Distinct and overlapping fMRI activation networks for processing of novel identities and locations of objects

The ventral visual stream processes information about the identity of objects (‘what’), whereas the dorsal stream processes the spatial locations of objects (‘where’). There is a corresponding, although disputed, distinction for the ventrolateral and dorsolateral prefrontal areas. Furthermore, there seems to be a distinction between the anterior and posterior medial temporal lobe (MTL) structures in the processing of novel items and new spatial arrangements, respectively. Functional differentiation of the intermediary mid‐line cortical and temporal neocortical structures that communicate with the occipitotemporal, occipitoparietal, prefrontal, and MTL structures, however, is unclear. Therefore, in the present functional magnetic resonance imaging (fMRI) study, we examined whether the distinction among the MTL structures extends to these closely connected cortical areas. The most striking difference in the fMRI responses during visual presentation of changes in either items or their locations was the bilateral activation of the temporal lobe and ventrolateral prefrontal cortical areas for novel object identification in contrast to wide parietal and dorsolateral prefrontal activation for the novel locations of objects. An anterior‐posterior distinction of fMRI responses similar to the MTL was observed in the cingulate/retrosplenial, and superior and middle temporal cortices. In addition to the distinct areas of activation, certain frontal, parietal, and temporo‐occipital areas responded to both object and spatial novelty, suggesting a common attentional network for both types of changes in the visual environment. These findings offer new insights to the functional roles and intrinsic specialization of the cingulate/retrosplenial, and lateral temporal cortical areas in visuospatial cognition.

[1]  M. Pihlajamäki,et al.  Visual Processing of Coherent Rotation in the Central Visual Field: An fMRI Study , 2003, Perception.

[2]  Karl J. Friston,et al.  Assessing the significance of focal activations using their spatial extent , 1994, Human brain mapping.

[3]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Projections to the neocortex , 2002, The Journal of comparative neurology.

[4]  P. Goldman-Rakic,et al.  Human Brain Mapping 6:14–32(1998) � Dissociation of Mnemonic and Perceptual Processes During Spatial and Nonspatial Working Memory Using fMRI , 2022 .

[5]  N. Kanwisher,et al.  The Generality of Parietal Involvement in Visual Attention , 1999, Neuron.

[6]  S. Carlson,et al.  Distribution of cortical activation during visuospatial n-back tasks as revealed by functional magnetic resonance imaging. , 1998, Cerebral cortex.

[7]  M. Mishkin,et al.  A selective mnemonic role for the hippocampus in monkeys: memory for the location of objects , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  F. Gray,et al.  Bilateral infarction of the anterior cingulate gyri and of the fornices Report of a case , 1981, Journal of the Neurological Sciences.

[9]  G. J. Romanes,et al.  The Neocortex of Macaca mulatta , 1948 .

[10]  Adrian M. Owen,et al.  The role of the lateral frontal cortex in mnemonic processing: the contribution of functional neuroimaging , 2000, Experimental Brain Research.

[11]  M. D’Esposito,et al.  Environmental Knowledge Is Subserved by Separable Dorsal/Ventral Neural Areas , 1997, The Journal of Neuroscience.

[12]  C. Stern,et al.  An fMRI Study of the Role of the Medial Temporal Lobe in Implicit and Explicit Sequence Learning , 2003, Neuron.

[13]  J. Downar,et al.  A multimodal cortical network for the detection of changes in the sensory environment , 2000, Nature Neuroscience.

[14]  J Xiong,et al.  Assessment and optimization of functional MRI analyses , 1996, Human brain mapping.

[15]  E. Maguire The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings. , 2001, Scandinavian journal of psychology.

[16]  L M Vaina,et al.  Functional segregation of color and motion processing in the human visual cortex: clinical evidence. , 1994, Cerebral cortex.

[17]  Bettina Sorger,et al.  Human Cortical Object Recognition from a Visual Motion Flowfield , 2003, The Journal of Neuroscience.

[18]  Leslie G. Ungerleider,et al.  Dissociation of object and spatial visual processing pathways in human extrastriate cortex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

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

[20]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents , 1994, The Journal of comparative neurology.

[21]  Edward E. Smith,et al.  Temporal dynamics of brain activation during a working memory task , 1997, Nature.

[22]  Ravi S. Menon,et al.  Differential Effects of Viewpoint on Object-Driven Activation in Dorsal and Ventral Streams , 2002, Neuron.

[23]  G. Rainer,et al.  Cognitive neuroscience: Neural mechanisms for detecting and remembering novel events , 2003, Nature Reviews Neuroscience.

[24]  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.

[25]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[26]  D. Amaral,et al.  Macaque monkey retrosplenial cortex: II. Cortical afferents , 2003, The Journal of comparative neurology.

[27]  W. Ritchie Russell,et al.  Dissociated visual perceptual and spatial deficits in focal lesions of the right hemisphere , 1969 .

[28]  J. Gabrieli,et al.  Neural Correlates of Encoding Space from Route and Survey Perspectives , 2002, The Journal of Neuroscience.

[29]  Seralynne D Vann,et al.  Extensive cytotoxic lesions of the rat retrosplenial cortex reveal consistent deficits on tasks that tax allocentric spatial memory. , 2002, Behavioral neuroscience.

[30]  Malcolm P. Young,et al.  Objective analysis of the topological organization of the primate cortical visual system , 1992, Nature.

[31]  B. Postle,et al.  An fMRI Investigation of Cortical Contributions to Spatial and Nonspatial Visual Working Memory , 2000, NeuroImage.

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

[33]  M Petrides,et al.  Architecture and connections of retrosplenial area 30 in the rhesus monkey (macaca mulatta). , 1999, The European journal of neuroscience.

[34]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[35]  J. Gore,et al.  A Stimulus-Driven Approach to Object Identity and Location Processing in the Human Brain , 2000, Neuron.

[36]  P. Goldman-Rakic,et al.  Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  S. Mizumori,et al.  Temporary Inactivation of the Retrosplenial Cortex Causes a Transient Reorganization of Spatial Coding in the Hippocampus , 2001, The Journal of Neuroscience.

[38]  W. Penny,et al.  Random-Effects Analysis , 2002 .

[39]  A. Nobre,et al.  The Large-Scale Neural Network for Spatial Attention Displays Multifunctional Overlap But Differential Asymmetry , 1999, NeuroImage.

[40]  D. Pandya,et al.  Post‐rolandic cortical projections of the superior temporal sulcus in the rhesus monkey , 1991, The Journal of comparative neurology.

[41]  G. V. Van Hoesen,et al.  Prosopagnosia , 1982, Neurology.

[42]  M. Mishkin,et al.  Object Recognition and Location Memory in Monkeys with Excitotoxic Lesions of the Amygdala and Hippocampus , 1998, The Journal of Neuroscience.

[43]  G. Mangun,et al.  The neural mechanisms of top-down attentional control , 2000, Nature Neuroscience.

[44]  Gereon R Fink,et al.  Cerebral correlates of alerting, orienting and reorienting of visuospatial attention: an event-related fMRI study , 2004, NeuroImage.

[45]  Alan C. Evans,et al.  A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[46]  G. Egan,et al.  Widespread Dorsal Stream Activation during a Parametric Mental Rotation Task, Revealed with Functional Magnetic Resonance Imaging , 2002, NeuroImage.

[47]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[48]  P. Goldman-Rakic,et al.  Dissociation of object and spatial processing domains in primate prefrontal cortex. , 1993, Science.

[49]  Maija Pihlajamäki,et al.  Visual presentation of novel objects and new spatial arrangements of objects differentially activates the medial temporal lobe subareas in humans , 2004, The European journal of neuroscience.

[50]  Malcolm W. Brown,et al.  Different Contributions of the Hippocampus and Perirhinal Cortex to Recognition Memory , 1999, The Journal of Neuroscience.

[51]  K. Uğurbil,et al.  Neural correlates of visual form and visual spatial processing , 1999, Human brain mapping.

[52]  M. Bar,et al.  Cortical Analysis of Visual Context , 2003, Neuron.

[53]  N. Takahashi,et al.  Pure topographic disorientation due to right retrosplenial lesion , 1997, Neurology.

[54]  M. Raichle,et al.  Localization of a human system for sustained attention by positron emission tomography , 1991, Nature.