Neural basis of protracted developmental changes in visuo-spatial working memory
Open accessAbstract
Developmental studies have shown that visuo-spatial working memory (VSWM) performance improves throughout childhood and adolescence into young adulthood. The neural basis of this protracted development is poorly understood. In this study, we used functional MRI (fMRI) to examine VSWM function in children, adolescents, and young adults, ages 7-22. Subjects performed a 2-back VSWM experiment that required dynamic storage and manipulation of spatial information. Accuracy and response latency on the VSWM task improved gradually, extending into young adulthood. Age-related increases in brain activation were observed in focal regions of the left and right dorsolateral prefrontal cortex, left ventrolateral prefrontal cortex (including Broca's area), left premotor cortex, and left and right posterior parietal cortex. Multiple regression analysis was used to examine the relative contributions of age, accuracy, and response latency on activation. Our analysis showed that age was the most significant predictor of activation in these brain regions. These findings provide strong evidence for a process of protracted functional maturation of bilateral fronto-parietal neural networks involved in VSWM development. At least two neural systems involved in VSWM mature together: (i) a right hemisphere visuo-spatial attentional system, and (ii) a left hemisphere phonological storage and rehearsal system. These observations suggest that visually and verbally mediated mnemonic processes, and their neural representations, develop concurrently during childhood and adolescence and into young adulthood.
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Age-related changes were found in several brain regions including the dorsolateral prefrontal cortex and the posterior parietal cortex bilaterally.
“Age-related changes were found in several brain regions including the dorsolateral prefrontal cortex and the posterior parietal cortex bilaterally (see Figure 6).”
From Development of the adolescent brain: implications for executive function and social cognition (2006) · cites this paper as Kwon, Reiss, and Menon, 2002
Activation in left and right prefrontal cortex and posterior parietal cortex increases during a working memory task.
“Increasing activation in left and right prefrontal cortex and posterior parietal cortex during working memory task”
From Development of the adolescent brain: implications for executive function and social cognition (2006) · cites this paper as Kwon et al., 2002
Cites
The episodic buffer: a new component of working memory?
Baddeley, A. (2000) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(00)01538-2 · Cited by 7,359 · see citing works
A developmental functional MRI study of prefrontal activation during performance of a go-no-go task
Casey, B. J., Trainor, R. J., Orendi, J. L., Schubert, A. B., Nystrom, L. E., Giedd, J. N., Castellanos, F. X., Haxby, J. V., Noll, D. C., Cohen, J. D., et al. (1997) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1997.9.6.835 · Cited by 1,106 · see citing works
Age differences in the frontal lateralization of verbal and spatial working memory revealed by PET
Reuter-Lorenz, P. A., Jonides, J., Smith, E. E., Hartley, A., Miller, A., Marshuetz, C., & Koeppe, R. A. (2000) · Journal of Cognitive Neuroscience · doi:10.1162/089892900561814 · Cited by 998 · see citing works
Processing speed as a mental capacity
Kail, R., & Salthouse, T. A. (1994) · Acta Psychologica · doi:10.1016/0001-6918(94)90003-5 · Cited by 850 · see citing works
Klingberg, T., Forssberg, H., & Westerberg, H. (2002) · Journal of Cognitive Neuroscience · doi:10.1162/089892902317205276 · Cited by 695 · see citing works
A Developmental fMRI Study of the Stroop Color-Word Task
Adleman, N. E., Menon, V., Blasey, C. M., White, C. D., Warsofsky, I. S., Glover, G. H., & Reiss, A. L. (2002) · NeuroImage · doi:10.1006/nimg.2001.1046 · Cited by 569 · see citing works
Self-citationThe development of visuo-spatial working memory
Pickering, S. J. (2001) · Memory · doi:10.1080/09658210143000182 · Cited by 214 · see citing works
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Functional connectivity in the resting brain: a network analysis of the default mode hypothesis
Greicius, M. D., Krasnow, B., Reiss, A. L., & Menon, V. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0135058100 · Cited by 6,358 · see citing works
Self-citationWhy do many psychiatric disorders emerge during adolescence?
Paus, T., Keshavan, M., & Giedd, J. N. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2513 · Cited by 3,123 · see citing works
A Developmental Perspective on Executive Function
Best, J. R., & Miller, P. H. (2010) · Child Development · doi:10.1111/j.1467-8624.2010.01499.x · Cited by 2,692 · see citing works
Understanding adolescence as a period of social–affective engagement and goal flexibility
Crone, E. A., & Dahl, R. E. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3313 · Cited by 2,507 · see citing works
Development of the adolescent brain: implications for executive function and social cognition
Blakemore, S., & Choudhury, S. (2006) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2006.01611.x · Cited by 2,328 · see citing works
Age-related change in executive function: Developmental trends and a latent variable analysis
Huizinga, M., Dolan, C. V., & van der Molen, M. W. (2006) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2006.01.010 · Cited by 1,636 · see citing works
Training and plasticity of working memory
Klingberg, T. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.05.002 · Cited by 1,585 · see citing works
Normal development of brain circuits
Tau, G. Z., & Peterson, B. S. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.115 · Cited by 1,391 · see citing works
Mapping brain maturation and cognitive development during adolescence
Paus, T. (2005) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.12.008 · Cited by 1,348 · see citing works
Adolescent suicide and suicidal behavior
Bridge, J. A., Goldstein, T. R., & Brent, D. A. (2006) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2006.01615.x · Cited by 1,361 · see citing works
Increased prefrontal and parietal activity after training of working memory
Olesen, P. J., Westerberg, H., & Klingberg, T. (2004) · Nature Neuroscience · doi:10.1038/nn1165 · Cited by 1,317 · see citing works
MARTINUSSEN, R., HAYDEN, J., HOGG-JOHNSON, S., & TANNOCK, R. (2005) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/01.chi.0000153228.72591.73 · Cited by 1,297 · see citing works
20 years of the default mode network: A review and synthesis.
Menon, V. (2023) · Neuron · doi:10.1016/j.neuron.2023.04.023 · Cited by 934 · see citing works
“9,10 It was striking that brain areas that showed increased responses with cognitive load differed depending on the task and cognitive domain, but areas with suppressed brain response remained consistent.”
BackgroundSelf-citationBarnea-Goraly, N., Menon, V., Eckert, M., Tamm, L., Bammer, R., Karchemskiy, A., Dant, C. C., & Reiss, A. L. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi062 · Cited by 848 · see citing works
Self-citationKlingberg, T., Forssberg, H., & Westerberg, H. (2002) · Journal of Cognitive Neuroscience · doi:10.1162/089892902317205276 · Cited by 695 · see citing works
Rubia, K., Smith, A. B., Woolley, J., Nosarti, C., Heyman, I., Taylor, E., & Brammer, M. (2006) · Human Brain Mapping · doi:10.1002/hbm.20237 · Cited by 632 · see citing works
A Developmental Perspective on Alcohol and Youths 16 to 20 Years of Age
Brown, S. A., McGue, M., Maggs, J., Schulenberg, J., Hingson, R., Swartzwelder, S., Martin, C., Chung, T., Tapert, S. F., Sher, K., et al. (2008) · Pediatrics · doi:10.1542/peds.2007-2243d · Cited by 612 · see citing works
Figner, B., Mackinlay, R. J., Wilkening, F., & Weber, E. U. (2009) · Journal of Experimental Psychology: Learning, Memory, and Cognition · doi:10.1037/a0014983 · Cited by 625 · see citing works
The development of nonverbal working memory and executive control processes in adolescents
Luciana, M., Conklin, H. M., Hooper, C. J., & Yarger, R. S. (2005) · Child Development · doi:10.1111/j.1467-8624.2005.00872.x · Cited by 567 · see citing works
White matter development in adolescence: A DTI study
Asato, M. R., Terwilliger, R., Woo, J., & Luna, B. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp282 · Cited by 512 · see citing works
Hooper, C. J., Luciana, M., Conklin, H. M., & Yarger, R. S. (2004) · Developmental Psychology · doi:10.1037/0012-1649.40.6.1148 · Cited by 412 · see citing works
Olesen, P. J., Nagy, Z., Westerberg, H., & Klingberg, T. (2003) · Cognitive Brain Research · doi:10.1016/j.cogbrainres.2003.09.003 · Cited by 397 · see citing works
Neurodevelopmental changes in working memory and cognitive control
Bunge, S. A., & Wright, S. B. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.02.005 · Cited by 381 · see citing works
Uddin, L. Q. (2010) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2010.00021 · Cited by 343 · see citing works
The Prefrontal Cortex: Functional Neural Development During Early Childhood
Tsujimoto, S. (2008) · The Neuroscientist · doi:10.1177/1073858408316002 · Cited by 291 · see citing works
Adolescent development of the neural circuitry for thinking about intentions
Blakemore, S.-J., den Ouden, H., Choudhury, S., & Frith, C. (2007) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsm009 · Cited by 250 · see citing works
Diffusion tensor imaging for understanding brain development in early life
Qiu, A., Mori, S., & Miller, M. I. (2015) · Annual Review of Psychology · doi:10.1146/annurev-psych-010814-015340 · Cited by 238 · see citing works
Rethinking schizophrenia in the context of normal neurodevelopment
Catts, V. S., Fung, S. J., Long, L. E., Joshi, D., Vercammen, A., Allen, K. M., Fillman, S. G., Rothmond, D. A., Sinclair, D., Tiwari, Y., et al. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00060 · Cited by 206 · see citing works
The self-regulating brain: cortical-subcortical feedback and the development of intelligent action.
Lewis, M. D., & Todd, R. M. (2007) · Cognitive Development · doi:10.1016/j.cogdev.2007.08.004 · Cited by 194 · see citing works
Functional brain connectivity at rest changes after working memory training
Jolles, D. D., van Buchem, M. A., Crone, E. A., & Rombouts, S. A. R. B. (2013) · Human Brain Mapping · doi:10.1002/hbm.21444 · Cited by 183 · see citing works
Chaddock-Heyman, L., Hillman, C. H., Cohen, N. J., & Kramer, A. F. (2014) · Monographs of the Society for Research in Child Development · doi:10.1111/mono.12129 · Cited by 152 · see citing works
Effects of age and sex on developmental neural networks of visual–spatial attention allocation
Rubia, K., Hyde, Z., Halari, R., Giampietro, V., & Smith, A. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.02.058 · Cited by 148 · see citing works
The change of the brain activation patterns as children learn algebra equation solving
Qin, Y., Carter, C. S., Silk, E. M., Stenger, V. A., Fissell, K., Goode, A., & Anderson, J. R. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401227101 · Cited by 142 · see citing works
The physiology of developmental changes in BOLD functional imaging signals
Harris, J. J., Reynell, C., & Attwell, D. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.04.001 · Cited by 142 · see citing works
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Blackford, J. U., & Pine, D. S. (2012) · Child and Adolescent Psychiatric Clinics of North America · doi:10.1016/j.chc.2012.05.002 · Cited by 138 · see citing works
Development of Working Memory Maintenance
Geier, C. F., Garver, K., Terwilliger, R., & Luna, B. (2009) · Journal of Neurophysiology · doi:10.1152/jn.90562.2008 · Cited by 136 · see citing works
The developing brain: from theory to neuroimaging and back
Crone, E. A., & Richard Ridderinkhof, K. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2010.12.001 · Cited by 125 · see citing works
Associations between white matter microstructure and infants' working memory
Short, S. J., Elison, J. T., Goldman, B. D., Styner, M., Gu, H., Connelly, M., Maltbie, E., Woolson, S., Lin, W., Gerig, G., et al. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2012.09.021 · Cited by 105 · see citing works
Smoking impacts on prefrontal attentional network function in young adult brains
Musso, F., Bettermann, F., Vucurevic, G., Stoeter, P., Konrad, A., & Winterer, G. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0499-8 · Cited by 93 · see citing works
Anxiety, Methylphenidate Response, and Working Memory in Children With ADHD
Bedard, A.-C., & Tannock, R. (2008) · Journal of Attention Disorders · doi:10.1177/1087054707311213 · Cited by 76 · see citing works
Developmental shifts in fMRI activations during visuospatial relational reasoning
Eslinger, P. J., Blair, C., Wang, J., Lipovsky, B., Realmuto, J., Baker, D., Thorne, S., Gamson, D., Zimmerman, E., Rohrer, L., et al. (2009) · Brain and Cognition · doi:10.1016/j.bandc.2008.04.010 · Cited by 75 · see citing works
Holmes, J., Gathercole, S. E., & Dunning, D. L. (2010) · Advances in Child Development and Behavior · doi:10.1016/b978-0-12-374748-8.00001-9 · Cited by 66 · see citing works
Linking<scp>GABA</scp>and glutamate levels to cognitive skill acquisition during development
Cohen Kadosh, K., Krause, B., King, A. J., Near, J., & Cohen Kadosh, R. (2015) · Human Brain Mapping · doi:10.1002/hbm.22921 · Cited by 64 · see citing works
Tobacco use across the formative years: a road map to developmental vulnerabilities
Jamner, L., Whalen, C., Loughlin, S., Mermelstein, R., Audrain-McGovern, J., Krishnan-Sarin, S., Worden, J., & Leslie, F. (2003) · Nicotine & Tobacco Research · doi:10.1080/14622200310001625573 · Cited by 60 · see citing works
Faridi, N., Karama, S., Burgaleta, M., White, M. T., Evans, A. C., Fonov, V., Collins, D. L., & Waber, D. P. (2015) · Neuropsychology · doi:10.1037/neu0000079 · Cited by 42 · see citing works
van Ewijk, H., Weeda, W. D., Heslenfeld, D. J., Luman, M., Hartman, C. A., Hoekstra, P. J., Faraone, S. V., Franke, B., Buitelaar, J. K., & Oosterlaan, J. (2015) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2015.07.003 · Cited by 39 · see citing works
Spann, M. N., Bansal, R., Rosen, T. S., & Peterson, B. S. (2014) · Human Brain Mapping · doi:10.1002/hbm.22487 · Cited by 29 · see citing works
Zhou, X., Zhu, D., King, S. G., Lees, C. J., Bennett, A. J., Salinas, E., Stanford, T. R., & Constantinidis, C. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1518147113 · Cited by 23 · see citing works
Skalaban, L. J., Cohen, A. O., Conley, M. I., Lin, Q., Schwartz, G. N., Ruiz-Huidobro, N. A. M., Cannonier, T., Martinez, S. A., & Casey, B. J. (2022) · Learning & Memory · doi:10.1101/lm.053539.121 · Cited by 14 · see citing works
McKenna, R., Rushe, T., & Woodcock, K. A. (2017) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00154 · Cited by 13 · see citing works
- Authors
- Kwon, H., Reiss, A. L., & Menon, V.
- Affiliations
- Stanford Medicine (US)
- Corresponding author
- Menon, V.
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2002-09-20
- Volume
- 99
- Issue
- 20
- Pages
- 13336-13341
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC130634
- OpenAlex
- W2061198654
- Cited by
- 441
- References
- 7
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 21 · 2023: 12 · 2022: 10 · 2021: 21 · 2020: 18 · 2019: 15 · 2018: 24 · 2017: 23 · 2016: 19 · 2015: 30 · 2014: 24 · 2013: 26 · 2012: 21
- FWCI
- 19.21
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (MH62430, MH01142, MH50547, K02MH001142, R01MH050047, R03MH062430)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (K25HD040761, HD40761, R01HD031715, HD31715)
- Topics
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Abilities and Testing
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Social Sciences › Psychology › Neuropsychology and Physiological Psychology › Developmental and Educational Neuropsychology
- Keywords
- visuospatial working memory, cognitive development, brain maturation, dorsolateral prefrontal cortex, ventrolateral prefrontal cortex, Broca's area, premotor cortex, posterior parietal cortex, frontoparietal network, visuospatial attention, children and adolescents
- MeSH terms
- Adolescent, Adult, Age Factors, Brain, Brain Mapping, Child, Humans, Magnetic Resonance Imaging, Memory, Models, Neurological, Regression Analysis, Spatial Behavior, Verbal Behavior
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