Cortical Areas Involved in Object, Background, and Object-Background Processing Revealed with Functional Magnetic Resonance Adaptation

Previous work has suggested that object and place processing are neuroanatomically dissociated in ventral visual areas under conditions of passive viewing. It has also been shown that the hippocampus and parahippocampal gyrus mediate the integration of objects with background scenes in functional imaging studies, but only when encoding or retrieval processes have been directed toward the relevant stimuli. Using functional magnetic resonance adaptation, we demonstrated that object, background scene, and contextual integration of selectively repeated objects and background scenes could be dissociated during the passive viewing of naturalistic pictures involving object-scene pairings. Specifically, bilateral fusiform areas showed adaptation to object repetition, regardless of whether the associated scene was novel or repeated, suggesting sensitivity to object processing. Bilateral parahippocampal regions showed adaptation to background scene repetition, regardless of whether the focal object was novel or repeated, suggesting selectivity for background scene processing. Finally, bilateral parahippocampal regions distinct from those involved in scene processing and the right hippocampus showed adaptation only when the unique pairing of object with background scene was repeated, suggesting that these regions perform binding operations.

[1]  D C Park,et al.  Picture memory in older adults: effects of contextual detail at encoding and retrieval. , 1984, Journal of gerontology.

[2]  P M Grasby,et al.  Brain systems for encoding and retrieval of auditory-verbal memory. An in vivo study in humans. , 1995, Brain : a journal of neurology.

[3]  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.

[4]  Marcia K. Johnson,et al.  Feature memory and binding in young and older adults , 1996, Memory & cognition.

[5]  T. Allison,et al.  Differential Sensitivity of Human Visual Cortex to Faces, Letterstrings, and Textures: A Functional Magnetic Resonance Imaging Study , 1996, The Journal of Neuroscience.

[6]  Leslie G. Ungerleider,et al.  Face encoding and recognition in the human brain. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Charles L. Wilson,et al.  Single Neuron Activity in Human Hippocampus and Amygdala during Recognition of Faces and Objects , 1997, Neuron.

[8]  Leslie G. Ungerleider,et al.  Selective attention to face identity and color studied with f MRI , 1997, Human brain mapping.

[9]  H Eichenbaum,et al.  Declarative memory: insights from cognitive neurobiology. , 1997, Annual review of psychology.

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

[11]  M. Raichle,et al.  Anatomic Localization and Quantitative Analysis of Gradient Refocused Echo-Planar fMRI Susceptibility Artifacts , 1997, NeuroImage.

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

[13]  B. Weber,et al.  Human hippocampus establishes associations in memory , 1997, Hippocampus.

[14]  A. Dale,et al.  Selective averaging of rapidly presented individual trials using fMRI , 1997, Human brain mapping.

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

[16]  N. Kanwisher,et al.  Covert visual attention modulates face-specific activity in the human fusiform gyrus: fMRI study. , 1998, Journal of neurophysiology.

[17]  D J Wyper,et al.  Associative encoding of pictures activates the medial temporal lobes , 1998, Human brain mapping.

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

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

[20]  H G Wieser,et al.  Human hippocampus associates information in memory. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[21]  N. Cohen,et al.  Hippocampal system and declarative (relational) memory: Summarizing the data from functional neuroimaging studies , 1999, Hippocampus.

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

[23]  Marcia K. Johnson,et al.  Aging and reflective processes of working memory: binding and test load deficits. , 2000, Psychology and aging.

[24]  C. Jack,et al.  Memory and MRI-based hippocampal volumes in aging and AD , 2000, Neurology.

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

[26]  B. Knowlton,et al.  Remembering episodes: a selective role for the hippocampus during retrieval , 2000, Nature Neuroscience.

[27]  M. Bar,et al.  Cortical Mechanisms Specific to Explicit Visual Object Recognition , 2001, Neuron.

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

[29]  A. T. Smith,et al.  Estimating receptive field size from fMRI data in human striate and extrastriate visual cortex. , 2001, Cerebral cortex.

[30]  Craig E. L. Stark,et al.  When zero is not zero: The problem of ambiguous baseline conditions in fMRI , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[31]  N. Kanwisher,et al.  Neuroimaging of cognitive functions in human parietal cortex , 2001, Current Opinion in Neurobiology.

[32]  N. Kanwisher,et al.  The lateral occipital complex and its role in object recognition , 2001, Vision Research.

[33]  E. Maguire,et al.  The Human Hippocampus and Spatial and Episodic Memory , 2002, Neuron.

[34]  John C Gore,et al.  The role of the parietal cortex in visual feature binding , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[35]  T. Shallice,et al.  Face repetition effects in implicit and explicit memory tests as measured by fMRI. , 2002, Cerebral cortex.

[36]  O Josephs,et al.  Dissociable Human Perirhinal, Hippocampal, and Parahippocampal Roles during Verbal Encoding , 2002, The Journal of Neuroscience.

[37]  M. Behrmann,et al.  Impact of learning on representation of parts and wholes in monkey inferotemporal cortex , 2002, Nature Neuroscience.

[38]  M. Rugg,et al.  Repetition effects elicited by objects and their contexts: An fMRI study , 2003, Human brain mapping.

[39]  K. Grill-Spector The neural basis of object perception , 2003, Current Opinion in Neurobiology.

[40]  Douglas C. Noll,et al.  Working Memory for Complex Scenes: Age Differences in Frontal and Hippocampal Activations , 2003, Journal of Cognitive Neuroscience.

[41]  Michael W. L. Chee,et al.  Common and Segregated Neuronal Networks for Different Languages Revealed Using Functional Magnetic Resonance Adaptation , 2003, Journal of Cognitive Neuroscience.

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

[43]  Paul E. Downing,et al.  Viewpoint-Specific Scene Representations in Human Parahippocampal Cortex , 2003, Neuron.

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

[45]  J-M Hopf,et al.  Dynamics of feature binding during object-selective attention , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[46]  M. Chee,et al.  Functional Imaging of Working Memory after 24 Hr of Total Sleep Deprivation , 2004, The Journal of Neuroscience.

[47]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[48]  Charles E Connor,et al.  Underlying principles of visual shape selectivity in posterior inferotemporal cortex , 2004, Nature Neuroscience.

[49]  Kerry Lee,et al.  Recognition memory for studied words is determined by cortical activation differences at encoding but not during retrieval , 2004, NeuroImage.

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

[51]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.