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Neural Underpinnings of Working Memory in Adult Survivors of Childhood Brain Tumors

Published online by Cambridge University Press:  03 August 2015

Tricia Z. King ,
Sabrina Na  and
Hui Mao
Tricia Z. King*
Affiliation:
Department of Psychology and Neuroscience Institute, Georgia State University
Sabrina Na
Affiliation:
Department of Psychology and Neuroscience Institute, Georgia State University
Hui Mao
Affiliation:
Department of Radiology and Imaging Sciences, Emory University
*
Correspondence and reprint requests to: Tricia Z. King, Georgia State University Department of Psychology, P.O. Box 5010, Atlanta, GA 30302-5010. E-mail: tzking@gsu.edu
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Abstract

Adult survivors of childhood brain tumors are at risk for cognitive performance deficits that require the core cognitive skill of working memory. Our goal was to examine the neural mechanisms underlying working memory performance in survivors. We studied the working memory of adult survivors of pediatric posterior fossa brain tumors using a letter n-back paradigm with varying cognitive workload (0-, 1-, 2-, and 3-back) and functional magnetic resonance imaging as well as neuropsychological measures. Survivors of childhood brain tumors evidenced lower working memory performance than demographically matched healthy controls. Whole-brain analyses revealed significantly greater blood-oxygen level dependent (BOLD) activation in the left superior / middle frontal gyri and left parietal lobe during working memory (2-back versus 0-back contrast) in survivors. Left frontal BOLD response negatively correlated with 2- and 3-back working memory performance, Auditory Consonant Trigrams (ACT), and Digit Span Backwards. In contrast, parietal lobe BOLD response negatively correlated with 0-back (vigilance task) and ACT. The results revealed that adult survivors of childhood posterior fossa brain tumors recruited additional cognitive control resources in the prefrontal lobe during increased working memory demands. This increased prefrontal activation is associated with lower working memory performance and is consistent with the allocation of latent resources theory. (JINS, 2015, 21, 494–505)

Keywords

NeuroimagingExecutive functionPosterior fossaNeoplasmn-backPediatric
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 21 , Issue 7 , August 2015 , pp. 494 - 505
Copyright
Copyright © The International Neuropsychological Society 2015 

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References

Armstrong, G. T., Liu, Q., Yasui, Y., Huang, S., Ness, K. K., Leisenring, W., & Packer, R. J. (2009). Long-term outcomes among adult survivors of childhood central nervous system malignancies in the Childhood Cancer Survivor Study. Journal of the National Cancer Institute, 101(13), 946–958. doi:10.1093/jnci/djp148 CrossRefGoogle ScholarPubMed
Baddeley, A. (2012). Working memory: Theories, models, and controversies. Annual Review of Psychology, 63, 1–29. doi:10.1146/annurev-psych-120710-100422 Google Scholar
Brown, J. (1958). Some tests of the decay theory of immediate memory. Quarterly Journal of Experimental Psychology, 10(1), 12–21.CrossRefGoogle Scholar
Dennis, M., Francis, D. J., Cirino, P. T., Schachar, R., Barnes, M. A., & Fletcher, J. M. (2009). Why IQ is not a covariate in cognitive studies of neurodevelopmental disorders. Journal of the International Neuropsychological Society, 15(3), 331–343. doi:10.1017/S1355617709090481 Google Scholar
Dennis, M., Spiegler, B. J., Obonsawin, M. C., Maria, B. L., Cowell, C., Hoffman, H. J., & Ehrlich, R. M. (1992). Brain tumors in children and adolescents--III. Effects of radiation and hormone status on intelligence and on working, associative and serial-order memory. Neuropsychologia, 30(3), 257–275.CrossRefGoogle ScholarPubMed
First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. W. (1997). Structured clinical interview for DSM-IV axis 1 disorders (SCID-I)-clinical version. Arlington, VA: American Psychiatric Publishing.Google Scholar
Greve, D. N., & Fischl, B. (2009). Accurate and robust brain image alignment using boundary-based registration. Neuroimage, 48(1), 63–72. doi:10.1016/j.neuroimage.2009.06.060 Google Scholar
Gurney, J. G., Kadan-Lottick, N. S., Packer, R. J., Neglia, J. P., Sklar, C. A., Punyko, J. A., & Robison, L. L. (2003). Endocrine and cardiovascular late effects among adult survivors of childhood brain tumors: Childhood Cancer Survivor Study. Cancer, 97(3), 663–673. doi:10.1002/cncr.11095 Google Scholar
Gurney, J. G., Krull, K. R., Kadan-Lottick, N., Nicholson, H. S., Nathan, P. C., Zebrack, B., & Ness, K. K. (2009). Social outcomes in the Childhood Cancer Survivor Study cohort. Journal of Clinical Oncology, 27(14), 2390–2395. doi:10.1200/jco.2008.21.1458 Google Scholar
Hillary, F. G., Medaglia, J. D., Gates, K., Molenaar, P. C., Slocomb, J., Peechatka, A., & Good, D. C. (2011). Examining working memory task acquisition in a disrupted neural network. Brain, 134(5), 1555–1570. doi:10.1093/brain/awr043 CrossRefGoogle Scholar
Kirchhoff, A. C., Krull, K. R., Ness, K. K., Armstrong, G. T., Park, E. R., Stovall, M., & Leisenring, W. (2011). Physical, mental, and neurocognitive status and employment outcomes in the childhood cancer survivor study cohort. Cancer Epidemiol Biomarkers & Prevention, 20(9), 1838–1849. doi:10.1158/1055-9965.epi-11-0239 Google Scholar
Medaglia, J. D., Chiou, K. S., Slocomb, J., Fitzpatrick, N. M., Wardecker, B. M., Ramanathan, D., & Hillary, F. G. (2012). The less BOLD, the wiser: Support for the latent resource hypothesis after traumatic brain injury. Human Brain Mapping, 33(4), 979–993. doi:10.1002/hbm.21264 Google Scholar
Ostrom, Q. T., de Blank, P. M., Kruchko, C., Petersen, C. M., Liao, P., Finlay, J. L., & Barnholtz-Sloan, J. S. (2015). Alex’s Lemonade Stand Foundation Infant and Childhood Primary Brain and Central Nervous System Tumors Diagnosed in the United States in 2007-2011. Neuro-Oncology, 16(Suppl. 10), x1–x36. doi:10.1093/neuonc/nou327 Google Scholar
Owen, A. M., McMillan, K. M., Laird, A. R., & Bullmore, E. (2005). N-back working memory paradigm: A meta-analysis of normative functional neuroimaging studies. Human Brain Mapping, 25(1), 46–59. doi:10.1002/hbm.20131 Google Scholar
Palmer, S. L. (2008). Neurodevelopmental impact on children treated for medulloblastoma: A review and proposed conceptual model. Developmental Disabilities Research Reviews, 14(3), 203–210. doi:10.1002/ddrr.32 Google Scholar
Perlstein, W. M., Dixit, N. K., Carter, C. S., Noll, D. C., & Cohen, J. D. (2003). Prefrontal cortex dysfunction mediates deficits in working memory and prepotent responding in schizophrenia. Biological Psychiatry, 53(1), 25–38.Google Scholar
Peterson, L. R., & Peterson, M. J. (1959). Short-term retention of individual verbal items. Journal of Expimental Psychology, 58, 193–198.Google Scholar
Price, C. J., & Friston, K. J. (1997). Cognitive conjunction: A new approach to brain activation experiments. Neuroimage, 5(4), 261–270.Google Scholar
Reeves, C. B., Palmer, S. L., Reddick, W. E., Merchant, T. E., Buchanan, G. M., Gajjar, A., & Mulhern, R. K. (2006). Attention and memory functioning among pediatric patients with medulloblastoma. Journal of Pediatric Psychology, 31(3), 272–280. doi:10.1093/jpepsy/jsj019 Google Scholar
Robinson, K. E., Fraley, C. E., Pearson, M. M., Kuttesch, J. F. Jr., & Compas, B. E. (2013). Neurocognitive late effects of pediatric brain tumors of the posterior fossa: A quantitative review. Journal of the International Neuropsychological Society, 19(1), 44–53. doi:10.1017/s1355617712000987 Google Scholar
Robinson, K. E., Pearson, M. M., Cannistraci, C. J., Anderson, A. W., Kuttesch, J. F. Jr., Wymer, K., & Compas, B. E. (2014a). Functional neuroimaging of working memory in survivors of childhood brain tumors and healthy children: Associations with coping and psychosocial outcomes. Child Neuropsychology, 1–24. doi:10.1080/09297049.2014.924492 Google Scholar
Robinson, K. E., Pearson, M. M., Cannistraci, C. J., Anderson, A. W., Kuttesch, J. F., Wymer, K., & Compas, B. E. (2014b). Neuroimaging of executive function in survivors of pediatric brain tumors and healthy controls. Neuropsychology, 28(5), 791–800. doi:10.1037/neu0000077 CrossRefGoogle ScholarPubMed
Schatz, J., Kramer, J. H., Ablin, A., & Matthay, K. K. (2000). Processing speed, working memory, and IQ: A developmental model of cognitive deficits following cranial radiation therapy. Neuropsychology, 14(2), 189–200.Google Scholar
Smith, E. E., & Jonides, J. (1997). Working memory: A view from neuroimaging. Cognitive Psychology, 33(1), 5–42. doi:10.1006/cogp.1997.0658 Google Scholar
Smith, E. E., & Jonides, J. (1998). Neuroimaging analyses of human working memory. Proceedings of the National Academy of Sciences of the United States of America, 95(20), 12061–12068.Google Scholar
Stuss, D. T. (1987). Contribution of frontal lobe injury to cognitive impairment after closed head injury: Methods of assessment and recent findings. In H. S. Levin, J. Grafman & H. M. Eisernberg (Eds.), Neurobehavioral recovery from head injury. New York: Oxford Uniersity Press.Google Scholar
Sweet, L. H., Rao, S. M., Primeau, M., Durgerian, S., & Cohen, R. A. (2006). Functional magnetic resonance imaging response to increased verbal working memory demands among patients with multiple sclerosis. Human Brain Mapping, 27(1), 28–36. doi:10.1002/hbm.20163 Google Scholar
Waber, D. P., Pomeroy, S. L., Chiverton, A. M., Kieran, M. W., Scott, R. M., Goumnerova, L. C., & Rivkin, M. J. (2006). Everyday cognitive function after craniopharyngioma in childhood. Pediatric Neurology, 34(1), 13–19. doi:10.1016/j.pediatrneurol.2005.06.002 Google Scholar
Wechsler, D. (1997). Wechsler Memory Scale- Third edition. Administration and scoring manual. San Antonio, TX: The Psychological Corporation.Google Scholar
Wechsler, D. (2011). Wechsler Abbreviated Scale of Intelligence- Second Edition Manual. Bloomington, MN: Pearson.Google Scholar
Wolfe, K. R., Madan-Swain, A., Hunter, G. R., Reddy, A. T., Banos, J., & Kana, R. K. (2013). An fMRI investigation of working memory and its relationship with cardiorespiratory fitness in pediatric posterior fossa tumor survivors who received cranial radiation therapy. Pediatric Blood & Cancer, 60(4), 669–675. doi:10.1002/pbc.24331 CrossRefGoogle ScholarPubMed
Wolfe, K. R., Madan-Swain, A., & Kana, R. K. (2012). Executive dysfunction in pediatric posterior fossa tumor survivors: A systematic literature review of neurocognitive deficits and interventions. Developmental Neuropsychology, 37(2), 153–175. doi:10.1080/87565641.2011.632462 CrossRefGoogle ScholarPubMed