Neurocognitive Development of the Resolution of Selective Visuo-Spatial Attention: Functional MRI Evidence From Object Tracking

Our ability to select relevant information from the environment is limited by the resolution of attention – i.e., the minimum size of the region that can be selected. Neural mechanisms that underlie this limit and its development are not yet understood. Functional magnetic resonance imaging (fMRI) was performed during an object tracking task in 7- and 11-year-old children, and in young adults. Object tracking activated canonical fronto-parietal attention systems and motion-sensitive area MT in children as young as 7 years. Object tracking performance improved with age, together with stronger recruitment of parietal attention areas and a shift from low-level to higher-level visual areas. Increasing the required resolution of spatial attention – which was implemented by varying the distance between target and distractors in the object tracking task – led to activation increases in fronto-insular cortex, medial frontal cortex including anterior cingulate cortex (ACC) and supplementary motor area, superior colliculi, and thalamus. This core circuitry for attentional precision was recruited by all age groups, but ACC showed an age-related activation reduction. Our results suggest that age-related improvements in selective visual attention and in the resolution of attention are characterized by an increased use of more functionally specialized brain regions during the course of development.

[1]  J. Stiles,et al.  The development of visuospatial processing , 2020, Neural Circuit and Cognitive Development.

[2]  Damien A. Fair,et al.  Development of large-scale functional networks from birth to adulthood: A guide to the neuroimaging literature , 2017, NeuroImage.

[3]  Catherine Fassbender,et al.  Minimizing noise in pediatric task-based functional MRI; Adolescents with developmental disabilities and typical development , 2017, NeuroImage.

[4]  T. Moore,et al.  Neural Mechanisms of Selective Visual Attention. , 2017, Annual review of psychology.

[5]  Mukesh Dhamala,et al.  The salience network dynamics in perceptual decision-making , 2016, NeuroImage.

[6]  Kaustubh Supekar,et al.  Distinct Global Brain Dynamics and Spatiotemporal Organization of the Salience Network , 2016, PLoS biology.

[7]  Mukesh Dhamala,et al.  Interactions Among the Brain Default-Mode, Salience, and Central-Executive Networks During Perceptual Decision-Making of Moving Dots , 2016, Brain Connect..

[8]  Markus Huff,et al.  Viewpoint matters: Exploring the involvement of reference frames in multiple object tracking from a developmental perspective , 2016 .

[9]  K. Hwang,et al.  The Contribution of Network Organization and Integration to the Development of Cognitive Control , 2015, PLoS biology.

[10]  Lars T. Westlye,et al.  Functional connectivity indicates differential roles for the intraparietal sulcus and the superior parietal lobule in multiple object tracking , 2015, NeuroImage.

[11]  D. Bassett,et al.  Emergence of system roles in normative neurodevelopment , 2015, Proceedings of the National Academy of Sciences.

[12]  Dima Amso,et al.  The attentive brain: insights from developmental cognitive neuroscience , 2015, Nature Reviews Neuroscience.

[13]  C. Lange-Küttner,et al.  How to learn places without spatial concepts: Does the what-and-where reaction time system in children regulate learning during stimulus repetition? , 2015, Brain and Cognition.

[14]  Valerio Santangelo Forced to remember: When memory is biased by salient information , 2015, Behavioural Brain Research.

[15]  Lucina Q. Uddin,et al.  Asymmetric development of dorsal and ventral attention networks in the human brain , 2015, Developmental Cognitive Neuroscience.

[16]  Jonathan D. Power,et al.  Recent progress and outstanding issues in motion correction in resting state fMRI , 2015, NeuroImage.

[17]  L. Uddin Salience processing and insular cortical function and dysfunction , 2014, Nature Reviews Neuroscience.

[18]  J. Siderov,et al.  Foveal crowding differs in children and adults. , 2014, Journal of vision.

[19]  Marko Wilke,et al.  Isolated Assessment of Translation or Rotation Severely Underestimates the Effects of Subject Motion in fMRI Data , 2014, PloS one.

[20]  Jonathan P. McNulty,et al.  The salience network is responsible for switching between the default mode network and the central executive network: Replication from DCM , 2014, NeuroImage.

[21]  Soonjo Hwang,et al.  Neurodevelopmental changes in the responsiveness of systems involved in top down attention and emotional responding , 2014, Neuropsychologia.

[22]  O. Houdé,et al.  Changes in Cortical Thickness in 6-Year-Old Children Open Their Mind to a Global Vision of the World , 2014, BioMed research international.

[23]  Jonathan D. Power,et al.  Statistical improvements in functional magnetic resonance imaging analyses produced by censoring high‐motion data points , 2014, Human brain mapping.

[24]  Björn N. S. Vlaskamp,et al.  Crowded visual search in children with normal vision and children with visual impairment , 2014, Vision Research.

[25]  Samuel D. Carpenter,et al.  Structural and Functional Rich Club Organization of the Brain in Children and Adults , 2014, PloS one.

[26]  K. Wolf,et al.  The development of attentional resolution , 2014 .

[27]  G. Glover,et al.  Causal interactions between fronto-parietal central executive and default-mode networks in humans , 2013, Proceedings of the National Academy of Sciences.

[28]  Benjamin O Turner,et al.  Number of events and reliability in fMRI , 2013, Cognitive, Affective, & Behavioral Neuroscience.

[29]  YuanYe Ma,et al.  Regulation of brain activity in the fusiform face and parahippocampal place areas in 7–11-year-old children , 2013, Brain and Cognition.

[30]  T. Horowitz,et al.  Swapping or dropping? Electrophysiological measures of difficulty during multiple object tracking , 2013, Cognition.

[31]  Swathi P. Iyer,et al.  Distinct neural signatures detected for ADHD subtypes after controlling for micro-movements in resting state functional connectivity MRI data , 2012, Front. Syst. Neurosci..

[32]  John L.R. Rubenstein,et al.  Neural circuit development and function in the healthy and diseased brain , 2013 .

[33]  Deepti R. Bathula,et al.  Distinct neuropsychological subgroups in typically developing youth inform heterogeneity in children with ADHD , 2012, Proceedings of the National Academy of Sciences.

[34]  Marko Wilke,et al.  An alternative approach towards assessing and accounting for individual motion in fMRI timeseries , 2012, NeuroImage.

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

[36]  Kaustubh Supekar,et al.  Developmental Maturation of Dynamic Causal Control Signals in Higher-Order Cognition: A Neurocognitive Network Model , 2012, PLoS Comput. Biol..

[37]  Markus Huff,et al.  Spatial reference in multiple object tracking. , 2012, Experimental psychology.

[38]  M. Carrasco Visual attention: The past 25 years , 2011, Vision Research.

[39]  O. Houdé,et al.  The Shift from Local to Global Visual Processing in 6-Year-Old Children Is Associated with Grey Matter Loss , 2011, PloS one.

[40]  A. Gazzaley,et al.  Neural indices of improved attentional modulation over middle childhood , 2011, Developmental Cognitive Neuroscience.

[41]  Robert H. Wurtz,et al.  Thalamic pathways for active vision , 2011, Trends in Cognitive Sciences.

[42]  L. Itti,et al.  Mechanisms of top-down attention , 2011, Trends in Neurosciences.

[43]  E. Macaluso,et al.  Stimulus-Driven Orienting of Visuo-Spatial Attention in Complex Dynamic Environments , 2011, Neuron.

[44]  P. Mazaika Motion Correction and Despike Functions , 2011 .

[45]  D. Maurer,et al.  Developmental changes during childhood in single-letter acuity and its crowding by surrounding contours. , 2010, Journal of experimental child psychology.

[46]  G. Scerif Attention trajectories, mechanisms and outcomes: at the interface between developing cognition and environment. , 2010, Developmental science.

[47]  Marc Joliot,et al.  Mapping numerical processing, reading, and executive functions in the developing brain: an fMRI meta-analysis of 52 studies including 842 children. , 2010, Developmental science.

[48]  Joel Stoddard,et al.  Atypical functional brain activation during a multiple object tracking task in girls with Turner syndrome: neurocorrelates of reduced spatiotemporal resolution. , 2010, American journal on intellectual and developmental disabilities.

[49]  S. Petersen,et al.  The “Task B problem” and other considerations in developmental functional neuroimaging , 2010, Human brain mapping.

[50]  G. Alvarez,et al.  The number of attentional foci and their precision are dissociated in the posterior parietal cortex. , 2010, Cerebral cortex.

[51]  Puiu F. Balan,et al.  Attention as a decision in information space , 2010, Trends in Cognitive Sciences.

[52]  Rozmin Halari,et al.  Effects of age and sex on developmental neural networks of visual–spatial attention allocation , 2010, NeuroImage.

[53]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[54]  Richard J Krauzlis,et al.  Inactivation of primate superior colliculus impairs covert selection of signals for perceptual judgments , 2010, Nature Neuroscience.

[55]  Beatriz Luna,et al.  The Maturation of Task Set-Related Activation Supports Late Developmental Improvements in Inhibitory Control , 2009, The Journal of Neuroscience.

[56]  J. Stiles,et al.  Hierarchical forms processing in adults and children. , 2009, Journal of experimental child psychology.

[57]  Jonathan D. Power,et al.  Functional Brain Networks Develop from a “Local to Distributed” Organization , 2009, PLoS Comput. Biol..

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

[59]  B. Scholl What Have We Learned about Attention from Multiple-Object Tracking (and Vice Versa)? , 2009 .

[60]  Beatriz Luna,et al.  Development of working memory maintenance. , 2009, Journal of neurophysiology.

[61]  M. E. Wheeler,et al.  Maturational changes in anterior cingulate and frontoparietal recruitment support the development of error processing and inhibitory control. , 2008, Cerebral cortex.

[62]  V. Menon,et al.  A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks , 2008, Proceedings of the National Academy of Sciences.

[63]  Ernst Martin,et al.  Dorsal stream development in motion and structure-from-motion perception , 2008, NeuroImage.

[64]  George A Alvarez,et al.  How many objects can you track? Evidence for a resource-limited attentive tracking mechanism. , 2007, Journal of vision.

[65]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[66]  J. Gottlieb From Thought to Action: The Parietal Cortex as a Bridge between Perception, Action, and Cognition , 2007, Neuron.

[67]  Jesper Tegnér,et al.  Brain activity related to working memory and distraction in children and adults. , 2006, Cerebral cortex.

[68]  Beatriz Luna,et al.  Brain Basis of Developmental Change in Visuospatial Working Memory , 2006, Journal of Cognitive Neuroscience.

[69]  C. Lange-Küttner Drawing Boundaries: From Individual to Common Region--The Development of Spatial Region Attribution in Children. , 2006 .

[70]  Vinod Menon,et al.  Where and When the Anterior Cingulate Cortex Modulates Attentional Response: Combined fMRI and ERP Evidence , 2006, Journal of Cognitive Neuroscience.

[71]  M. Chun,et al.  Dissociable neural mechanisms supporting visual short-term memory for objects , 2006, Nature.

[72]  Jin Fan,et al.  Development of attentional networks: An fMRI study with children and adults , 2005, NeuroImage.

[73]  V. Bondarko,et al.  Visual Acuity and the Crowding Effect in 8- to 17-Year-Old Schoolchildren , 2005, Human Physiology.

[74]  N. P. Bichot,et al.  A visual salience map in the primate frontal eye field. , 2005, Progress in brain research.

[75]  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 .

[76]  Susan K Lemieux,et al.  Retinotopic organization in children measured with fMRI. , 2004, Journal of vision.

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

[78]  R. Allen,et al.  Attention and expertise in multiple target tracking , 2004 .

[79]  Katsumi Aoki,et al.  Recent development of flow visualization , 2004, J. Vis..

[80]  James R. Booth,et al.  Neural development of selective attention and response inhibition , 2003, NeuroImage.

[81]  R Turner,et al.  Optimized EPI for fMRI studies of the orbitofrontal cortex , 2003, NeuroImage.

[82]  Suzanne E. Welcome,et al.  Mapping cortical change across the human life span , 2003, Nature Neuroscience.

[83]  P. Cavanagh,et al.  The Spatial Resolution of Visual Attention , 2001, Cognitive Psychology.

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

[85]  Joan Stiles,et al.  The effects of stimulus density on children’s analysis of hierarchical patterns , 2001 .

[86]  K. R. Ridderinkhof,et al.  Attention and selection in the growing child: views derived from developmental psychophysiology , 2000, Biological Psychology.

[87]  R. Turner,et al.  Characterization and Correction of Interpolation Effects in the Realignment of fMRI Time Series , 2000, NeuroImage.

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

[89]  M. Goldberg,et al.  The representation of visual salience in monkey parietal cortex , 1998, Nature.

[90]  J. Burack,et al.  A developmental study of visual attention: Issues of filtering efficiency and focus , 1997 .

[91]  R. Goodman The Strengths and Difficulties Questionnaire: a research note. , 1997, Journal of child psychology and psychiatry, and allied disciplines.

[92]  P. Cavanagh,et al.  Attentional resolution and the locus of visual awareness , 1996, Nature.

[93]  D. Levi,et al.  The two-dimensional shape of spatial interaction zones in the parafovea , 1992, Vision Research.

[94]  J. Enns,et al.  Developmental changes in selective and integrative visual attention. , 1985, Journal of experimental child psychology.

[95]  D. Navon Forest before trees: The precedence of global features in visual perception , 1977, Cognitive Psychology.

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

[97]  J. Raven,et al.  Manual for Raven's progressive matrices and vocabulary scales , 1962 .