Cortical Circuit for Binding Object Identity and Location During Multiple-Object Tracking

Abstract Sustained multifocal attention for moving targets requires binding object identities with their locations. The brain mechanisms of identity‐location binding during attentive tracking have remained unresolved. In 2 functional magnetic resonance imaging experiments, we measured participants’ hemodynamic activity during attentive tracking of multiple objects with equivalent (multiple‐object tracking) versus distinct (multiple identity tracking, MIT) identities. Task load was manipulated parametrically. Both tasks activated large frontoparietal circuits. MIT led to significantly increased activity in frontoparietal and temporal systems subserving object recognition and working memory. These effects were replicated when eye movements were prohibited. MIT was associated with significantly increased functional connectivity between lateral temporal and frontal and parietal regions. We propose that coordinated activity of this network subserves identity‐location binding during attentive tracking.

[1]  R. Marois,et al.  "What" and "where" in the intraparietal sulcus: an FMRI study of object identity and location in visual short-term memory. , 2010, Cerebral cortex.

[2]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[3]  S. Yantis Multielement visual tracking: Attention and perceptual organization , 1992, Cognitive Psychology.

[4]  E. Granholm,et al.  Pupillary responses index cognitive resource limitations. , 1996, Psychophysiology.

[5]  Todd S Horowitz,et al.  The what–where trade-off in multiple-identity tracking , 2011, Attention, perception & psychophysics.

[6]  Markus H. Sneve,et al.  Pupil size signals mental effort deployed during multiple object tracking and predicts brain activity in the dorsal attention network and the locus coeruleus. , 2014, Journal of Vision.

[7]  T. Paus,et al.  Cortical regions involved in eye movements, shifts of attention, and gaze perception , 2005, Human brain mapping.

[8]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[9]  Terry M. Peters,et al.  3D statistical neuroanatomical models from 305 MRI volumes , 1993, 1993 IEEE Conference Record Nuclear Science Symposium and Medical Imaging Conference.

[10]  Mark D'Esposito,et al.  From cognitive to neural models of working memory , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[11]  Mikko Sams,et al.  Synchronous brain activity across individuals underlies shared psychological perspectives , 2014, NeuroImage.

[12]  Jari Saramäki,et al.  Reorganization of functionally connected brain subnetworks in high‐functioning autism , 2015, Human brain mapping.

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

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

[15]  Adam Ferguson,et al.  The Identity-Location Binding Problem , 2015, Cogn. Sci..

[16]  J. Wolfe,et al.  Tracking unique objects , 2007, Perception & psychophysics.

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

[18]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[19]  T. Paus Location and function of the human frontal eye-field: A selective review , 1996, Neuropsychologia.

[20]  Katherine M. Armstrong,et al.  Visual and oculomotor selection: links, causes and implications for spatial attention , 2006, Trends in Cognitive Sciences.

[21]  N. J. Herrod,et al.  Redefining the functional organization of working memory processes within human lateral prefrontal cortex , 1999, The European journal of neuroscience.

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

[23]  Thomas Serre,et al.  Reading the mind's eye: Decoding category information during mental imagery , 2010, NeuroImage.

[24]  J. Hyönä,et al.  Position tracking and identity tracking are separate systems: Evidence from eye movements , 2016, Cognition.

[25]  S. Kosslyn,et al.  Brain areas underlying visual mental imagery and visual perception: an fMRI study. , 2004, Brain research. Cognitive brain research.

[26]  Z. Pylyshyn Some puzzling findings in multiple object tracking: I. Tracking without keeping track of object identities , 2004 .

[27]  A. Amedi,et al.  Functional imaging of human crossmodal identification and object recognition , 2005, Experimental Brain Research.

[28]  J. G. Snodgrass,et al.  A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. , 1980, Journal of experimental psychology. Human learning and memory.

[29]  P. Howe,et al.  The more often you see an object, the easier it becomes to track it. , 2010, Journal of vision.

[30]  Angela R Laird,et al.  Comparison of Fourier and wavelet resampling methods , 2004, Magnetic resonance in medicine.

[31]  J. Wolfe,et al.  Using Fmri to Distinguish Components of the Multiple Object Tracking Task , 1994 .

[32]  Jukka Hyönä,et al.  Dynamic binding of identity and location information: A serial model of multiple identity tracking , 2008, Cognitive Psychology.

[33]  P. Cavanagh,et al.  Tracking multiple targets with multifocal attention , 2005, Trends in Cognitive Sciences.

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

[35]  Kathryn M. McMillan,et al.  N‐back working memory paradigm: A meta‐analysis of normative functional neuroimaging studies , 2005, Human brain mapping.

[36]  J. Hyönä,et al.  Is multiple object tracking carried out automatically by an early vision mechanism independent of higher‐order cognition? An individual difference approach , 2004 .

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

[38]  R. Cameron Craddock,et al.  A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics , 2013, NeuroImage.