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fMRI reveals alteration of spatial working memory networks across adolescence

Published online by Cambridge University Press:  26 August 2005

ALECIA D. SCHWEINSBURG
Affiliation:
Department of Psychology, University of California, San Diego, La Jolla, California
BONNIE J. NAGEL
Affiliation:
Department of Psychiatry, University of California, San Diego, La Jolla, California Veterans Medical Research Foundation, San Diego, California
SUSAN F. TAPERT
Affiliation:
Department of Psychiatry, University of California, San Diego, La Jolla, California VA San Diego Healthcare System, San Diego, California Veterans Medical Research Foundation, San Diego, California

Abstract

Recent studies have described neuromaturation and cognitive development across the lifespan, yet few neuroimaging studies have investigated task-related alterations in brain activity during adolescence. We used functional magnetic resonance imaging (fMRI) to examine brain response to a spatial working memory (SWM) task in 49 typically developing adolescents (25 females and 24 males; ages 12–17). No gender or age differences were found for task performance during SWM. However, age was positively associated with SWM brain response in left prefrontal and bilateral inferior posterior parietal regions. Age was negatively associated with SWM activation in bilateral superior parietal cortex. Gender was significantly associated with SWM response; females demonstrated diminished anterior cingulate activation and males demonstrated greater response in frontopolar cortex than females. Our findings indicate that the frontal and parietal neural networks involved in spatial working memory change over the adolescent age range and are further influenced by gender. These changes may represent evolving mnemonic strategies subserved by ongoing adolescent brain development. (JINS, 2005, 11, 631–644.)

Type
Research Article
Copyright
© 2005 The International Neuropsychological Society

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References

REFERENCES

American Psychiatric Association. (1994). DSM-IV: Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC: American Psychiatric Association.
Baddeley, A. (1992). Working memory. Science, 255, 556559.Google Scholar
Baddeley, A.D. (1986). Working memory. Oxford: Oxford University Press.
Bandettini, P.A., Jesmanowicz, A., Wong, E.C., & Hyde, J.S. (1993). Processing strategies for time-course data sets in functional MRI of the human brain. Magnetic Resonance in Medicine, 30, 161173.Google Scholar
Barnfield, A.M. (1999). Development of sex differences in spatial memory. Perceptual and Motor Skills, 89, 339350.CrossRefGoogle Scholar
Baron, R.M. & Kenny, D.A. (1986). The moderator-mediator variable distinction in social psychological research: Conceptual, strategic, and statistical considerations. Journal of Personality and Social Psychology, 51, 11731182.Google Scholar
Braver, T.S. & Bongiolatti, S.R. (2002). The role of frontopolar cortex in subgoal processing during working memory. Neuroimage, 15, 523536.Google Scholar
Brooks-Gunn, J., Warren, M.P., Rosso, J., & Gargiulo, J. (1987). Validity of self-report measures of girls' pubertal status. Child Development, 58, 829841.Google Scholar
Cabeza, R. & Nyberg, L. (2000). Imaging cognition II: An empirical review of 275 PET and fMRI studies. Journal of Cognitive Neuroscience, 12, 147.Google Scholar
Caldwell, L.C., Schweinsburg, A.D., Nagel, B.J., Barlett, V.C., Brown, S.A., & Tapert, S.F. (2005). Gender and adolescent alcohol use disorders on BOLD (blood oxygen level dependent) response to spatial working memory. Alcohol and Alcoholism, 40, 194200.Google Scholar
Casey, B.J., Cohen, J.D., Jezzard, P., Turner, R., Noll, D.C., Trainor, R.J., Giedd, J., Kaysen, D., Hertz-Pannier, L., & Rapoport, J.L. (1995). Activation of prefrontal cortex in children during a nonspatial working memory task with functional MRI. Neuroimage, 2, 221229.Google Scholar
Christoff, K. & Gabrieli, J.D. (2000). The frontopolar cortex and human cognition: Evidence for a rostrocaudal hierarchical organization within the human prefrontal cortex. Psychobiology, 28, 168186.Google Scholar
Christoff, K., Ream, J.M., Geddes, L.P., & Gabrieli, J.D. (2003). Evaluating self-generated information: Anterior prefrontal contributions to human cognition. Behavioral Neuroscience, 117, 11611168.Google Scholar
Cox, R.W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research 29, 162173.Google Scholar
Diamond, M.C. (1991). Hormonal effects on the development of cerebral lateralization. Psychoneuroendocrinology, 16, 121129.Google Scholar
Duff, S.J. & Hampson, E. (2001). A sex difference on a novel spatial working memory task in humans. Brain and Cognition, 47, 470493.CrossRefGoogle Scholar
Durston, S., Hulshoff Pol, H.E., Casey, B.J., Giedd, J.N., Buitelaar, J.K., & van Engeland, H. (2001). Anatomical MRI of the developing human brain: What have we learned? Journal of the American Academy of Child and Adolescent Psychiatry, 40, 10121020.Google Scholar
Forman, S.D., Cohen, J.D., Fitzgerald, M., Eddy, W.F., Mintun, M.A., & Noll, D.C. (1995). Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): Use of a cluster-size threshold. Magnetic Resonance in Medicine, 33 636647.Google Scholar
Gathercole, S.E. (1999). Cognitive approaches to the development of short-term memory. Trends in Cognitive Sciences, 3, 410419.Google Scholar
Gathercole, S.E., Pickering, S.J., Ambridge, B., & Wearing, H. (2004). The structure of working memory from 4 to 15 years of age. Developmental Psychology, 40, 177190.Google Scholar
Giedd, J.N. (2004). Structural magnetic resonance imaging of the adolescent brain. Annals of the New York Academy of Sciences, 1021, 7785.CrossRefGoogle Scholar
Giedd, J.N., Blumenthal, J., Jeffries, N.O., Castellanos, F.X., Liu, H., Zijdenbos, A., Giedd, J.N., Blumenthal, J., Jeffries, N.O., Castellanos, F.X., Liu, H., Zijdenbos, A., Paus, T., Evans, A.C., & Rapoport, J.L. (1999). Brain development during childhood and adolescence: A longitudinal MRI study. Nature Neuroscience, 2, 861863.Google Scholar
Gogtay, N., Giedd, J.N., Lusk, L., Hayashi, K.M., Greenstein, D., Vaituzis, A.C., Nugent, T.F. 3rd, Herman, D.H., Clasen, L.S., Toga, A.W., Rapoport, J.L., & Thompson, P.M. (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences, U.S.A., 21, 81748179.Google Scholar
Huttenlocher, P.R. (1990). Morphometric study of human cerebral cortex development. Neuropsychologia, 28, 517527.CrossRefGoogle Scholar
Jordan, K., Wustenberg, T., Heinze, H.J., Peters, M., & Jancke, L. (2002). Women and men exhibit different cortical activation patterns during mental rotation tasks. Neuropsychologia, 40, 23972408.Google Scholar
Judd, C.M. & Kenny, D.A. (1981). Process analysis: Estimating mediation in evaluation research. Evaluation Review, 5, 602619.CrossRefGoogle Scholar
Kindermann, S.S., Brown, G.G., Zorrilla, L.E., Olsen, R.K., & Jeste, D.V. (2004). Spatial working memory among middle-aged and older patients with schizophrenia and volunteers using fMRI. Schizophrenia Research, 68, 203216.CrossRefGoogle Scholar
Klingberg, T., Forssberg, H., & Westerberg, H. (2002). Increased brain activity in frontal and parietal cortex underlies the development of visuospatial working memory capacity during childhood. Journal of Cognitive Neuroscience, 14, 110.Google Scholar
Kwon, H., Reiss, A.L., & Menon, V. (2002). Neural basis of protracted developmental changes in visuo-spatial working memory. Proceedings of the National Academy of Sciences, U.S.A., 99, 1333613341.CrossRefGoogle Scholar
Lancaster, J.L., Woldorff, M.G., Parsons, L.M., Liotti, M., Freitas, C.S., Rainey, L., Kochunov, P.V., Nickerson, D., Mikiten, S.A., & Fox, P.T. (2000). Automated Talairach atlas labels for functional brain mapping. Human Brain Mapping, 10, 120131.Google Scholar
Lawrence, N.S., Ross, T.J., Hoffmann, R., Garavan, H., & Stein, E.A. (2003). Multiple neuronal networks mediate sustained attention. Journal of Cognitive Neuroscience, 15, 10281038.CrossRefGoogle Scholar
Loring-Meier, S. & Halpern, D.F. (1999). Sex differences in visuospatial working memory: Components of cognitive processing. Psychonomic Bulletin and Review, 6, 464471.CrossRefGoogle Scholar
Luks, T.L., Simpson, G.V., Feiwell, R.J., & Miller, W.L. (2002). Evidence for anterior cingulate cortex involvement in monitoring preparatory attentional set. Neuroimage, 17, 792802.Google Scholar
Luna, B., Garver, K.E., Urban, T.A., Lazar, N.A., & Sweeney, J.A. (2004). Maturation of cognitive processes from late childhood to adulthood. Child Development, 75, 13571372.CrossRefGoogle Scholar
MacDonald, A.W. 3rd, Cohen, J.D., Stenger, V.A., & Carter, C.S. (2000). Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science, 288, 18351838.Google Scholar
Manoach, D.S., White, N.S., Lindgren, K.A., Heckers, S., Coleman, M.J., Dubal, S., & Holzman, P.S. (2004). Hemispheric specialization of the lateral prefrontal cortex for strategic processing during spatial and shape working memory. Neuroimage, 21, 894903.CrossRefGoogle Scholar
McKiernan, K.A., Kaufman, J.N., Kucera-Thompson, J., & Binder, J.R. (2003). A parametric manipulation of factors affecting task-induced deactivation in functional neuroimaging. Journal of Cognitive Neuroscience, 15, 394408.Google Scholar
Nikolova, P., Stoyanov, Z., & Negrev, N. (1994). Functional brain asymmetry, handedness and menarcheal age. International Journal of Psychophysiology, 18, 213215.Google Scholar
Passarotti, A.M., Paul, B.M., Bussiere, J.R., Buxton, R.B., Wong, E.C., & Stiles, J. (2003). The development of face and location processing: An fMRI study. Developmental Science, 6, 100117.CrossRefGoogle Scholar
Paus, T., Zijdenbos, A., Worsley, K., Collins, D.L., Blumenthal, J., Giedd, J.N., Rapoport, J.L., & Evans, A.C. (1999). Structural maturation of neural pathways in children and adolescents: In vivo study. Science, 283, 19081911.Google Scholar
Petersen, A., Crockett, L., Richards, M., & Boxer, A. (1988). A self-report measure of pubertal status: Reliability, validity, and initial norms. Journal of Youth and Adolescence, 17, 117133.CrossRefGoogle Scholar
Schweinsburg, A.D., Schweinsburg, B.C., Cheung, E.H., Brown, G.G., Brown, S.A., & Tapert, S.F. (2005). fMRI response to spatial working memory in adolescents with comorbid marijuana and alcohol use disorders. Drug and Alcohol Dependence. 79, 201210.Google Scholar
Smith, E.E. & Jonides, J. (1998). Neuroimaging analyses of human working memory. Proceedings of the National Academy of Sciences, U.S.A., 95, 1206112068.Google Scholar
Sowell, E.R., Peterson, B.S., Thompson, P.M., Welcome, S.E., Henkenius, A.L., & Toga, A.W. (2003). Mapping cortical change across the human life span. Nature Neuroscience, 6, 309315.Google Scholar
Talairach, J. & Tournoux, P. (1988). Coplanar stereotaxic atlas of the human brain. Three-dimensional proportional system: An approach to cerebral imaging. New York: Thieme.
Tapert, S.F., Brown, G.G., Kindermann, S.S., Cheung, E.H., Frank, L.R., & Brown, S.A. (2001). fMRI measurement of brain dysfunction in alcohol-dependent young women. Alcoholism: Clinical and Experimental Research, 25, 236245.Google Scholar
Tapert, S.F., Cheung, E.H., Brown, G.G., Frank, L.R., Paulus, M.P., Schweinsburg, A.D., Meloy, M.J., & Brown, S.A. (2003). Neural response to alcohol stimuli in adolescents with alcohol use disorder. Archives of General Psychiatry, 60, 727735.Google Scholar
Tapert, S.F., Schweinsburg, A.D., Barlett, V.C., Brown, G.G., Brown, S.A., Frank, L.R., Brown, G.G., & Meloy, M.J. (2004). Blood oxygen level dependent response and spatial working memory in adolescents with alcohol use disorders. Alcoholism: Clinical and Experimental Research, 28, 15771586.Google Scholar
Thomas, K.M., King, S.W., Franzen, P.L., Welsh, T.F., Berkowitz, A.L., Noll, D.C., Birmaher, V., & Casey, B.J. (1999). A developmental functional MRI study of spatial working memory. Neuroimage, 10, 327338.Google Scholar
Thomsen, T., Hugdahl, K., Ersland, L., Barndon, R., Lundervold, A., Smievoll, A.I., Roscher, B.E., & Sundberg, H. (2000). Functional magnetic resonance imaging (fMRI) study of sex differences in a mental rotation task. Medical Science Monitor, 6, 11861196.Google Scholar
Ungerleider, L.G. & Haxby, J.V. (1994). ‘What’ and ‘where’ in the human brain. Current Opinion in Neurobiology, 4, 157165.Google Scholar
Vecchi, T. & Girelli, L. (1998). Gender differences in visuo-spatial processing: The importance of distinguishing between passive storage and active manipulation. Acta Psychologica (Amst), 99, 116.Google Scholar
Voyer, D., Voyer, S., & Bryden, M.P. (1995). Magnitude of sex differences in spatial abilities: A meta-analysis and consideration of critical variables. Psychological Bulletin, 117, 250270.CrossRefGoogle Scholar
Vuontela, V., Steenari, M.R., Carlson, S., Koivisto, J., Fjallberg, M., & Aronen, E.T. (2003). Audiospatial and visuospatial working memory in 6–13 year old school children. Learning and Memory, 10, 7481.Google Scholar
Wager, T.D., Jonides, J., & Reading, S. (2004). Neuroimaging studies of shifting attention: A meta-analysis. Neuroimage, 22, 16791693.CrossRefGoogle Scholar
Wager, T.D. & Smith, E.E. (2003). Neuroimaging studies of working memory: A meta-analysis. Cognitive, Affective, & Behavioral Neuroscience, 3, 255274.Google Scholar
Ward, B.D. (1997). Simultaneous inference for FMRI data. Milwaukee, WI: Biophysics Research Institute, Medical College of Wisconsin.
Ward, B.D. (2002). Deconvolution analysis of FMRI time series data. Milwaukee, WI: Biophysics Research Institute, Medical College of Wisconsin.
Wechsler, D. (1993). Manual for the Wechsler Intelligence Scale for Children–III. San Antonio, TX: Psychological Corporation.
Wechsler, D. (1997). Manual for the Wechsler Adult Intelligence Scale–III. San Antonio, TX: Psychological Corporation.
Wechsler, D. (1999). Wechsler Abbreviated Scale of Intelligence. San Antonio, TX: Psychological Corporation.
Weiss, E., Siedentopf, C.M., Hofer, A., Deisenhammer, E.A., Hoptman, M.J., Kremser, C., Golaszewski, S., Felber, S., Fleischhacker, W.W., & Delazer, M. (2003). Sex differences in brain activation pattern during a visuospatial cognitive task: A functional magnetic resonance imaging study in healthy volunteers. Neuroscience Letters, 344, 169172.Google Scholar
Wong, E.C., Luh, W.M., Buxton, R.B., & Frank, L.R. (2000). Single slab high resolution 3D whole brain imaging using spiral FSE. Proceedings of the International Society for Magnetic Resonance in Medicine, 8, 683.Google Scholar
Zald, D.H. & Iacono, W.G. (1998). The development of spatial working memory abilities. Developmental Neuropsychology, 14, 563578.CrossRefGoogle Scholar