciences.

[66]  Y. Kamitani,et al.  Regulation of Motor Representation by Phase–Amplitude Coupling in the Sensorimotor Cortex , 2012, The Journal of Neuroscience.

[67]  Rutvik H. Desai,et al.  The neurobiology of semantic memory , 2011, Trends in Cognitive Sciences.

[68]  Alex Martin,et al.  Semantic memory and the brain: structure and processes , 2001, Current Opinion in Neurobiology.

[69]  Jeremy Freeman,et al.  Inter-area correlations in the ventral visual pathway reflect feature integration. , 2010, Journal of vision.

[70]  S. Thompson-Schill.  Neuroimaging studies of semantic memory: inferring “how” from “where” , 2003, Neuropsychologia.

[71]  Lawrence W Barsalou,et al.  Simulation, situated conceptualization, and prediction , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[72]  Rocky Ross,et al.  Mental models , 2004, SIGA.