Repetition suppression in occipital–temporal visual areas is modulated by physical rather than semantic features of objects

Functional magnetic-resonance imaging was used to identify areas involved in naming objects and to examine which of these areas adapted to either physical or semantics features of objects. We presented successive pairs of objects that were either the same exemplar of an object, different exemplars of that object, or different objects. By controlling for differences in physical features between pairs of different exemplars and different objects, visual areas in the occipital-temporal cortex were subject to repetition suppression when the same exemplars of an object were repeated, but not when different exemplars of an object were repeated. This was true independent of whether or not participants named objects. Repetition suppression in visual areas appeared therefore bound to physical features. Nevertheless, repetition suppression for physical features was greater in left visual areas when objects were named, suggesting that naming, known to depend on mechanisms in the left hemisphere, may induce greater attentional modulation in the left than in the right visual areas. Taken together, we propose that the difference between our findings and those of earlier studies that report semantic influences can be explained by the failure of those studies to control for differences in the appearance of different exemplars. Left frontal areas showed repetition suppression when either the same or different exemplars of an object were repeated, but only when participants named objects. These results suggest that visual areas process information about physical features without semantic modulation by higher-order areas, and that left frontal areas process semantic features, but the engagement of these processes is task modulated.

[1]  H. Bülthoff,et al.  Representation of the perceived 3-D object shape in the human lateral occipital complex. , 2003, Cerebral cortex.

[2]  G. Ojemann,et al.  Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. , 1989, Journal of neurosurgery.

[3]  G W Humphreys,et al.  Varieties of Object Constancy , 1989, The Quarterly journal of experimental psychology. A, Human experimental psychology.

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

[5]  E. Wojciulik,et al.  Attention increases neural selectivity in the human lateral occipital complex , 2004, Nature Neuroscience.

[6]  Ravi S. Menon,et al.  Differential Effects of Viewpoint on Object-Driven Activation in Dorsal and Ventral Streams , 2002, Neuron.

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

[8]  Nancy Kanwisher,et al.  Divide and conquer: A defense of functional localizers , 2006, NeuroImage.

[9]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[10]  Michael S. Beauchamp,et al.  Automatic Priming of Semantically Related Words Reduces Activity in the Fusiform Gyrus , 2005, Journal of Cognitive Neuroscience.

[11]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[12]  I. Biederman,et al.  Size invariance in visual object priming , 1992 .

[13]  A. Schleicher,et al.  Broca's region revisited: Cytoarchitecture and intersubject variability , 1999, The Journal of comparative neurology.

[14]  Angela R Laird,et al.  Meta‐analyses of object naming: Effect of baseline , 2005, Human brain mapping.

[15]  Dave Bartram,et al.  The role of visual and semantic codes in object naming , 1974 .

[16]  I. Biederman,et al.  Recognizing depth-rotated objects: Evidence and conditions for three-dimensional viewpoint invariance. , 1993 .

[17]  R. Henson,et al.  Multiple levels of visual object constancy revealed by event-related fMRI of repetition priming , 2002, Nature Neuroscience.

[18]  T. Hendler,et al.  A hierarchical axis of object processing stages in the human visual cortex. , 2001, Cerebral cortex.

[19]  D. Schacter,et al.  Perceptual specificity in visual object priming: functional magnetic resonance imaging evidence for a laterality difference in fusiform cortex , 2001, Neuropsychologia.

[20]  T. Braver,et al.  Anterior Cingulate and the Monitoring of Response Conflict: Evidence from an fMRI Study of Overt Verb Generation , 2000, Journal of Cognitive Neuroscience.

[21]  Josh H. McDermott,et al.  Functional imaging of human visual recognition. , 1996, Brain research. Cognitive brain research.

[22]  A. Dale,et al.  Functional-Anatomic Correlates of Object Priming in Humans Revealed by Rapid Presentation Event-Related fMRI , 1998, Neuron.

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

[24]  S. Edelman,et al.  Differential Processing of Objects under Various Viewing Conditions in the Human Lateral Occipital Complex , 1999, Neuron.

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

[26]  K. Johnston,et al.  Top-Down Control-Signal Dynamics in Anterior Cingulate and Prefrontal Cortex Neurons following Task Switching , 2007, Neuron.

[27]  Ravi S. Menon,et al.  Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[28]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[29]  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.

[30]  B. Rapp,et al.  Discreteness and interactivity in spoken word production. , 2000, Psychological review.

[31]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

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

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

[34]  R. Henson.  Neuroimaging studies of priming , 2003, Progress in Neurobiology.

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

[36]  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.

[37]  B. Duchaine,et al.  Visual Agnosia, 2nd Ed. , 2005 .

[38]  G. Glover.  Deconvolution of Impulse Response in Event-Related BOLD fMRI1 , 1999, NeuroImage.

[39]  Alan C. Evans,et al.  A general statistical analysis for fMRI data , 2000, NeuroImage.

[40]  M. E. Walton,et al.  Cognitive Neuroscience: Resolving Conflict in and over the Medial Frontal Cortex , 2005, Current Biology.

[41]  Peter A. Bandettini,et al.  Experimental designs and processing strategies for fMRI studies involving overt verbal responses , 2004, NeuroImage.

[42]  K Tanaka,et al.  Neuronal mechanisms of object recognition. , 1993, Science.

[43]  D. Burnham,et al.  The delayed trigger voice key: An improved analogue voice key for psycholinguistic research , 2005, Behavior research methods.

[44]  Kenneth F. Valyear,et al.  A double dissociation between sensitivity to changes in object identity and object orientation in the ventral and dorsal visual streams: A human fMRI study , 2006, Neuropsychologia.

[45]  M. Masson,et al.  Using confidence intervals in within-subject designs , 1994, Psychonomic bulletin & review.

[46]  Wilma Koutstaal,et al.  Neural mechanisms of visual object priming: evidence for perceptual and semantic distinctions in fusiform cortex , 2003, NeuroImage.

[47]  M Abecassis,et al.  Word Frequencies in Written and Spoken English. , 2010 .

[48]  R. Henson,et al.  BOLD repetition decreases in object-responsive ventral visual areas depend on spatial attention. , 2004, Journal of neurophysiology.

[49]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Tutis Vilis,et al.  Task-related laterality effects in the lateral occipital complex , 2007, Brain Research.

[51]  Alex Martin,et al.  Long-lasting cortical plasticity in the object naming system , 2000, Nature Neuroscience.

[52]  G. Orban,et al.  Selectivity of Neuronal Adaptation Does Not Match Response Selectivity: A Single-Cell Study of the fMRI Adaptation Paradigm , 2006, Neuron.