Automatic Top-Down Processing Explains Common Left Occipito-Temporal Responses to Visual Words and Objects

Previous studies have demonstrated that a region in the left ventral occipito-temporal (LvOT) cortex is highly selective to the visual forms of written words and objects relative to closely matched visual stimuli. Here, we investigated why LvOT activation is not higher for reading than picture naming even though written words and pictures of objects have grossly different visual forms. To compare neuronal responses for words and pictures within the same LvOT area, we used functional magnetic resonance imaging adaptation and instructed participants to name target stimuli that followed briefly presented masked primes that were either presented in the same stimulus type as the target (word–word, picture–picture) or a different stimulus type (picture–word, word–picture). We found that activation throughout posterior and anterior parts of LvOT was reduced when the prime had the same name/response as the target irrespective of whether the prime-target relationship was within or between stimulus type. As posterior LvOT is a visual form processing area, and there was no visual form similarity between different stimulus types, we suggest that our results indicate automatic top-down influences from pictures to words and words to pictures. This novel perspective motivates further investigation of the functional properties of this intriguing region.

[1]  Francis T. Durso,et al.  Facilitation in naming and categorizing repeated pictures and words. , 1979 .

[2]  T H Carr,et al.  Early extraction of meaning from pictures and its relation to conscious identification. , 1980, Journal of experimental psychology. Human perception and performance.

[3]  E. G. Jones Cerebral Cortex , 1987, Cerebral Cortex.

[4]  W. Glaser Picture naming , 1992, Cognition.

[5]  J Grainger,et al.  A study of masked form priming in picture and word naming , 1994, Memory & cognition.

[6]  C. Price,et al.  Three Distinct Ventral Occipitotemporal Regions for Reading and Object Naming , 1999, NeuroImage.

[7]  Rajesh P. N. Rao,et al.  Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. , 1999 .

[8]  P. Starreveld,et al.  Picture naming: identical priming and word frequency interact , 1999 .

[9]  J. Segui,et al.  Semantic and Associative Priming in Picture Naming , 2000, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[10]  S Lehéricy,et al.  The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. , 2000, Brain : a journal of neurology.

[11]  K. Grill-Spector,et al.  fMR-adaptation: a tool for studying the functional properties of human cortical neurons. , 2001, Acta psychologica.

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

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

[14]  S. Dehaene,et al.  The priming method: imaging unconscious repetition priming reveals an abstract representation of number in the parietal lobes. , 2001, Cerebral cortex.

[15]  S. Dehaene,et al.  The visual word form area: a prelexical representation of visual words in the fusiform gyrus , 2002, Neuroreport.

[16]  S. Dehaene,et al.  Language-specific tuning of visual cortex? Functional properties of the Visual Word Form Area. , 2002, Brain : a journal of neurology.

[17]  J. B. Levitt,et al.  Circuits for Local and Global Signal Integration in Primary Visual Cortex , 2002, The Journal of Neuroscience.

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

[19]  H. Spekreijse,et al.  Masking Interrupts Figure-Ground Signals in V1 , 2002, Journal of Cognitive Neuroscience.

[20]  Tzu-Chen Yeh,et al.  Frequency effects of Chinese character processing in the brain: an event-related fMRI study , 2003, NeuroImage.

[21]  A. Mechelli,et al.  Neuroimaging Studies of Word and Pseudoword Reading: Consistencies, Inconsistencies, and Limitations , 2003, Journal of Cognitive Neuroscience.

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

[23]  R. Henson,et al.  Neural response suppression, haemodynamic repetition effects, and behavioural priming , 2003, Neuropsychologia.

[24]  M. Masson,et al.  Beyond spreading activation: An influence of relatedness proportion on masked semantic priming , 2003, Psychonomic bulletin & review.

[25]  Stephen José Hanson,et al.  Combinatorial codes in ventral temporal lobe for object recognition: Haxby (2001) revisited: is there a “face” area? , 2004, NeuroImage.

[26]  Joseph T Devlin,et al.  The pro and cons of labelling a left occipitotemporal region: “the visual word form area” , 2004, NeuroImage.

[27]  Jean-Francois Mangin,et al.  Automatized clustering and functional geometry of human parietofrontal networks for language, space, and number , 2004, NeuroImage.

[28]  J B Poline,et al.  Letter Binding and Invariant Recognition of Masked Words , 2004, Psychological science.

[29]  Martin Kronbichler,et al.  The visual word form area and the frequency with which words are encountered: evidence from a parametric fMRI study , 2004, NeuroImage.

[30]  M. Sigman,et al.  The neural code for written words: a proposal , 2005, Trends in Cognitive Sciences.

[31]  A. Mechelli,et al.  Reading and reading disturbance , 2005, Current Opinion in Neurobiology.

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

[33]  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.

[34]  E. Halgren,et al.  Top-down facilitation of visual recognition. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Paul M Matthews,et al.  The Role of the Posterior Fusiform Gyrus in Reading , 2006, Journal of Cognitive Neuroscience.

[36]  Karl J. Friston,et al.  A free energy principle for the brain , 2006, Journal of Physiology-Paris.

[37]  Nikolaus Weiskopf,et al.  Optimal EPI parameters for reduction of susceptibility-induced BOLD sensitivity losses: A whole-brain analysis at 3 T and 1.5 T , 2006, NeuroImage.

[38]  Marianna D. Eddy,et al.  Masked repetition priming and event-related brain potentials: a new approach for tracking the time-course of object perception. , 2006, Psychophysiology.

[39]  Gui Xue,et al.  Language experience shapes fusiform activation when processing a logographic artificial language: An fMRI training study , 2006, NeuroImage.

[40]  R N Henson,et al.  Mechanisms of top-down facilitation in perception of visual objects studied by FMRI. , 2007, Cerebral cortex.

[41]  N. Kanwisher,et al.  Visual word processing and experiential origins of functional selectivity in human extrastriate cortex , 2007, Proceedings of the National Academy of Sciences.

[42]  Stanislas Dehaene,et al.  Task-specific change of unconscious neural priming in the cerebral language network , 2007, Proceedings of the National Academy of Sciences.

[43]  Mariano Sigman,et al.  Hierarchical Coding of Letter Strings in the Ventral Stream: Dissecting the Inner Organization of the Visual Word-Form System , 2007, Neuron.

[44]  Phillip J. Holcomb,et al.  Spatial dynamics of masked picture repetition effects , 2007, NeuroImage.

[45]  Stanislas Dehaene,et al.  Cerebral bases of subliminal and supraliminal priming during reading. , 2007, Cerebral cortex.

[46]  James L. McClelland,et al.  Dissociating stimulus‐driven semantic and phonological effect during reading and naming , 2006, Human brain mapping.

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

[48]  Russell A. Poldrack,et al.  The Neural Substrates of Visual Perceptual Learning of Words: Implications for the Visual Word Form Area Hypothesis , 2007, Journal of Cognitive Neuroscience.

[49]  C. Gilbert,et al.  Brain States: Top-Down Influences in Sensory Processing , 2007, Neuron.

[50]  Karl J. Friston,et al.  Evoked brain responses are generated by feedback loops , 2007, Proceedings of the National Academy of Sciences.

[51]  S. Rombouts,et al.  Selective activation around the left occipito‐temporal sulcus for words relative to pictures: Individual variability or false positives? , 2007, Human brain mapping.

[52]  P. Sumner,et al.  Oscillations in Motor Priming: Positive Rebound Follows the Inhibitory Phase in the Masked Prime Paradigm , 2008, Journal of motor behavior.

[53]  Dennis Norris,et al.  Perception as evidence accumulation and Bayesian inference: insights from masked priming. , 2008, Journal of experimental psychology. General.

[54]  John D. E. Gabrieli,et al.  An fMRI analysis of object priming and workload in the precuneus complex , 2008, Neuropsychologia.

[55]  Zhong-Lin Lu,et al.  Sensitivity to orthographic familiarity in the occipito-temporal region , 2008, NeuroImage.

[56]  N. Kanwisher,et al.  Feedback of pVisual Object Information to Foveal Retinotopic Cortex , 2008, Nature Neuroscience.

[57]  Florent Aubry,et al.  Piecemeal recruitment of left-lateralized brain areas during reading: A spatio-functional account , 2008, NeuroImage.

[58]  S. Dehaene,et al.  The role of invariant line junctions in object and visual word recognition , 2009, Vision Research.

[59]  John Duncan,et al.  Evidence for long-range feedback in target detection: Detection of semantic targets modulates activity in early visual areas , 2009, Neuropsychologia.

[60]  Tilo Kircher,et al.  Priming words with pictures: Neural correlates of semantic associations in a cross‐modal priming task using fMRI , 2009, Human brain mapping.

[61]  Joseph T. Devlin,et al.  Consistency and variability in functional localisers , 2009, NeuroImage.

[62]  K. R. Ridderinkhof,et al.  Dissociating consciousness from inhibitory control: evidence for unconsciously triggered response inhibition in the stop-signal task. , 2009, Journal of experimental psychology. Human perception and performance.

[63]  Bert Reynvoet,et al.  Mechanisms of masked priming: a meta-analysis. , 2009, Psychological bulletin.