Effects of implied physical effort in sensory-motor and pre-frontal cortex during language comprehension

Embodied theories of conceptual knowledge suggest that sensory-motor representations of actions similar to those involved in the performance of the action described are recruited during language comprehension. The extent of this recruitment, however, and the brain mechanisms supporting this process remain unknown. Using fMRI, we investigated these issues by examining how people understand sentences that convey three different degrees of physical effort and by comparing this process to action execution. To understand the effort implied by the stimulus sentences, object and action properties associated with nouns and verbs respectively needed to be integrated: pushing the piano implies more physical effort than pushing the chair. Results indicated that a pre-motor region, which was also active in action execution, was sensitive to the degree of effort implied by the language. Interestingly, the anterior inferior frontal gyrus, a region typically associated with semantic processing, was not active in action execution but was nevertheless modulated by the effort implied. Inter-region correlations also suggested that this region was strongly correlated with pre-motor and posterior temporal regions. Overall, results suggest that (a) language understanding elicits action representations retaining a degree of specificity that was previously unsuspected, including unique properties of interactions with objects, and (b) these representations, which result from integrating the words' semantic information, may be computed within a collaborative neural network that includes the anterior inferior frontal gyrus.

[1]  Kenneth F. Valyear,et al.  Dissociating Arbitrary Stimulus-Response Mapping from Movement Planning during Preparatory Period: Evidence from Event-Related Functional Magnetic Resonance Imaging , 2006, The Journal of Neuroscience.

[2]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

[3]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[4]  J. Mazziotta,et al.  Functional segregation within pars opercularis of the inferior frontal gyrus: evidence from fMRI studies of imitation and action observation. , 2005, Cerebral cortex.

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

[6]  S. Dehaene,et al.  Topographical Layout of Hand, Eye, Calculation, and Language-Related Areas in the Human Parietal Lobe , 2002, Neuron.

[7]  J. Haxby,et al.  Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects , 1999, Nature Neuroscience.

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

[9]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[10]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[11]  U Noppeney,et al.  The neural areas that control the retrieval and selection of semantics , 2004, Neuropsychologia.

[12]  Karl J. Friston Functional and effective connectivity in neuroimaging: A synthesis , 1994 .

[13]  J. Fuster The Prefrontal Cortex—An Update Time Is of the Essence , 2001, Neuron.

[14]  Karl J. Friston,et al.  Action selectivity in parietal and temporal cortex. , 2005, Brain research. Cognitive brain research.

[15]  A. Damasio,et al.  Neural Correlates of Naming Actions and of Naming Spatial Relations , 2001, NeuroImage.

[16]  G. Rizzolatti,et al.  Congruent Embodied Representations for Visually Presented Actions and Linguistic Phrases Describing Actions , 2006, Current Biology.

[17]  Philippe A. Chouinard,et al.  Role of the Primary Motor and Dorsal Premotor Cortices in the Anticipation of Forces during Object Lifting , 2005, The Journal of Neuroscience.

[18]  G. Rizzolatti,et al.  The Organization of the Frontal Motor Cortex. , 2000, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[19]  H. Sakata,et al.  Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. , 2000, Journal of neurophysiology.

[20]  Lorraine K Tyler,et al.  Fronto-temporal brain systems supporting spoken language comprehension , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[21]  G. Rizzolatti,et al.  Listening to action-related sentences modulates the activity of the motor system: a combined TMS and behavioral study. , 2005, Brain research. Cognitive brain research.

[22]  Laurel J. Buxbaum,et al.  Deficient internal models for planning hand–object interactions in apraxia , 2005, Neuropsychologia.

[23]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

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

[25]  R. Hari,et al.  Temporal dynamics of cortical representation for action. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[26]  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.

[27]  N Makris,et al.  Location of lesions in stroke patients with deficits in syntactic processing in sentence comprehension. , 1996, Brain : a journal of neurology.

[28]  Anders M. Dale,et al.  N400-like Magnetoencephalography Responses Modulated by Semantic Context, Word Frequency, and Lexical Class in Sentences , 2002, NeuroImage.

[29]  Friedemann Pulvermüller,et al.  Brain Signatures of Meaning Access in Action Word Recognition , 2005, Journal of Cognitive Neuroscience.

[30]  Derek K. Jones,et al.  Virtual in Vivo Interactive Dissection of White Matter Fasciculi in the Human Brain , 2002, NeuroImage.

[31]  Abraham Z Snyder,et al.  Reliability of functional localization using fMRI , 2003, NeuroImage.

[32]  Scott T. Grafton,et al.  A distributed left hemisphere network active during planning of everyday tool use skills. , 2004, Cerebral cortex.

[33]  E. Naito,et al.  Somatic Sensation of Hand-Object Interactive Movement Is Associated with Activity in the Left Inferior Parietal Cortex , 2006, The Journal of Neuroscience.

[34]  Thomas Wolbers,et al.  Hippocampus activity differentiates good from poor learners of a novel lexicon , 2005, NeuroImage.

[35]  M. D’Esposito,et al.  Frontal Networks for Learning and Executing Arbitrary Stimulus-Response Associations , 2005, The Journal of Neuroscience.

[36]  Claudia Scorolli,et al.  Language-induced motor activity in bi-manual object lifting , 2009, Experimental Brain Research.

[37]  S. Bookheimer Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. , 2002, Annual review of neuroscience.

[38]  Maryellen C. MacDonald,et al.  Context-dependent interpretation of words: Evidence for interactive neural processes , 2007, NeuroImage.

[39]  Murray Grossman,et al.  Left Inferior Parietal Representations for Skilled Hand-Object Interactions: Evidence from Stroke and Corticobasal Degeneration , 2007, Cortex.

[40]  N. Logothetis What we can do and what we cannot do with fMRI , 2008, Nature.

[41]  Marco Tettamanti,et al.  Semantic domain-specific functional integration for action-related vs. abstract concepts , 2010, Brain and Language.

[42]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[43]  G. Orban,et al.  Observing Others: Multiple Action Representation in the Frontal Lobe , 2005, Science.

[44]  G. Murphy,et al.  The Representation of Polysemous Words , 2001 .

[45]  G. Rizzolatti,et al.  Parietal cortex: from sight to action , 1997, Current Opinion in Neurobiology.

[46]  C Chiarello,et al.  Imageability and distributional typicality measures of nouns and verbs in contemporary English , 1999, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[47]  C. Fiebach,et al.  Modulation of Inferotemporal Cortex Activation during Verbal Working Memory Maintenance , 2006, Neuron.

[48]  R. Passingham,et al.  Specialisation within the prefrontal cortex: the ventral prefrontal cortex and associative learning , 2000, Experimental Brain Research.

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

[50]  G. Rizzolatti,et al.  Hearing Sounds, Understanding Actions: Action Representation in Mirror Neurons , 2002, Science.

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

[52]  B. Rosen,et al.  Motor cortex activation is related to force of squeezing , 2002, Human brain mapping.

[53]  Friedemann Pulvermüller,et al.  Brain mechanisms linking language and action , 2005, Nature Reviews Neuroscience.

[54]  Karl J. Friston,et al.  Dynamic Diaschisis: Anatomically Remote and Context-Sensitive Human Brain Lesions , 2001, Journal of Cognitive Neuroscience.

[55]  Sharlene D. Newman,et al.  Imagery in sentence comprehension: an fMRI study , 2004, NeuroImage.

[56]  M. Just,et al.  The neural bases of sentence comprehension: a fMRI examination of syntactic and lexical processing. , 2001, Cerebral cortex.

[57]  C. Price The anatomy of language: contributions from functional neuroimaging , 2000, Journal of anatomy.

[58]  Billi Randall,et al.  Cortical Differentiation for Nouns and Verbs Depends on Grammatical Markers , 2008, Journal of Cognitive Neuroscience.

[59]  I. Johnsrude,et al.  The problem of functional localization in the human brain , 2002, Nature Reviews Neuroscience.

[60]  Alan C. Evans,et al.  A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[61]  E Halgren,et al.  Rapid distributed fronto-parieto-occipital processing stages during working memory in humans. , 2002, Cerebral cortex.

[62]  L. Tyler,et al.  Modulation of motor and premotor cortices by actions, action words and action sentences , 2009, Neuropsychologia.

[63]  R. Johansson,et al.  Cortical activity in precision- versus power-grip tasks: an fMRI study. , 2000, Journal of neurophysiology.

[64]  Cameron S Carter,et al.  Prefrontal Cortex Guides Context-Appropriate Responding during Language Production , 2004, Neuron.

[65]  M. Hallett,et al.  Functional properties of brain areas associated with motor execution and imagery. , 2003, Journal of neurophysiology.

[66]  David Poeppel,et al.  Processing correlates of lexical semantic complexity , 2003, Cognition.

[67]  F. Pulvermüller,et al.  Grasping Ideas with the Motor System: Semantic Somatotopy in Idiom Comprehension , 2009 .

[68]  J. Kable,et al.  Neural Substrates of Action Event Knowledge , 2002, Journal of Cognitive Neuroscience.

[69]  Anne Cutler,et al.  The access and processing of idiomatic expressions , 1979 .

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

[71]  N. Dronkers,et al.  Lesion analysis of the brain areas involved in language comprehension , 2004, Cognition.

[72]  G. Rizzolatti,et al.  Neurophysiological mechanisms underlying the understanding and imitation of action , 2001, Nature Reviews Neuroscience.

[73]  B. Postle Working memory as an emergent property of the mind and brain , 2006, Neuroscience.

[74]  Nathalie Tzourio-Mazoyer,et al.  New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical electrostimulations. , 2005, Brain : a journal of neurology.

[75]  D. V. Cramon,et al.  Functional–anatomical concepts of human premotor cortex: evidence from fMRI and PET studies , 2003, NeuroImage.

[76]  Allen Ardestani,et al.  Distributed and associative working memory. , 2007, Cerebral cortex.

[77]  D. Kemmerer,et al.  The Two-Level Theory of verb meaning: An approach to integrating the semantics of action with the mirror neuron system , 2010, Brain and Language.

[78]  G. Murphy,et al.  Paper has been my ruin: Conceptual relations of polysemous senses , 2002 .

[79]  Friedemann Pulvermüller,et al.  Early MEG Activation Dynamics in the Left Temporal and Inferior Frontal Cortex Reflect Semantic Context Integration , 2007, Journal of Cognitive Neuroscience.

[80]  S. Thompson-Schill,et al.  The frontal lobes and the regulation of mental activity , 2005, Current Opinion in Neurobiology.

[81]  Michael P. Kaschak,et al.  Grounding language in action , 2002, Psychonomic bulletin & review.

[82]  A. Caramazza,et al.  Concepts Are More than Percepts: The Case of Action Verbs , 2008, The Journal of Neuroscience.

[83]  C. Büchel,et al.  Event-Related fMRI Reveals Cortical Sites Involved in Contextual Sentence Integration , 2002, NeuroImage.

[84]  G. Rizzolatti,et al.  Parietal Lobe: From Action Organization to Intention Understanding , 2005, Science.

[85]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[86]  Jody C. Culham,et al.  Orientation sensitivity to graspable objects: An fMRI adaptation study , 2007, NeuroImage.

[87]  François Lazeyras,et al.  Anatomical variability of the lateral frontal lobe surface: implication for intersubject variability in language neuroimaging , 2005, NeuroImage.

[88]  M. Brett,et al.  Actions Speak Louder Than Functions: The Importance of Manipulability and Action in Tool Representation , 2003, Journal of Cognitive Neuroscience.

[89]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[90]  J. Fuster,et al.  From perception to action: temporal integrative functions of prefrontal and parietal neurons. , 1999, Cerebral cortex.

[91]  Stephen M. Smith,et al.  Functional MRI : an introduction to methods , 2002 .

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

[93]  Scott T. Grafton,et al.  Actions or Hand-Object Interactions? Human Inferior Frontal Cortex and Action Observation , 2003, Neuron.

[94]  David Badre,et al.  Semantic retrieval, mnemonic control, and prefrontal cortex. , 2002, Behavioral and cognitive neuroscience reviews.