A right visual field advantage for visual processing of manipulable objects

Information about object-associated manipulations is lateralized to left parietal regions, while information about the visual form of tools is represented bilaterally in ventral occipito-temporal cortex. It is unknown how lateralization of motor-relevant information in left-hemisphere dorsal stream regions may affect the visual processing of manipulable objects. We used a lateralized masked priming paradigm to test for a right visual field (RVF) advantage in tool processing. Target stimuli were tools and animals, and briefly presented primes were identical to or scrambled versions of the targets. In Experiment 1, primes were presented either to the left or to the right of the centrally presented target, while in Experiment 2, primes were presented in one of eight locations arranged radially around the target. In both experiments, there was a RVF advantage in priming effects for tool but not for animal targets. Control experiments showed that participants were at chance for matching the identity of the lateralized primes in a picture–word matching experiment and also ruled out a general RVF speed-of-processing advantage for tool images. These results indicate that the overrepresentation of tool knowledge in the left hemisphere affects visual object recognition and suggests that interactions between the dorsal and ventral streams occurs during object categorization.

[1]  Tim Shallice,et al.  The different neural correlates of action and functional knowledge in semantic memory: an FMRI study. , 2008, Cerebral cortex.

[2]  A. Chatterjee.  Disembodying cognition , 2010, Language and Cognition.

[3]  Sergio E. Chaigneau,et al.  THE SIMILARITY-IN-TOPOGRAPHY PRINCIPLE: RECONCILING THEORIES OF CONCEPTUAL DEFICITS , 2003, Cognitive neuropsychology.

[4]  L. Jakobson,et al.  A neurological dissociation between perceiving objects and grasping them , 1991, Nature.

[5]  E. Ringelstein,et al.  Handedness and hemispheric language dominance in healthy humans. , 2000, Brain : a journal of neurology.

[6]  Bradford Z. Mahon,et al.  Action-Related Properties Shape Object Representations in the Ventral Stream , 2007, Neuron.

[7]  Gregory Króliczak,et al.  Atypical lateralization of language predicts cerebral asymmetries in parietal gesture representations , 2011, Neuropsychologia.

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

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

[10]  Leslie G. Ungerleider.  Two cortical visual systems , 1982 .

[11]  Salvatore Maria Aglioti,et al.  The Sound of Actions in Apraxia , 2008, Current Biology.

[12]  Alfonso Caramazza,et al.  The orchestration of the sensory-motor systems: Clues from Neuropsychology , 2005, Cognitive neuropsychology.

[13]  Bradford Z. Mahon,et al.  Action-related properties of objects shape object representations in the ventral stream , 2007 .

[14]  J R Hodges,et al.  "What" and "how": evidence for the dissociation of object knowledge and mechanical problem-solving skills in the human brain. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[15]  C. Koch,et al.  A category-specific response to animals in the right human amygdala , 2011, Nature Neuroscience.

[16]  Daniel N. Bub,et al.  Different modes of word recognition in the left and right visual fields , 1988, Brain and Language.

[17]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[18]  L. Buxbaum,et al.  Distinctions between manipulation and function knowledge of objects: evidence from functional magnetic resonance imaging. , 2005, Brain research. Cognitive brain research.

[19]  S. Thorpe,et al.  Speed of processing in the human visual system , 1996, Nature.

[20]  R. Ilmoniemi,et al.  Functional links between motor and language systems , 2005, The European journal of neuroscience.

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

[22]  Alfonso Caramazza,et al.  What is the role of motor simulation in action and object recognition? Evidence from apraxia , 2007, Cognitive neuropsychology.

[23]  M. Kiefer,et al.  Action observation can prime visual object recognition , 2009, Experimental Brain Research.

[24]  K. Heilman,et al.  A Cognitive Neuropsychological Model of Limb Praxis , 1991 .

[25]  Leif D. Nelson,et al.  False-Positive Psychology , 2011, Psychological science.

[26]  F. Fang,et al.  Cortical responses to invisible objects in the human dorsal and ventral pathways , 2005, Nature Neuroscience.

[27]  Bradford Z. Mahon,et al.  The Role of the Dorsal Visual Processing Stream in Tool Identification , 2010, Psychological science.

[28]  Melvyn A Goodale,et al.  Dual routes to action: contributions of the dorsal and ventral streams to adaptive behavior. , 2005, Progress in brain research.

[29]  Ronald A. Rensink,et al.  Competition for consciousness among visual events: the psychophysics of reentrant visual processes. , 2000, Journal of experimental psychology. General.

[30]  Alex Martin,et al.  Representation of Manipulable Man-Made Objects in the Dorsal Stream , 2000, NeuroImage.

[31]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

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

[33]  Alex Martin,et al.  NEURAL FOUNDATIONS FOR UNDERSTANDING SOCIAL AND MECHANICAL CONCEPTS , 2003, Cognitive neuropsychology.

[34]  R. Mansfield,et al.  Analysis of visual behavior , 1982 .

[35]  Scott T. Grafton,et al.  Graspable objects grab attention when the potential for action is recognized , 2003, Nature Neuroscience.

[36]  E. Thorndike.  Ideo-motor action. , 1913 .

[37]  F. Previc.  Functional specialization in the lower and upper visual fields in humans: Its ecological origins and neurophysiological implications , 1990, Behavioral and Brain Sciences.

[38]  A. Caramazza,et al.  Letter identification processes in reading: Distractor interference reveals an automatically engaged, domain-specific mechanism , 2006, Cognitive neuropsychology.

[39]  G. Glover,et al.  Retinotopic organization in human visual cortex and the spatial precision of functional MRI. , 1997, Cerebral cortex.

[40]  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.

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

[42]  A. Sirigu,et al.  The role of sensorimotor experience in object recognition. A case of multimodal agnosia. , 1991, Brain : a journal of neurology.

[43]  JamesW. Lewis.  Cortical Networks Related to Human Use of Tools , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[44]  K. Heilman,et al.  Ideational apraxia: A deficit in tool selection and use , 1989, Annals of neurology.

[45]  Agnes Roby-Brami,et al.  A neuropsychological perspective on the link between language and praxis in modern humans , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

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

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

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

[50]  Markus Graf,et al.  The role of action representations in visual object recognition , 2006, Experimental Brain Research.

[51]  M S Gazzaniga,et al.  Dissociation of language and cognition. A psychological profile of two disconnected right hemispheres. , 1984, Brain : a journal of neurology.

[52]  Alfonso Caramazza,et al.  Differential Activity for Animals and Manipulable Objects in the Anterior Temporal Lobes , 2011, Journal of Cognitive Neuroscience.

[53]  C. Koch,et al.  Visual Selective Behavior Can Be Triggered by a Feed-Forward Process , 2003, Journal of Cognitive Neuroscience.

[54]  A. Damasio,et al.  A neural basis for the retrieval of conceptual knowledge , 1997, Neuropsychologia.

[55]  M. Brysbaert,et al.  A right visual field advantage for tool-recognition in the visual half-field paradigm , 2011, Neuropsychologia.

[56]  Gregory Króliczak,et al.  A common network in the left cerebral hemisphere represents planning of tool use pantomimes and familiar intransitive gestures at the hand-independent level. , 2009, Cerebral cortex.

[57]  Karl J. Friston,et al.  Two distinct neural mechanisms for category-selective responses. , 2006, Cerebral cortex.

[58]  Zoë R. Hunter,et al.  Visual half-field experiments are a good measure of cerebral language dominance if used properly: Evidence from fMRI , 2008, Neuropsychologia.

[59]  C. Chiarello,et al.  Lexical decision and naming asymmetries: Influence of response selection and response bias , 1988, Brain and Language.

[60]  Alfonso Caramazza,et al.  Unconscious processing dissociates along categorical lines , 2008, Proceedings of the National Academy of Sciences.

[61]  Richard J. Epstein,et al.  Current perspectives in dysphasia , 1985 .

[62]  M. Wallace,et al.  Visual Localization Ability Influences Cross-Modal Bias , 2003, Journal of Cognitive Neuroscience.

[63]  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.

[64]  Scott H. Johnson-Frey.  The neural bases of complex tool use in humans , 2004, Trends in Cognitive Sciences.

[65]  G. Gigli,et al.  Degraded Semantic Knowledge And Accurate Object Use , 2007, Cortex.

[66]  S. Kastner,et al.  Two hierarchically organized neural systems for object information in human visual cortex , 2008, Nature Neuroscience.

[67]  Leslie G. Ungerleider.  Functional Brain Imaging Studies of Cortical Mechanisms for Memory , 1995, Science.

[68]  H. Heuer,et al.  Perspectives on Perception and Action , 1989 .

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

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

[71]  J. Grainger,et al.  Effects of prime—target spatial separation and attentional deployment on masked repetition priming , 2008, Perception & psychophysics.

[72]  Bradford Z. Mahon,et al.  A critical look at the embodied cognition hypothesis and a new proposal for grounding conceptual content , 2008, Journal of Physiology-Paris.