Dissociating the representation of action- and sound-related concepts in middle temporal cortex

Modality-specific models of conceptual memory propose close links between concepts and the sensory-motor systems. Neuroimaging studies found, in different subject groups, that action-related and sound-related concepts activated different parts of posterior middle temporal gyrus (pMTG), suggesting a modality-specific representation of conceptual features. However, as these different parts of pMTG are close to each other, it is possible that the observed anatomical difference is merely related to interindividual variability. In the present functional magnetic resonance imaging study, we now investigated within the same participant group a possible conceptual feature-specific organization in pMTG. Participants performed lexical decisions on sound-related (e.g., telephone) and action-related (hammer) words. Sound words elicited higher activity in anterior pMTG adjacent to auditory association cortex, but action-related words did so in posterior pMTG close to motion sensitive areas. These results confirm distinct conceptual representations of sound and action in pMTG, just adjacent to the respective modality-specific cortices.

[1]  Isabel Gauthier,et al.  Auditory and Action Semantic Features Activate Sensory-Specific Perceptual Brain Regions , 2003, Current Biology.

[2]  P. A. Lewis,et al.  Brain mechanisms for mood congruent memory facilitation , 2005, NeuroImage.

[3]  Glyn W. Humphreys,et al.  From objects to names: A cognitive neuroscience approach , 1999, Psychological research.

[4]  Jeffrey R Binder,et al.  Human brain regions involved in recognizing environmental sounds. , 2004, Cerebral cortex.

[5]  James W. Lewis,et al.  Audio-Visual Perception of Everyday Natural Objects - Hemodynamic Studies in Humans , 2010 .

[6]  Friedemann Pulvermüller,et al.  The Word Processing Deficit in Semantic Dementia: All Categories Are Equal, but Some Categories Are More Equal than Others , 2010, Journal of Cognitive Neuroscience.

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

[8]  James L. McClelland,et al.  Are there mental lexicons? The role of semantics in lexical decision , 2010, Brain Research.

[9]  L. Barsalou,et al.  Grounding the human conceptual system in perception, action, and internal states , 2013 .

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

[11]  Glyn W. Humphreys,et al.  Cascade processes in picture identification , 1988 .

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

[13]  M. Kiefer,et al.  Conceptual representations in mind and brain: Theoretical developments, current evidence and future directions , 2012, Cortex.

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

[15]  Ferath Kherif,et al.  Distributed cell assemblies for general lexical and category‐specific semantic processing as revealed by fMRI cluster analysis , 2009, Human brain mapping.

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

[17]  John R. Anderson.  The Architecture of Cognition , 1983 .

[18]  Bradford Z. Mahon,et al.  The organization of conceptual knowledge: the evidence from category-specific semantic deficits , 2003, Trends in Cognitive Sciences.

[19]  Christian Gerlach,et al.  A Review of Functional Imaging Studies on Category Specificity , 2007, Journal of Cognitive Neuroscience.

[20]  Karl J. Friston,et al.  A direct quantitative relationship between the functional properties of human and macaque V5 , 2000, Nature Neuroscience.

[21]  Markus Kiefer,et al.  Neuroplasticity of semantic representations for musical instruments in professional musicians , 2011, NeuroImage.

[22]  Xiaoping P. Hu,et al.  fMRI evidence for word association and situated simulation in conceptual processing , 2008, Journal of Physiology-Paris.

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

[24]  B. Mesquita,et al.  Adjustment to Chronic Diseases and Terminal Illness Health Psychology : Psychological Adjustment to Chronic Disease , 2006 .

[25]  M. Kiefer.  The N400 is modulated by unconsciously perceived masked words: further evidence for an automatic spreading activation account of N400 priming effects. , 2002, Brain research. Cognitive brain research.

[26]  M. Kiefer,et al.  The Sound of Concepts: Four Markers for a Link between Auditory and Conceptual Brain Systems , 2008, The Journal of Neuroscience.

[27]  B. Argall,et al.  Integration of Auditory and Visual Information about Objects in Superior Temporal Sulcus , 2004, Neuron.

[28]  G I de Zubicaray,et al.  The semantic interference effect in the picture‐word paradigm: An event‐related fMRI study employing overt responses , 2001, Human brain mapping.

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

[30]  Anne Cutler,et al.  A theory of lexical access in speech production , 1999, Behavioral and Brain Sciences.

[31]  R. Zatorre,et al.  Voice-selective areas in human auditory cortex , 2000, Nature.

[32]  Jacob Cohen.  Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[33]  S. Koelsch.  Neural substrates of processing syntax and semantics in music , 2005, Current Opinion in Neurobiology.

[34]  Mark Drakesmith,et al.  Posterior middle temporal gyrus is involved in verbal and non-verbal semantic cognition: Evidence from rTMS , 2012 .

[35]  Charles D. Smith,et al.  Dissociation of Automatic and Strategic Lexical-Semantics: Functional Magnetic Resonance Imaging Evidence for Differing Roles of Multiple Frontotemporal Regions , 2006, The Journal of Neuroscience.

[36]  James L. McClelland,et al.  Structure and deterioration of semantic memory: a neuropsychological and computational investigation. , 2004, Psychological review.

[37]  Natalie M. Trumpp,et al.  Losing the sound of concepts: Damage to auditory association cortex impairs the processing of sound-related concepts , 2013, Cortex.

[38]  F Pulvermüller,et al.  Nouns and verbs in the intact brain: evidence from event-related potentials and high-frequency cortical responses. , 1999, Cerebral cortex.

[39]  G. Lakoff,et al.  The Brain's concepts: the role of the Sensory-motor system in conceptual knowledge , 2005, Cognitive neuropsychology.

[40]  R. Zatorre,et al.  Behavioral and neural correlates of perceived and imagined musical timbre , 2004, Neuropsychologia.

[41]  Antonio R. Damasio,et al.  The Brain Binds Entities and Events by Multiregional Activation from Convergence Zones , 1989, Neural Computation.

[42]  Markus Kiefer,et al.  Repetition-priming Modulates Category-related Effects on Event-related Potentials: Further Evidence for Multiple Cortical Semantic Systems , 2005, Journal of Cognitive Neuroscience.

[43]  Markus Kiefer,et al.  Conceptual Flexibility in the Human Brain: Dynamic Recruitment of Semantic Maps from Visual, Motor, and Motion-related Areas , 2008, Journal of Cognitive Neuroscience.

[44]  David J. M. Kraemer,et al.  Musical imagery: Sound of silence activates auditory cortex , 2005, Nature.

[45]  L. Fadiga,et al.  Active perception: sensorimotor circuits as a cortical basis for language , 2010, Nature Reviews Neuroscience.

[46]  Olaf Hauk,et al.  Experience-dependent Plasticity of Conceptual Representations in Human Sensory-Motor Areas , 2007, Journal of Cognitive Neuroscience.

[47]  Leslie G. Ungerleider,et al.  Neural correlates of category-specific knowledge , 1996, Nature.

[48]  Peter Hagoort,et al.  Retrieval and unification of syntactic structure in sentence comprehension: an FMRI study using word-category ambiguity. , 2009, Cerebral cortex.