Maintaining coherence of dynamic objects requires coordination of neural systems extended from anterior frontal to posterior parietal brain cortices

Object representation in visual working memory enables humans to perceive a consistent visual world and must satisfy two attributes: coherence and dynamic updating. The present study measured brain activity using functional magnetic resonance imaging (fMRI) during the multiple object permanence tracking (MOPT) task, which requires observers to process simultaneously both coherence maintenance and dynamic updating of objects. Whole brain analysis revealed anterior and ventral parts of frontal area and dorsal frontoparietal activation during both object-moving and object-stationary conditions. Subsequent region-of-interest analyses in the anterior/ventral frontal and the dorsal frontoparietal regions revealed that these two systems engage the two different cognitive processes involved in the MOPT task, with coherency maintenance processed in the anterior/ventral frontal areas and spatial processing in the dorsal frontoparietal network. These results suggest that cooperation between these two systems underpins object representations in visual working memory.

[1]  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.

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

[3]  M. D’Esposito,et al.  Functional MRI studies of spatial and nonspatial working memory. , 1998, Brain research. Cognitive brain research.

[4]  Leslie G. Ungerleider,et al.  Object and spatial visual working memory activate separate neural systems in human cortex. , 1996, Cerebral cortex.

[5]  Jun Saiki,et al.  Spatiotemporal characteristics of dynamic feature binding in visual working memory , 2003, Vision Research.

[6]  A. Dale,et al.  Functional–Anatomic Study of Episodic Retrieval II. Selective Averaging of Event-Related fMRI Trials to Test the Retrieval Success Hypothesis , 1998, NeuroImage.

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

[8]  Alan C. Evans,et al.  Memory for object features versus memory for object location: a positron-emission tomography study of encoding and retrieval processes , 1996 .

[9]  E. Tulving Episodic memory and common sense: how far apart? , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[10]  Edward E. Smith,et al.  Spatial working memory in humans as revealed by PET , 1993, Nature.

[11]  J. D. E. Gabrieli,et al.  Integration of diverse information in working memory within the frontal lobe , 2000, Nature Neuroscience.

[12]  P. Cavanagh,et al.  Cortical fMRI activation produced by attentive tracking of moving targets. , 1998, Journal of neurophysiology.

[13]  Jun Saiki,et al.  Feature binding in object-file representations of multiple moving items. , 2003, Journal of vision.

[14]  D. Schacter,et al.  Functional–Anatomic Study of Episodic Retrieval Using fMRI I. Retrieval Effort versus Retrieval Success , 1998, NeuroImage.

[15]  Alan Cowey,et al.  Temporal aspects of visual search studied by transcranial magnetic stimulation , 1997, Neuropsychologia.

[16]  J. Jay Todd,et al.  Capacity limit of visual short-term memory in human posterior parietal cortex , 2004, Nature.

[17]  M. Corbetta,et al.  Superior Parietal Cortex Activation During Spatial Attention Shifts and Visual Feature Conjunction , 1995, Science.

[18]  P. Cavanagh,et al.  Attention Response Functions Characterizing Brain Areas Using fMRI Activation during Parametric Variations of Attentional Load , 2001, Neuron.

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

[20]  Z W Pylyshyn,et al.  Tracking multiple independent targets: evidence for a parallel tracking mechanism. , 1988, Spatial vision.

[21]  S. Carey,et al.  Infants’ Metaphysics: The Case of Numerical Identity , 1996, Cognitive Psychology.

[22]  E. Tulving,et al.  Task-related and item-related brain processes of memory retrieval. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Marcia K. Johnson,et al.  fMRI evidence of age-related hippocampal dysfunction in feature binding in working memory. , 2000, Brain research. Cognitive brain research.

[24]  Hiroshi Niino,et al.  4. Inner structure of the head of axisymmetric gravity currents , 2000 .

[25]  A. Owen,et al.  Anterior prefrontal cortex: insights into function from anatomy and neuroimaging , 2004, Nature Reviews Neuroscience.

[26]  Endel Tulving,et al.  Prefrontal cortex and episodic memory retrieval mode. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[27]  A. Treisman,et al.  Binding in short-term visual memory. , 2002, Journal of experimental psychology. General.

[28]  H Pashler,et al.  Familiarity and visual change detection , 1988, Perception & psychophysics.

[29]  D. Perrett,et al.  Integration of form and motion in the anterior superior temporal polysensory area (STPa) of the macaque monkey. , 1996, Journal of neurophysiology.

[30]  Alan C. Evans,et al.  Specific Involvement of Human Parietal Systems and the Amygdala in the Perception of Biological Motion , 1996, The Journal of Neuroscience.

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

[32]  Scott A. Huettel,et al.  Dissociating the Neural Mechanisms of Visual Attention in Change Detection Using Functional MRI , 2001, Journal of Cognitive Neuroscience.

[33]  E. Stein,et al.  Multiple Neuronal Networks Mediate Sustained Attention , 2003, Journal of Cognitive Neuroscience.

[34]  C. Frith,et al.  Neural correlates of change detection and change blindness , 2001, Nature Neuroscience.

[35]  A. Treisman,et al.  Parietal contributions to visual feature binding: evidence from a patient with bilateral lesions , 1995, Science.

[36]  A R McIntosh,et al.  Functional brain maps of retrieval mode and recovery of episodic information , 1995, Neuroreport.

[37]  C. Koch,et al.  Brain Areas Specific for Attentional Load in a Motion-Tracking Task , 2001, Journal of Cognitive Neuroscience.

[38]  S C Rao,et al.  Integration of what and where in the primate prefrontal cortex. , 1997, Science.