Localizing subprocesses of visual search by correlating local brain activation in fMRI with response time model parameters

In a complex cognitive task such as overt visual search, several subprocesses interact in quick alternation, such as attentional selections (i.e., spatially constrained modulation of perception) and attentional shifts/eye movements. Since temporal resolution in fMRI is low, it is difficult to assign local brain activations to these subprocesses with traditional analysis. The present paper investigates a new approach: with the response time model STRAVIS [Müller-Plath G, Pollmann S. Determining subprocesses of visual feature search with reaction time models. Psychol Res 2003;67:80-105], a visual search process is decomposed into hypothetical cognitive subprocesses and quantitatively described by individually estimated parameters like the size of the attentional focus or the attentional dwell time. In the fMRI experiment we administered the search task, correlated the estimated model parameter values for dwell time and (reciprocal) focus size to BOLD-responses, and thereby identified putative neural networks that are jointly active in the task but differentially specialized to the subprocesses attentional selection and attentional shift. First, the methodological approach was validated by the results agreeing with the literature for predefined brain areas. Second, our findings might add to the literature by specifying several more brain areas probably belonging to the two networks. Third, compared to a more traditional data analysis (contrasts of mean BOLD responses in the factorial experimental design) the method of individually correlating model parameters to BOLD proved superior provided one accepts the theoretical assumptions underlying each of the approaches. Our results demonstrate the utility of combining mathematical modeling and fMRI to investigate the neural substrates of a complex task such as visual search.

[1]  Jia Fc,et al.  [Event-related functional magnetic resonance imaging]. , 2001, Sheng li ke xue jin zhan [Progress in physiology].

[2]  Z Li,et al.  Contextual influences in V1 as a basis for pop out and asymmetry in visual search. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[3]  A. Berthoz,et al.  An anatomical landmark for the supplementary eye fields in human revealed with functional magnetic resonance imaging. , 1999, Cerebral cortex.

[4]  T. Egner,et al.  Cognitive control mechanisms resolve conflict through cortical amplification of task-relevant information , 2005, Nature Neuroscience.

[5]  J. Reynolds,et al.  Attentional modulation of visual processing. , 2004, Annual review of neuroscience.

[6]  G Lohmann,et al.  LIPSIA--a new software system for the evaluation of functional magnetic resonance images of the human brain. , 2001, Computerized medical imaging and graphics : the official journal of the Computerized Medical Imaging Society.

[7]  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 .

[8]  Zhaoping Li A saliency map in primary visual cortex , 2002, Trends in Cognitive Sciences.

[9]  S. Pollmann,et al.  Object working memory and visuospatial processing: functional neuroanatomy analyzed by event-related fMRI , 2000, Experimental Brain Research.

[10]  B. C. Motter Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. , 1993, Journal of neurophysiology.

[11]  J. Wolfe,et al.  What Can 1 Million Trials Tell Us About Visual Search? , 1998 .

[12]  L. Nyberg,et al.  Common fronto-parietal activity in attention, memory, and consciousness: Shared demands on integration? , 2005, Consciousness and Cognition.

[13]  Scott E. Maxwell,et al.  Designing Experiments and Analyzing Data: A Model Comparison Perspective , 1990 .

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

[15]  M. Rushworth,et al.  Attention Systems and the Organization of the Human Parietal Cortex , 2001, The Journal of Neuroscience.

[16]  E. DeYoe,et al.  Mapping striate and extrastriate visual areas in human cerebral cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[17]  M. Corbetta,et al.  Neural Systems for Visual Orienting and Their Relationships to Spatial Working Memory , 2002, Journal of Cognitive Neuroscience.

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

[19]  Stefan Pollmann,et al.  Determining subprocesses of visual feature search with reaction time models , 2003, Psychological research.

[20]  Jacob Cohen Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

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

[22]  J. Wolfe,et al.  Guided Search 2.0 A revised model of visual search , 1994, Psychonomic bulletin & review.

[23]  T. Moore,et al.  Microstimulation of the frontal eye field and its effects on covert spatial attention. , 2004, Journal of neurophysiology.

[24]  Notger G. Müller,et al.  The functional neuroanatomy of visual conjunction search: a parametric fMRI study , 2003, NeuroImage.

[25]  Leslie G. Ungerleider,et al.  Sustained Activity in the Medial Wall during Working Memory Delays , 1998, The Journal of Neuroscience.

[26]  J. Gallant,et al.  Goal-Related Activity in V4 during Free Viewing Visual Search Evidence for a Ventral Stream Visual Salience Map , 2003, Neuron.

[27]  Michael S. Beauchamp,et al.  A Parametric fMRI Study of Overt and Covert Shifts of Visuospatial Attention , 2001, NeuroImage.

[28]  R Verleger,et al.  Lateralized human cortical activity for shifting visuospatial attention and initiating saccades. , 1998, Journal of neurophysiology.

[29]  A. Treisman,et al.  Conjunction search revisited , 1990 .

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

[31]  R. Desimone,et al.  Competitive Mechanisms Subserve Attention in Macaque Areas V2 and V4 , 1999, The Journal of Neuroscience.

[32]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[33]  S. Zeki,et al.  The architecture of the colour centre in the human visual brain: new results and a review * , 2000, The European journal of neuroscience.

[34]  A Treisman,et al.  Feature analysis in early vision: evidence from search asymmetries. , 1988, Psychological review.

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

[36]  H. Spekreijse,et al.  Correspondence of presaccadic activity in the monkey primary visual cortex with saccadic eye movements. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[37]  M. Sereno,et al.  Mapping of Contralateral Space in Retinotopic Coordinates by a Parietal Cortical Area in Humans , 2001, Science.

[38]  P H Schiller,et al.  Visual representations during saccadic eye movements. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Edgar Erdfelder,et al.  GPOWER: A general power analysis program , 1996 .

[40]  E. DeYoe,et al.  A physiological correlate of the 'spotlight' of visual attention , 1999, Nature Neuroscience.

[41]  O Josephs,et al.  Event-related functional magnetic resonance imaging: modelling, inference and optimization. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[42]  Katherine M. Armstrong,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2003, Nature.

[43]  M. Mesulam A cortical network for directed attention and unilateral neglect , 1981, Annals of neurology.

[44]  Leslie G. Ungerleider,et al.  Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. , 1998, Science.

[45]  Leslie G. Ungerleider,et al.  Neuroimaging Studies of Attention: From Modulation of Sensory Processing to Top-Down Control , 2003, The Journal of Neuroscience.

[46]  M. Mesulam,et al.  Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[47]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[48]  M. Goldberg,et al.  The role of the parietal cortex in the neural processing of saccadic eye movements. , 2003, Advances in neurology.

[49]  B. J. McCurtain,et al.  Dorsal cortical regions subserving visually guided saccades in humans: an fMRI study. , 1998, Cerebral cortex.

[50]  Richard S. J. Frackowiak,et al.  Functional localization of the system for visuospatial attention using positron emission tomography. , 1997, Brain : a journal of neurology.