Development of Spatial and Verbal Working Memory Capacity in the Human Brain

A core aspect of working memory (WM) is the capacity to maintain goal-relevant information in mind, but little is known about how this capacity develops in the human brain. We compared brain activation, via fMRI, between children (ages 7–12 years) and adults (ages 20–29 years) performing tests of verbal and spatial WM with varying amounts (loads) of information to be maintained in WM. Children made disproportionately more errors than adults as WM load increased. Children and adults exhibited similar hemispheric asymmetry in activation, greater on the right for spatial WM and on the left for verbal WM. Children, however, failed to exhibit the same degree of increasing activation across WM loads as was exhibited by adults in multiple frontal and parietal cortical regions. Thus, children exhibited adult-like hemispheric specialization, but appeared immature in their ability to marshal the neural resources necessary to maintain large amounts of verbal or spatial information in WM.

[1]  Susanne M. Jaeggi,et al.  Does excessive memory load attenuate activation in the prefrontal cortex? Load-dependent processing in single and dual tasks: functional magnetic resonance imaging study , 2003, NeuroImage.

[2]  H. Niki,et al.  Prefrontal cortical unit activity and delayed alternation performance in monkeys. , 1971, Journal of neurophysiology.

[3]  R. Coppola,et al.  Physiological characteristics of capacity constraints in working memory as revealed by functional MRI. , 1999, Cerebral cortex.

[4]  Lisa T. Eyler,et al.  Neural correlates of verbal learning in adolescent alcohol and marijuana users. , 2011, Addiction.

[5]  E. Zarahn,et al.  The Role of Prefrontal Cortex in Sensory Memory and Motor Preparation: An Event-Related fMRI Study , 2000, NeuroImage.

[6]  J. Jonides,et al.  Dissociating verbal and spatial working memory using PET. , 1996, Cerebral cortex.

[7]  Kristina M. Visscher,et al.  Functional Neuroanatomical Differences Between Adults and School-Age Children in the Processing of Single Words , 2002, Science.

[8]  Alan C. Evans,et al.  A General Statistical Analysis for fMRI Data , 2000, NeuroImage.

[9]  Patrick C. Kyllonen,et al.  Reasoning ability is (little more than) working-memory capacity?! , 1990 .

[10]  Douglas C. Noll,et al.  Activation of Prefrontal Cortex in Children during a Nonspatial Working Memory Task with Functional MRI , 1995, NeuroImage.

[11]  J. Fuster,et al.  Effects of cooling parietal cortex on prefrontal units in delay tasks , 1989, Brain Research.

[12]  M. Just,et al.  From the SelectedWorks of Marcel Adam Just 1992 A capacity theory of comprehension : Individual differences in working memory , 2017 .

[13]  Alison R Preston,et al.  Comparison of spiral-in/out and spiral-out BOLD fMRI at 1.5 and 3 T , 2004, NeuroImage.

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

[15]  Jonathan D. Cohen,et al.  Working Memory for Letters, Shapes, and Locations: fMRI Evidence against Stimulus-Based Regional Organization in Human Prefrontal Cortex , 2000, NeuroImage.

[16]  Laura Ann Petitto,et al.  Left Hemisphere Cerebral Specialization for Babies While Babbling , 2002, Science.

[17]  M. Mintun,et al.  Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. , 1996, Journal of neurophysiology.

[18]  M. D’Esposito,et al.  Functional MRI studies of spatial and nonspatial working memory. , 1998, Brain research. Cognitive brain research.

[19]  Christopher S. Monk,et al.  Functional neuroanatomy of spatial working memory in children. , 2000, Developmental psychology.

[20]  T. Desmet,et al.  The development of working memory: exploring the complementarity of two models. , 2000, Journal of experimental child psychology.

[21]  Richard S. J. Frackowiak,et al.  The neural correlates of the verbal component of working memory , 1993, Nature.

[22]  Leslie G. Ungerleider,et al.  Distinguishing the Functional Roles of Multiple Regions in Distributed Neural Systems for Visual Working Memory , 2000, NeuroImage.

[23]  Edward E. Smith,et al.  Spatial working memory in humans as revealed by PET , 1993, Nature.

[24]  J. Cohen,et al.  Relation of prefrontal cortex dysfunction to working memory and symptoms in schizophrenia. , 2001, The American journal of psychiatry.

[25]  N. Cowan.  The magical number 4 in short-term memory: A reconsideration of mental storage capacity , 2001, Behavioral and Brain Sciences.

[26]  E. Lenneberg.  Biological Foundations of Language , 1967 .

[27]  J. Jonides,et al.  Neuroimaging analyses of human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[28]  P. Goldman-Rakic,et al.  Functional magnetic resonance imaging of human prefrontal cortex activation during a spatial working memory task. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[29]  K. Grill-Spector,et al.  Differential development of high-level visual cortex correlates with category-specific recognition memory , 2007, Nature Neuroscience.

[30]  J. Fuster,et al.  Functional interactions between inferotemporal and prefrontal cortex in a cognitive task , 1985, Brain Research.

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

[32]  Serge A R B Rombouts,et al.  Developmental differences in prefrontal activation during working memory maintenance and manipulation for different memory loads. , 2011, Developmental science.

[33]  Catherine T. Best,et al.  Development of infant ear asymmetries for speech and music , 1982, Perception & psychophysics.

[34]  P. Goldman-Rakic,et al.  Activation of human prefrontal cortex during spatial and nonspatial working memory tasks measured by functional MRI. , 1996, Cerebral cortex.

[35]  P. Ellen Grant,et al.  Developmental neural networks in children performing a Categorical N-Back Task , 2006, NeuroImage.

[36]  John E. Desmond,et al.  Load- and practice-dependent increases in cerebro-cerebellar activation in verbal working memory: an fMRI study , 2005, NeuroImage.

[37]  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.

[38]  Leslie G. Ungerleider,et al.  The role of prefrontal cortex in working memory: examining the contents of consciousness. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[39]  Lawrence R. Frank,et al.  Functional MRI of Global and Local Processing in Children , 2002, NeuroImage.

[40]  K. R. Ridderinkhof,et al.  The developing brain: From theory to neuroimaging and back , 2011, Developmental Cognitive Neuroscience.

[41]  G. Glover,et al.  Spiral‐in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts , 2001, Magnetic resonance in medicine.

[42]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[43]  Gary H. Glover,et al.  Default-mode function and task-induced deactivation have overlapping brain substrates in children , 2008, NeuroImage.

[44]  G. Hitch,et al.  What limits children's working memory span? Theoretical accounts and applications for scholastic development. , 2001, Journal of experimental psychology. General.

[45]  P. Carpenter,et al.  Individual differences in working memory and reading , 1980 .

[46]  Yaakov Stern,et al.  Positive evidence against human hippocampal involvement in working memory maintenance of familiar stimuli. , 2004, Cerebral cortex.

[47]  M. Paule,et al.  Developmental aspects of delayed matching-to-sample task performance in children. , 2000, Neurotoxicology and teratology.

[48]  Boreom Lee,et al.  White matter neuroplastic changes in long-term trained players of the game of “Baduk” (GO): A voxel-based diffusion-tensor imaging study , 2010, NeuroImage.

[49]  J. Fuster,et al.  Delayed-matching and delayed-response deficit from cooling dorsolateral prefrontal cortex in monkeys. , 1976, Journal of comparative and physiological psychology.

[50]  Edward E. Smith,et al.  Dissociation of Storage and Rehearsal in Verbal Working Memory: Evidence From Positron Emission Tomography , 1996 .

[51]  B. Ambridge,et al.  The structure of working memory from 4 to 15 years of age. , 2004, Developmental psychology.

[52]  Gary H. Glover,et al.  Breath holding reveals differences in fMRI BOLD signal in children and adults , 2005, NeuroImage.

[53]  J. Desmond,et al.  Load-Dependent Roles of Frontal Brain Regions in the Maintenance of Working Memory , 1999, NeuroImage.

[54]  G. Glover,et al.  Regularized higher‐order in vivo shimming , 2002, Magnetic resonance in medicine.

[55]  S Hale,et al.  Verbal and spatial working memory in school-age children: developmental differences in susceptibility to interference. , 1997, Developmental psychology.

[56]  R. Coppola,et al.  Specific versus Nonspecific Brain Activity in a Parametric N-Back Task , 2000, NeuroImage.

[57]  John D E Gabrieli,et al.  The role of the prefrontal cortex in the maintenance of verbal working memory: an event-related FMRI analysis. , 2005, Neuropsychology.

[58]  Douglas C. Noll,et al.  A Developmental Functional MRI Study of Spatial Working Memory , 1999, NeuroImage.

[59]  M. D’Esposito.  Working memory. , 2008, Handbook of clinical neurology.

[60]  L. Petitto,et al.  Biological Foundations of Language , 1967, Neurology.

[61]  David F. Bjorklund,et al.  How age changes in knowledge base contribute to the development of children's memory: An interpretive review , 1987 .

[62]  Monica Luciana,et al.  Working Memory Performance in Typically Developing Children and Adolescents: Behavioral Evidence of Protracted Frontal Lobe Development , 2007, Developmental neuropsychology.

[63]  N. Ramsey,et al.  Working memory capacity in schizophrenia: a parametric fMRI study , 2004, Schizophrenia Research.

[64]  Shigeru Watanabe,et al.  Longitudinal study of spatial working memory development in young children , 2009, Neuroreport.

[65]  M. Manosevitz.  High-Speed Scanning in Human Memory , .

[66]  Edward E. Smith,et al.  A Parametric Study of Prefrontal Cortex Involvement in Human Working Memory , 1996, NeuroImage.

[67]  Susan F Tapert,et al.  Neuropsychological Predictors of BOLD Response During a Spatial Working Memory Task in Adolescents: What Can Performance Tell Us About fMRI Response Patterns? , 2005, Journal of clinical and experimental neuropsychology.

[68]  Alexandra J. Golby,et al.  Functional MRI of memory in the hippocampus: Laterality indices may be more meaningful if calculated from whole voxel distributions , 2006, NeuroImage.

[69]  V. Menon,et al.  Neural basis of protracted developmental changes in visuo-spatial working memory , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[70]  Leslie G. Ungerleider,et al.  Neural Correlates of Visual Working Memory fMRI Amplitude Predicts Task Performance , 2002, Neuron.

[71]  R. B. Freeman,et al.  The ontogeny of brain lateralization for speech and nonspeech stimuli , 1975, Brain and Language.

[72]  G. E. Alexander,et al.  Neuron Activity Related to Short-Term Memory , 1971, Science.

[73]  Randall W Engle,et al.  Working memory, short-term memory, and general fluid intelligence: a latent-variable approach. , 1999, Journal of experimental psychology. General.

[74]  Edward E. Smith,et al.  Age Differences in the Frontal Lateralization of Verbal and Spatial Working Memory Revealed by PET , 2000, Journal of Cognitive Neuroscience.

[75]  Hans Forssberg,et al.  Increased Brain Activity in Frontal and Parietal Cortex Underlies the Development of Visuospatial Working Memory Capacity during Childhood , 2002, Journal of Cognitive Neuroscience.

[76]  B. Postle,et al.  Functional neuroanatomical double dissociation of mnemonic and executive control processes contributing to working memory performance. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[77]  M. D’Esposito,et al.  The Influence of Working-Memory Demand and Subject Performance on Prefrontal Cortical Activity , 2002, Journal of Cognitive Neuroscience.

[78]  D. Manoach,et al.  Prefrontal cortex fMRI signal changes are correlated with working memory load , 1997, Neuroreport.

[79]  B Macwhinney,et al.  The PsyScope experiment-building system. , 1997, Spatial vision.

[80]  Edward E. Smith,et al.  The Role of Parietal Cortex in Verbal Working Memory , 1998, The Journal of Neuroscience.

[81]  P. Goldman-Rakic,et al.  Sustained Mnemonic Response in the Human Middle Frontal Gyrus during On-Line Storage of Spatial Memoranda , 2002, Journal of Cognitive Neuroscience.

[82]  Susan F Tapert,et al.  fMRI reveals alteration of spatial working memory networks across adolescence , 2005, Journal of the International Neuropsychological Society.

[83]  Raymond J Dolan,et al.  Maintenance versus manipulation in verbal working memory revisited: an fMRI study , 2003, NeuroImage.

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

[85]  J. Joseph,et al.  Prefrontal cortex and spatial sequencing in macaque monkey , 2004, Experimental Brain Research.