Flexible visual information representation in human parietal cortex

In many everyday activities, we must visually process multiple objects embedded in complex real world scenes. Our visual system can flexibly extract behaviorally relevant visual information from such scenes, even though it has a severely limited processing capacity. This dissertation proposes that human superior intra-­‐parietal sulcus (IPS) plays a central role in this flexible visual information processing. In Chapter 1, using functional magnetic resonance imaging (fMRI) with univariate analysis, I found that distractor processing in superior IPS was attenuated when target locations were known in advance. In Chapter 2, using multi-­‐voxel pattern analysis (MVPA), I showed that superior IPS encoded object shapes, but only when such information was required by task. In Chapter 3, I showed that, given a set of perceptually distinct, but semantically grouped visual inputs, superior IPS could represent abstract object identity. The neural similarity of identities in superior IPS significantly correlated with perceived similarity between identities, confirming the representation in this region indeed reflected identity. Taken together, these results suggest that human superior IPS encodes a wide range of visual information, from simple features to abstract identities, in a task-­‐dependent manner, enabling flexible goal-­‐directed visual information processing in the human brain.

[1]  Nancy Kanwisher,et al.  fMRI evidence for objects as the units of attentional selection , 1999, Nature.

[2]  N. Moray.  Attention in Dichotic Listening: Affective Cues and the Influence of Instructions , 1959 .

[3]  Z Kourtzi,et al.  Representation of Perceived Object Shape by the Human Lateral Occipital Complex , 2001, Science.

[4]  R. Marois,et al.  Posterior parietal cortex activity predicts individual differences in visual short-term memory capacity , 2005, Cognitive, affective & behavioral neuroscience.

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

[6]  Nancy Kanwisher,et al.  The distribution of category and location information across object-selective regions in human visual cortex , 2008, Proceedings of the National Academy of Sciences.

[7]  M. Chun,et al.  Dissociable neural mechanisms supporting visual short-term memory for objects , 2006, Nature.

[8]  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.

[9]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[10]  Edward K. Vogel,et al.  The capacity of visual working memory for features and conjunctions , 1997, Nature.

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

[12]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[13]  T. R. Jordan,et al.  Perception and action in 'visual form agnosia'. , 1991, Brain : a journal of neurology.

[14]  J. Duncan,et al.  Adaptive Coding of Task-Relevant Information in Human Frontoparietal Cortex , 2011, The Journal of Neuroscience.

[15]  Puiu F. Balan,et al.  Attention as a decision in information space , 2010, Trends in Cognitive Sciences.

[16]  N. Kanwisher,et al.  The Human Body , 2001 .

[17]  Dwight J. Kravitz,et al.  High-level visual object representations are constrained by position. , 2010, Cerebral cortex.

[18]  Maro G. Machizawa,et al.  Neural activity predicts individual differences in visual working memory capacity , 2004, Nature.

[19]  Y. Tsal,et al.  Perceptual load as a major determinant of the locus of selection in visual attention , 1994, Perception & psychophysics.

[20]  B. Scholl.  Objects and attention: the state of the art , 2001, Cognition.

[21]  J. Duncan.  An adaptive coding model of neural function in prefrontal cortex , 2001 .

[22]  Marlene Behrmann,et al.  Unraveling the distributed neural code of facial identity through spatiotemporal pattern analysis , 2011, Proceedings of the National Academy of Sciences.

[23]  David J. Freedman,et al.  Biased Associative Representations in Parietal Cortex , 2013, Neuron.

[24]  J. Deutsch,et al.  Attention: Some theoretical considerations. , 1963 .

[25]  Suzanne Corkin,et al.  Acquisition of motor skill after bilateral medial temporal-lobe excision , 1996 .

[26]  Adam C. Riggall,et al.  Distributed Patterns of Activity in Sensory Cortex Reflect the Precision of Multiple Items Maintained in Visual Short-Term Memory , 2013, The Journal of Neuroscience.

[27]  Justin L. Gardner,et al.  Feature-Specific Attentional Priority Signals in Human Cortex , 2011, The Journal of Neuroscience.

[28]  David D. Cox,et al.  Functional magnetic resonance imaging (fMRI) “brain reading”: detecting and classifying distributed patterns of fMRI activity in human visual cortex , 2003, NeuroImage.

[29]  Leslie G. Ungerleider,et al.  ‘What’ and ‘where’ in the human brain , 1994, Current Opinion in Neurobiology.

[30]  D. Kahneman,et al.  The reviewing of object files: Object-specific integration of information , 1992, Cognitive Psychology.

[31]  Nancy Kanwisher,et al.  Broad domain generality in focal regions of frontal and parietal cortex , 2013, Proceedings of the National Academy of Sciences.

[32]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[33]  John H. R. Maunsell,et al.  Shape selectivity in primate lateral intraparietal cortex , 1998, Nature.

[34]  Keiji Tanaka,et al.  Matching Categorical Object Representations in Inferior Temporal Cortex of Man and Monkey , 2008, Neuron.

[35]  Justin L. Vincent,et al.  Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. , 2008, Journal of neurophysiology.

[36]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[37]  David J. Freedman,et al.  Generalized associative representations in parietal cortex , 2011, Nature Neuroscience.

[38]  P. Goldman-Rakic.  Cellular basis of working memory , 1995, Neuron.

[39]  M Corbetta,et al.  Attentional modulation of neural processing of shape, color, and velocity in humans. , 1990, Science.

[40]  Z. Pylyshyn.  The role of location indexes in spatial perception: A sketch of the FINST spatial-index model , 1989, Cognition.

[41]  Lawrence H Snyder,et al.  Single Neurons in Posterior Parietal Cortex of Monkeys Encode Cognitive Set , 2004, Neuron.

[42]  E. Viding,et al.  Load theory of selective attention and cognitive control. , 2004, Journal of experimental psychology. General.

[43]  A. Caramazza,et al.  Decoding representations of face identity that are tolerant to rotation. , 2014, Cerebral cortex.

[44]  S. Edelman,et al.  Cue-Invariant Activation in Object-Related Areas of the Human Occipital Lobe , 1998, Neuron.

[45]  Dwight J. Kravitz,et al.  A new neural framework for visuospatial processing , 2011, Nature Reviews Neuroscience.

[46]  J. Duncan.  The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour , 2010, Trends in Cognitive Sciences.

[47]  N. Cowan.  The magical number 4 in short-term memory: A reconsideration of mental storage capacity , 2001, Behavioral and Brain Sciences.

[48]  E. Vogel,et al.  Word meanings can be accessed but not reported during the attentional blink , 1996, Nature.

[49]  M. Chun,et al.  Selecting and perceiving multiple visual objects , 2009, Trends in Cognitive Sciences.

[50]  N. Kanwisher,et al.  Cortical Regions Involved in Perceiving Object Shape , 2000, The Journal of Neuroscience.

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

[52]  David J. Freedman,et al.  Visual categorization and the parietal cortex , 2012, Front. Integr. Neurosci..

[53]  Dwight J. Kravitz,et al.  The ventral visual pathway: an expanded neural framework for the processing of object quality , 2013, Trends in Cognitive Sciences.

[54]  S. Luck,et al.  Discrete fixed-resolution representations in visual working memory , 2008, Nature.

[55]  J. Assad,et al.  Dynamic coding of behaviourally relevant stimuli in parietal cortex , 2002, Nature.

[56]  Doris Y. Tsao,et al.  Comparing face patch systems in macaques and humans , 2008, Proceedings of the National Academy of Sciences.

[57]  Ana Torralbo,et al.  Perceptual-Load-Induced Selection as a Result of Local Competitive Interactions in Visual Cortex , 2008, Psychological science.

[58]  M. Goldberg,et al.  Space and attention in parietal cortex. , 1999, Annual review of neuroscience.

[59]  Z. Pylyshyn.  Some primitive mechanisms of spatial attention , 1994, Cognition.

[60]  E. Renzi,et al.  Prosopagnosia can be associated with damage confined to the right hemisphere—An MRI and PET study and a review of the literature , 1994, Neuropsychologia.

[61]  Yaoda Xu,et al.  Visual grouping in human parietal cortex , 2007, Proceedings of the National Academy of Sciences.

[62]  David J. Freedman,et al.  Experience-dependent representation of visual categories in parietal cortex , 2006, Nature.

[63]  John-Dylan Haynes,et al.  Decoding the Contents of Visual Short-Term Memory from Human Visual and Parietal Cortex , 2012, The Journal of Neuroscience.

[64]  Jonathan D. Power,et al.  Multi-task connectivity reveals flexible hubs for adaptive task control , 2013, Nature Neuroscience.

[65]  Yaoda Xu.  The Role of the Superior Intraparietal Sulcus in Supporting Visual Short-Term Memory for Multifeature Objects , 2007, The Journal of Neuroscience.

[66]  Leslie G. Ungerleider,et al.  A neural system for human visual working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[67]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[68]  J. Duncan,et al.  Visual search and stimulus similarity. , 1989, Psychological review.

[69]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[70]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

[71]  Maro G. Machizawa,et al.  Neural measures reveal individual differences in controlling access to working memory , 2005, Nature.

[72]  David J. Freedman,et al.  Preferential Encoding of Visual Categories in Parietal Cortex Compared to Prefrontal Cortex , 2011, Nature Neuroscience.

[73]  David J. Freedman,et al.  Distinct Encoding of Spatial and Nonspatial Visual Information in Parietal Cortex , 2009, The Journal of Neuroscience.

[74]  Yaoda Xu,et al.  Representing connected and disconnected shapes in human inferior intraparietal sulcus , 2008, NeuroImage.

[75]  S. Corkin.  What's new with the amnesic patient H.M.? , 2002, Nature Reviews Neuroscience.

[76]  Yaoda Xu,et al.  The Neural Fate of Task-Irrelevant Features in Object-Based Processing , 2010, The Journal of Neuroscience.

[77]  M. D’Esposito.  Working memory. , 2008, Handbook of clinical neurology.

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

[79]  Maro G. Machizawa,et al.  Capacity limit of visual short-term memory in human posterior parietal cortex , 2004 .

[80]  G. Woodman,et al.  Neural fate of ignored stimuli: dissociable effects of perceptual and working memory load , 2004, Nature Neuroscience.

[81]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

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

[83]  John-Dylan Haynes,et al.  Decoding complex flow-field patterns in visual working memory , 2014, NeuroImage.

[84]  Yaoda Xu,et al.  Distinctive Neural Mechanisms Supporting Visual Object Individuation and Identification , 2009, Journal of Cognitive Neuroscience.

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

[86]  D. Broadbent.  Perception and communication , 1958 .

[87]  Adam C. Riggall,et al.  The Relationship between Working Memory Storage and Elevated Activity as Measured with Functional Magnetic Resonance Imaging , 2012, The Journal of Neuroscience.

[88]  N. Lavie.  Distracted and confused?: Selective attention under load , 2005, Trends in Cognitive Sciences.

[89]  B. Milner,et al.  Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M.☆ , 1968 .

[90]  Edward F. Ester,et al.  PSYCHOLOGICAL SCIENCE Research Article Stimulus-Specific Delay Activity in Human Primary Visual Cortex , 2022 .

[91]  M. Goldberg,et al.  The representation of visual salience in monkey parietal cortex , 1998, Nature.

[92]  S. Petersen,et al.  A dual-networks architecture of top-down control , 2008, Trends in Cognitive Sciences.

[93]  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.

[94]  R. Marois,et al.  Capacity limits of information processing in the brain , 2005, Trends in Cognitive Sciences.

[95]  K. Grill-Spector,et al.  The dynamics of object-selective activation correlate with recognition performance in humans , 2000, Nature Neuroscience.

[96]  John Duncan,et al.  Attentional modulation of stimulus representation in human fronto-parietal cortex , 2009, NeuroImage.

[97]  W. A. Phillips.  On the distinction between sensory storage and short-term visual memory , 1974 .

[98]  R. Goebel,et al.  Individual faces elicit distinct response patterns in human anterior temporal cortex , 2007, Proceedings of the National Academy of Sciences.

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

[100]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

[101]  Phonologic Mediation is Fundamental to Reading , 2012 .

[102]  M. Pinsk,et al.  Push-pull mechanism of selective attention in human extrastriate cortex. , 2004, Journal of neurophysiology.

[103]  P. Cavanagh,et al.  The Capacity of Visual Short-Term Memory is Set Both by Visual Information Load and by Number of Objects , 2004, Psychological science.

[104]  Chih-Jen Lin,et al.  LIBSVM: A library for support vector machines , 2011, TIST.