Evidence for intact memory-guided attention in school-aged children.

Visual scenes contain many statistical regularities such as the likely identity and location of objects that are present; with experience, such regularities can be encoded and can ultimately facilitate the deployment of spatial attention to important locations. Memory-guided attention has been extensively examined in adults with the 'contextual cueing' paradigm and has been linked to specific neural substrates - a medial temporal lobe (MTL)-frontoparietal network. However, it currently remains unknown when this ability comes 'online' during development. Thus, we examined the performance of school-aged children on an age-appropriate version of the contextual cueing paradigm. Children searched for a target fish among distractor fish in new displays and in 'old' displays on a touchscreen computer. Old displays repeated across blocks of trials and thus provided an opportunity for prior experience with the invariant configuration of the stimuli to guide attentional deployment. We found that over time children searched old displays significantly faster than new displays, thus revealing intact memory-guided attention and presumed function of an MTL-frontoparietal network in 5- to 9-year-olds. More generally, our findings suggest that children are remarkably sensitive to the inherent structure of their visual environment and this enables attentional deployment to become more efficient with experience.

[1]  D. Maurer,et al.  Developmental changes in attention: the effects of endogenous cueing and of distractors , 2001 .

[2]  P. Huttenlocher.  Morphometric study of human cerebral cortex development , 1990, Neuropsychologia.

[3]  A. Diamond,et al.  Rate of Maturation of the Hippocampus and the Developmental Progression of Children's Performance on the Delayed Non‐Matching to Sample and Visual Paired Comparison Tasks a , 1990, Annals of the New York Academy of Sciences.

[4]  M. Chun,et al.  Temporal contextual cuing of visual attention. , 2001, Journal of experimental psychology. Learning, memory, and cognition.

[5]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[6]  C. Rovee-Collier,et al.  The development of visual search in infants and very young children. , 2002, Journal of experimental child psychology.

[7]  J. Enns,et al.  LIFESPAN CHANGES IN ATTENTION: THE VISUAL SEARCH TASK , 1998 .

[8]  M. Chun,et al.  Top-Down Attentional Guidance Based on Implicit Learning of Visual Covariation , 1999 .

[9]  Jon Driver,et al.  Visual search in typically developing toddlers and toddlers with Fragile X or Williams syndrome. , 2004, Developmental science.

[10]  A. Lleras,et al.  Spatial context and top-down strategies in visual search. , 2004, Spatial vision.

[11]  Laurent Itti,et al.  The role of memory in guiding attention during natural vision. , 2006, Journal of vision.

[12]  M. Mishkin,et al.  Human memory development and its dysfunction after early hippocampal injury , 2006, Trends in Neurosciences.

[13]  M. Chun,et al.  Implicit, long-term spatial contextual memory. , 2003, Journal of experimental psychology. Learning, memory, and cognition.

[14]  Set size, novelty, and visual pop-out in infancy. , 1996, Journal of experimental psychology. Human perception and performance.

[15]  A. Treisman,et al.  A feature-integration theory of attention , 1980, Cognitive Psychology.

[16]  J W Rudy,et al.  The effect of age on children's learning of problems that require a configural association solution. , 1993, Developmental psychobiology.

[17]  Charles A. Nelson,et al.  The Ontogeny of Human Memory: A Cognitive Neuroscience Perspective. , 1995 .

[18]  Keith A. Schneider,et al.  Interhemispheric suppression: The case of the missing vertical meridian , 2010 .

[19]  M. Corbetta,et al.  Quantitative analysis of attention and detection signals during visual search. , 2003, Journal of neurophysiology.

[20]  M. Chun,et al.  Contextual Cueing: Implicit Learning and Memory of Visual Context Guides Spatial Attention , 1998, Cognitive Psychology.

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

[22]  N. Fox,et al.  Variations of the flanker paradigm: Assessing selective attention in young children , 2007, Behavior research methods.

[23]  Mark H. Johnson,et al.  Functional brain development in infants: elements of an interactive specialization framework. , 2000, Child development.

[24]  J. Rapoport,et al.  Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: Ages 4–18 years , 1995, The Journal of comparative neurology.

[25]  J. Gabrieli,et al.  Immature Frontal Lobe Contributions to Cognitive Control in Children Evidence from fMRI , 2002, Neuron.

[26]  Sarah Durston,et al.  A shift from diffuse to focal cortical activity with development. , 2006, Developmental science.

[27]  Richard N Aslin,et al.  Statistical learning of new visual feature combinations by infants , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[28]  H. Eichenbaum,et al.  On the Binding of Associations in Memory: Clues From Studies on the Role of the Hippocampal Region in Paired-Associate Learning , 1995 .

[29]  M. Bar.  Visual objects in context , 2004, Nature Reviews Neuroscience.

[30]  Yuhong Jiang,et al.  Intertrial temporal contextual cuing: association across successive visual search trials guides spatial attention. , 2005, Journal of experimental psychology. Human perception and performance.

[31]  J. H. Howard,et al.  Developmental differences in implicit learning of spatial context. , 2007, Neuropsychology.

[32]  D. Schnyer,et al.  A critical role for the anterior hippocampus in relational memory: Evidence from an fMRI study comparing associative and item recognition , 2004, Hippocampus.

[33]  M. Goldberg,et al.  Neuronal Activity in the Lateral Intraparietal Area and Spatial Attention , 2003, Science.

[34]  K. Kunz,et al.  Dissociating Striatal and Hippocampal Function Developmentally with a Stimulus–Response Compatibility Task , 2002, The Journal of Neuroscience.

[35]  N. P. Bichot,et al.  Dissociation of visual discrimination from saccade programming in macaque frontal eye field. , 1997, Journal of neurophysiology.

[36]  A. Meltzoff.  Infant Imitation After a 1-Week Delay: Long-Term Memory for Novel Acts and Multiple Stimuli. , 1988, Developmental psychology.

[37]  L. Squire,et al.  Perceptual learning, awareness, and the hippocampus , 2001, Hippocampus.

[38]  M. Chun,et al.  Memory deficits for implicit contextual information in amnesic subjects with hippocampal damage , 1999, Nature Neuroscience.

[39]  C. Büchel,et al.  The Role of Medial Temporal Lobe Structures in Implicit Learning An Event-Related fMRI Study , 2002, Neuron.

[40]  Christian Büchel,et al.  The role of medial temporal lobe structures in implicit learning: an event-related fMRI study , 2003 .

[41]  M. Masson,et al.  Using confidence intervals in within-subject designs , 1994, Psychonomic bulletin & review.

[42]  Scott P. Johnson,et al.  Visual statistical learning in infancy: evidence for a domain general learning mechanism , 2002, Cognition.

[43]  S. Yantis,et al.  Cortical mechanisms of space-based and object-based attentional control , 2003, Current Opinion in Neurobiology.

[44]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[45]  M. Goldsmith,et al.  Statistical Learning by 8-Month-Old Infants , 1996 .

[46]  William L. Gross,et al.  Hippocampal differentiation without recognition: an fMRI analysis of the contextual cueing task. , 2007, Learning & memory.

[47]  Harlene Hayne,et al.  Deferred imitation by 6- and 9-month-old infants: more evidence for declarative memory. , 1999 .

[48]  A. Toga,et al.  In vivo evidence for post-adolescent brain maturation in frontal and striatal regions , 1999, Nature Neuroscience.

[49]  Carter Wendelken,et al.  Neurocognitive development of the ability to manipulate information in working memory. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Peter M. Vishton,et al.  Rule learning by seven-month-old infants. , 1999, Science.

[51]  A. Diamond.  Normal development of prefrontal cortex from birth to young adulthood: Cognitive functions, anatomy, and biochemistry. , 2002 .

[52]  Timothy F. Brady,et al.  Spatial constraints on learning in visual search: modeling contextual cuing. , 2007, Journal of experimental psychology. Human perception and performance.

[53]  A. Nobre,et al.  Orienting Attention Based on Long-Term Memory Experience , 2006, Neuron.

[54]  J. Bachevalier,et al.  Revisiting the maturation of medial temporal lobe memory functions in primates. , 2000, Learning & memory.

[55]  John D E Gabrieli,et al.  Development of the declarative memory system in the human brain , 2007, Nature Neuroscience.

[56]  Gail S. Goodman,et al.  Neurodevelopmental Correlates of True and False Recognition , 2008, Cerebral cortex.

[57]  W. Overman,et al.  Ontogeny of place learning in children as measured in the radial arm maze, Morris search task, and open field task. , 1996, Behavioral neuroscience.

[58]  C. D. Frith,et al.  Brain Activations during Visual Search: Contributions of Search Efficiency versus Feature Binding , 2003, NeuroImage.

[59]  N. Fox,et al.  The relations between frontal brain electrical activity and cognitive development during infancy. , 1992, Child development.

[60]  H. Eichenbaum.  Hippocampus Cognitive Processes and Neural Representations that Underlie Declarative Memory , 2004, Neuron.

[61]  J. Gabrieli,et al.  Dissociation between explicit memory and configural memory in the human medial temporal lobe. , 2008, Cerebral cortex.

[62]  F. Passetti,et al.  Enhanced discrimination in autism , 2001, Proceedings of the 9th International Conference on Neural Information Processing, 2002. ICONIP '02..

[63]  J. Mazziotta,et al.  Positron emission tomography study of human brain functional development , 1987, Annals of neurology.

[64]  M. Chun,et al.  Contextual cueing of visual attention , 2022 .

[65]  J. Townsend,et al.  The development of attentional orienting during the school-age years , 2003 .