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Changes to Memory Structures in Children Treated for Posterior Fossa Tumors

Published online by Cambridge University Press:  24 January 2014

Lily Riggs ,
Eric Bouffet ,
Suzanne Laughlin ,
Normand Laperriere ,
Fang Liu ,
Jovanka Skocic ,
Nadia Scantlebury ,
Frank Wang ,
Nicholas J. Schoenhoff  and
Douglas Strother
...Show all authors
Lily Riggs
Affiliation:
Neurosciences and Mental Health, Hospital for Sick Children, Toronto, Ontario Department of Psychology, Hospital for Sick Children, Toronto, Ontario
Eric Bouffet
Affiliation:
Department of Haematology/Oncology, Hospital for Sick Children, Toronto, Ontario Department of Pediatrics, University of Toronto, Toronto, Ontario
Suzanne Laughlin
Affiliation:
Diagnostic Imaging, Hospital for Sick Children, Toronto, Ontario
Normand Laperriere
Affiliation:
Radiation Oncology, Princess Margaret Hospital, Toronto, Ontario
Fang Liu
Affiliation:
Neurosciences and Mental Health, Hospital for Sick Children, Toronto, Ontario
Jovanka Skocic
Affiliation:
Neurosciences and Mental Health, Hospital for Sick Children, Toronto, Ontario
Nadia Scantlebury
Affiliation:
Neurosciences and Mental Health, Hospital for Sick Children, Toronto, Ontario
Frank Wang
Affiliation:
Diagnostic Imaging, Hospital for Sick Children, Toronto, Ontario
Nicholas J. Schoenhoff
Affiliation:
Neurosciences and Mental Health, Hospital for Sick Children, Toronto, Ontario
Douglas Strother
Affiliation:
Departments of Oncology and Pediatrics, University of Calgary, Calgary, Alberta
Juliette Hukin
Affiliation:
Department of Oncology, British Columbia Children's Hospital, Vancouver, British Columbia
Christopher Fryer
Affiliation:
Department of Oncology, British Columbia Children's Hospital, Vancouver, British Columbia
Dina McConnell
Affiliation:
Department of Psychology, British Columbia Children's Hospital, Vancouver, British Columbia
Donald J. Mabbott*
Affiliation:
Neurosciences and Mental Health, Hospital for Sick Children, Toronto, Ontario Department of Psychology, Hospital for Sick Children, Toronto, Ontario Department of Haematology/Oncology, Hospital for Sick Children, Toronto, Ontario Department of Psychology, University of Toronto, Toronto, Ontario
*
Correspondence and reprint requests to: Donald J. Mabbott, Psychology Department, 555 University Avenue, Toronto, Ontario, Canada M5G 1X8. E-mail: [email protected]
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Abstract

Children treated for medulloblastoma (MB) exhibit long-term impairments in declarative memory, but the pathophysiology underlying this is unclear. Previous studies report declines in global white matter volume, but have failed to link this to declines in memory performance. We examined the effects of treatment on measures of global brain structure (i.e., total white and gray matter volume) and specific memory structures (i.e., hippocampus and uncinate fasciculus). We used volumetric MRI and diffusion tensor imaging in pediatric survivors of MB and one survivor of astrocytoma treated with cranial-spinal radiation (n = 20), and healthy controls (n = 13). Compared to controls, the survivor group exhibited reduced white matter volume, damage to the uncinate fasciculus, and a smaller right hippocampus. Critically, reduced hippocampal volume was not related to differences in brain volume, suggesting that the hippocampus may be especially vulnerable to treatment effects. A subset of the survivors (n = 10) also underwent memory testing using the Children's Memory Scale (CMS). Performance on the general index of the CMS was significantly correlated with measures of hippocampal volume and uncinate fasciculus. The examination of treatment effects on specific brain regions provides a better understanding of long-term cognitive outcome in children with brain tumors, particularly medulloblastoma. (JINS, 2014, 1, 1–13)

Keywords

HippocampusUncinate fasciculusWhite matterMagnetic resonance imaging (MRI)Diffusion tensor imaging (DTI)Probabilistic tractography
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 20 , Issue 2 , February 2014 , pp. 168 - 180
Copyright
Copyright © The International Neuropsychological Society 2014 

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References

Abayomi, O.K. (1996). Pathogenesis of irradiation-induced cognitive dysfunction. Acta Oncologica, 35(6), 659–663.Google Scholar
Andres-Mach, M., Rola, R., Fike, J.R. (2008). Radiation effects on neural precursor cells in the dentate gyrus. Cell and Tissue Research, 331(1), 251–262. doi:10.1007/s00441-007-0480-9 Google Scholar
Arndt, S., Cohen, G., Alliger, R.J., Swayze, V.W. Jr., Andreasen, N.C. (1991). Problems with ratio and proportion measures of imaged cerebral structures. Psychiatry Research, 40(1), 79–89.CrossRefGoogle ScholarPubMed
Beaulieu, C. (2002). The basis of anisotropic water diffusion in the nervous system – A technical review. NMR in Biomedicine, 15(7–8), 435–455. doi:10.1002/nbm.782 CrossRefGoogle ScholarPubMed
Behrens, T.E., Berg, H.J., Jbabdi, S., Rushworth, M.F., Woolrich, M.W. (2007). Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? Neuroimage, 34(1), 144–155. doi:10.1016/j.neuroimage.2006.09.018 Google Scholar
Ben Abdallah, N.M., Filipkowski, R.K., Pruschy, M., Jaholkowski, P., Winkler, J., Kaczmarek, L., Lipp, H.P. (2013). Impaired long-term memory retention: Common denominator for acutely or genetically reduced hippocampal neurogenesis in adult mice. Behavioural Brain Research. doi:10.1016/j.bbr.2013.05.034 CrossRefGoogle ScholarPubMed
Castilla-Ortega, E., Pedraza, C., Estivill-Torrus, G., Santin, L.J. (2011). When is adult hippocampal neurogenesis necessary for learning? evidence from animal research. Reviews in the Neurosciences, 22(3), 267–283. doi:10.1515/RNS.2011.027 CrossRefGoogle ScholarPubMed
Catani, M., Howard, R.J., Pajevic, S., Jones, D.K. (2002). Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage, 17(1), 77–94.Google Scholar
Catani, M., Thiebaut de Schotten, M. (2008). A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex, 44(8), 1105–1132. doi:10.1016/j.cortex.2008.05.004 Google Scholar
Copeland, D.R., deMoor, C., Moore, B.D. III, Ater, J.L. (1999). Neurocognitive development of children after a cerebellar tumor in infancy: A longitudinal study. Journal of Clinical Oncology, 17(11), 3476–3486.CrossRefGoogle ScholarPubMed
Demaster, D.M., Ghetti, S. (2012). Developmental differences in hippocampal and cortical contributions to episodic retrieval. Cortex, 49(6), 1482–1493. doi:10.1016/j.cortex.2012.08.004 Google Scholar
Dennis, M., Spiegler, B.J., Hetherington, C.R., Greenberg, M.L. (1996). Neuropsychological sequelae of the treatment of children with medulloblastoma. Journal of Neuro-Oncology, 29(1), 91–101.CrossRefGoogle ScholarPubMed
Duvernoy, H.M. (2005). The human hippocampus: Functional anatomy, vascularization and serial sections with MRI (3rd ed.). Berlin: Springer.CrossRefGoogle Scholar
Edelstein, K., Spiegler, B.J., Fung, S., Panzarella, T., Mabbott, D.J., Jewitt, N., Hodgson, D.C. (2011). Early aging in adult survivors of childhood medulloblastoma: Long-term neurocognitive, functional, and physical outcomes. Neuro-Oncology, 13(5), 536–545. doi:10.1093/neuonc/nor015 Google Scholar
Eichenbaum, H. (2013). What H.M. taught us. Journal of Cognitive Neuroscience, 25(1), 14–21. doi:10.1162/jocn_a_00285 Google Scholar
Eijkenboom, M., Van Der Staay, F.J. (1999). Spatial learning deficits in rats after injection of vincristine into the dorsal hippocampus. Neuroscience, 91(4), 1299–1313.CrossRefGoogle ScholarPubMed
Free, S.L., Bergin, P.S., Fish, D.R., Cook, M.J., Shorvon, S.D., Stevens, J.M. (1995). Methods for normalization of hippocampal volumes measured with MR. American Journal of Neuroradiology, 16(4), 637–643.Google Scholar
Gajjar, A., Chintagumpala, M., Ashley, D., Kellie, S., Kun, L.E., Merchant, T.E., Gilbertson, R.J. (2006). Risk-adapted craniospinal radiotherapy followed by high-dose chemotherapy and stem-cell rescue in children with newly diagnosed medulloblastoma (St Jude Medulloblastoma-96): Long-term results from a prospective, multicentre trial. The Lancet Oncology, 7(10), 813–820. doi:10.1016/S1470-2045(06)70867-1 Google Scholar
George, A.P., Kuehn, S.M., Vassilyadi, M., Richards, P.M., Parlow, S.E., Keene, D.L., Ventureyra, E.C. (2003). Cognitive sequelae in children with posterior fossa tumors. Pediatric Neurology, 28(1), 42–47.Google Scholar
Ghetti, S., Bunge, S.A. (2012). Neural changes underlying the development of episodic memory during middle childhood. Developmental Cognitive Neuroscience, 2(4), 381–395. doi:10.1016/j.dcn.2012.05.002 CrossRefGoogle ScholarPubMed
Ghetti, S., DeMaster, D.M., Yonelinas, A.P., Bunge, S.A. (2010). Developmental differences in medial temporal lobe function during memory encoding. The Journal of Neuroscience, 30(28), 9548–9556. doi:10.1523/JNEUROSCI.3500-09.2010 CrossRefGoogle ScholarPubMed
Gogtay, N., Nugent, T.F. III, Herman, D.H., Ordonez, A., Greenstein, D., Hayashi, K.M., Thompson, P.M. (2006). Dynamic mapping of normal human hippocampal development. Hippocampus, 16(8), 664–672. doi:10.1002/hipo.20193 CrossRefGoogle ScholarPubMed
Gold, J.J., Squire, L.R. (2005). Quantifying medial temporal lobe damage in memory-impaired patients. Hippocampus, 15(1), 79–85. doi:10.1002/hipo.20032 Google Scholar
Gottardo, N.G., Gajjar, A. (2006). Current therapy for medulloblastoma. Current Treatment Options in Neurology, 8(4), 319–334.Google Scholar
Habrand, J.L., De Crevoisier, R. (2001). Radiation therapy in the management of childhood brain tumors. Child's Nervous System, 17(3), 121–133.Google Scholar
Insausti, R., Cebada-Sanchez, S., Marcos, P. (2010). Postnatal development of the human hippocampal formation. Advances in Anatomy, Embryology and Cell Biology, 206, 1–86.Google Scholar
Isaacs, E.B., Vargha-Khadem, F., Watkins, K.E., Lucas, A., Mishkin, M., Gadian, D.G. (2003). Developmental amnesia and its relationship to degree of hippocampal atrophy. Proceedings of the National Academy of Sciences of the United States of America, 100(22), 13060–13063. doi:10.1073/pnas.1233825100 Google Scholar
Khong, P.L., Kwong, D.L., Chan, G.C., Sham, J.S., Chan, F.L., Ooi, G.C. (2003). Diffusion-tensor imaging for the detection and quantification of treatment-induced white matter injury in children with medulloblastoma: A pilot study. AJNR American Journal of Neuroradiology, 24(4), 734–740.Google Scholar
Khong, P.L., Leung, L.H., Fung, A.S., Fong, D.Y., Qiu, D., Kwong, D.L., Chan, G.C. (2006). White matter anisotropy in post-treatment childhood cancer survivors: Preliminary evidence of association with neurocognitive function. Journal of Clinical Oncology, 24(6), 884–890. doi:10.1200/JCO.2005.02.4505 Google Scholar
Kieffer-Renaux, V., Bulteau, C., Grill, J., Kalifa, C., Viguier, D., Jambaque, I. (2000). Patterns of neuropsychological deficits in children with medulloblastoma according to craniospatial irradiation doses. Developmental Medicine and Child Neurology, 42(11), 741–745.Google Scholar
Lafay-Cousin, L., Bouffet, E., Hawkins, C., Amid, A., Huang, A., Mabbott, D.J. (2009). Impact of radiation avoidance on survival and neurocognitive outcome in infant medulloblastoma. Current Oncology, 16(6), 21–28.Google Scholar
Law, N., Bouffet, E., Laughlin, S., Laperriere, N., Briere, M.E., Strother, D., Mabbott, D. (2011). Cerebello-thalamo-cerebral connections in pediatric brain tumor patients: Impact on working memory. Neuroimage, 56(4), 2238–2248. doi:10.1016/j.neuroimage.2011.03.065 Google Scholar
Lebel, C., Beaulieu, C. (2011). Longitudinal development of human brain wiring continues from childhood into adulthood. The Journal of Neuroscience, 31(30), 10937–10947. doi:10.1523/JNEUROSCI.5302-10.2011 Google Scholar
Lebel, C., Walker, L., Leemans, A., Phillips, L., Beaulieu, C. (2008). Microstructural maturation of the human brain from childhood to adulthood. Neuroimage, 40(3), 1044–1055. doi:10.1016/j.neuroimage.2007.12.053 CrossRefGoogle ScholarPubMed
Lerch, J.P., Yiu, A.P., Martinez-Canabal, A., Pekar, T., Bohbot, V.D., Frankland, P.W., Sled, J.G. (2011). Maze training in mice induces MRI-detectable brain shape changes specific to the type of learning. Neuroimage, 54(3), 2086–2095. doi:10.1016/j.neuroimage.2010.09.086 Google Scholar
Luskin, M.B. (1993). Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron, 11(1), 173–189.Google Scholar
Mabbott, D.J., Noseworthy, M.D., Bouffet, E., Rockel, C., Laughlin, S. (2006). Diffusion tensor imaging of white matter after cranial radiation in children for medulloblastoma: Correlation with IQ. Neuro-Oncology, 8(3), 244–252. doi:10.1215/15228517-2006-002 Google Scholar
Mabbott, D.J., Penkman, L., Witol, A., Strother, D., Bouffet, E. (2008). Core neurocognitive functions in children treated for posterior fossa tumors. Neuropsychology, 22(2), 159–168. doi:10.1037/0894-4105.22.2.159 Google Scholar
Mabbott, D.J., Rovet, J., Noseworthy, M.D., Smith, M.L., Rockel, C. (2009). The relations between white matter and declarative memory in older children and adolescents. Brain Research, 1294, 80–90. doi:10.1016/j.brainres.2009.07.046 Google Scholar
Madsen, T.M., Kristjansen, P.E., Bolwig, T.G., Wortwein, G. (2003). Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience, 119(3), 635–642.Google Scholar
McEwen, B.S. (1999). Stress and hippocampal plasticity. Annual Review of Neuroscience, 22, 105–122. doi:10.1146/annurev.neuro.22.1.105 Google Scholar
Monje, M.L., Palmer, T. (2003). Radiation injury and neurogenesis. Current Opinion in Neurology, 16(2), 129–134. doi:10.1097/01.wco.0000063772.81810.b7 Google Scholar
Monje, M.L., Vogel, H., Masek, M., Ligon, K.L., Fisher, P.G., Palmer, T.D. (2007). Impaired human hippocampal neurogenesis after treatment for central nervous system malignancies. Annals of Neurology, 62(5), 515–520. doi:10.1002/ana.21214 Google Scholar
Moore, B.D. III. (2005). Neurocognitive outcomes in survivors of childhood cancer. Journal of Pediatric Psychology, 30(1), 51–63.Google Scholar
Mulhern, R.K., Merchant, T.E., Gajjar, A., Reddick, W.E., Kun, L.E. (2004). Late neurocognitive sequelae in survivors of brain tumours in childhood. The Lancet Oncology, 5(7), 399–408. doi:10.1016/S1470-2045(04)01507-4 Google Scholar
Mulhern, R.K., Palmer, S.L., Reddick, W.E., Glass, J.O., Kun, L.E., Taylor, J., Gajjar, A. (2001). Risks of young age for selected neurocognitive deficits in medulloblastoma are associated with white matter loss. Journal of Clinical Oncology, 19(2), 472–479.Google Scholar
Mulhern, R.K., Reddick, W.E., Palmer, S.L., Glass, J.O., Elkin, T.D., Kun, L.E., Gajjar, A. (1999). Neurocognitive deficits in medulloblastoma survivors and white matter loss. Annals of Neurology, 46(6), 834–841.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Mulhern, R.K., White, H.A., Glass, J.O., Kun, L.E., Leigh, L., Thompson, S.J., Reddick, W.E. (2004). Attentional functioning and white matter integrity among survivors of malignant brain tumors of childhood. Journal of the International Neuropsychological Society, 10(2), 180–189 doi:10.1017/S135561770410204X Google Scholar
Nagel, B.J., Delis, D.C., Palmer, S.L., Reeves, C., Gajjar, A., Mulhern, R.K. (2006). Early patterns of verbal memory impairment in children treated for medulloblastoma. Neuropsychology, 20(1), 105–112. doi:10.1037/0894-4105.20.1.105 Google Scholar
Nagel, B.J., Palmer, S.L., Reddick, W.E., Glass, J.O., Helton, K.J., Wu, S., Mulhern, R.K. (2004). Abnormal hippocampal development in children with medulloblastoma treated with risk-adapted irradiation. AJNR American Journal of Neuroradiology, 25(9), 1575–1582.Google Scholar
Nagy, Z., Westerberg, H., Klingberg, T. (2004). Maturation of white matter is associated with the development of cognitive functions during childhood. Journal of Cognitive Neuroscience, 16(7), 1227–1233. doi:10.1162/0898929041920441 CrossRefGoogle ScholarPubMed
Ofen, N., Chai, X.J., Schuil, K.D., Whitfield-Gabrieli, S., Gabrieli, J.D. (2012). The development of brain systems associated with successful memory retrieval of scenes. The Journal of Neuroscience, 32(29), 10012–10020. doi:10.1523/JNEUROSCI.1082-11.2012 Google Scholar
Olsen, R.K., Palombo, D.J., Rabin, J.S., Levine, B., Ryan, J.D., Rosenbaum, R.S. (2013). Volumetric analysis of medial temporal lobe subregions in developmental amnesia using high-resolution magnetic resonance imaging. Hippocampus, doi:10.1002/hipo.22153 Google Scholar
Padovani, L., Andre, N., Constine, L.S., Muracciole, X. (2012). Neurocognitive function after radiotherapy for paediatric brain tumours. Nature Reviews. Neurology, 8(10), 578–588. doi:10.1038/nrneurol.2012.182 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
Palmer, S.L., Goloubeva, O., Reddick, W.E., Glass, J.O., Gajjar, A., Kun, L., Mulhern, R.K. (2001). Patterns of intellectual development among survivors of pediatric medulloblastoma: A longitudinal analysis. Journal of Clinical Oncology, 19(8), 2302–2308.Google Scholar
Palmer, S.L., Reddick, W.E., Gajjar, A. (2007). Understanding the cognitive impact on children who are treated for medulloblastoma. Journal of Pediatric Psychology, 32(9), 1040–1049. doi:10.1093/jpepsy/jsl056 Google Scholar
Pereira, J.B., Junque, C., Bartres-Faz, D., Ramirez-Ruiz, B., Marti, M.J., Tolosa, E. (2013). Regional vulnerability of hippocampal subfields and memory deficits in Parkinson's disease. Hippocampus, 23(8), 720–728. doi:10.1002/hipo.22131 Google Scholar
Pfefferbaum, A., Mathalon, D.H., Sullivan, E.V., Rawles, J.M., Zipursky, R.B., Lim, K.O. (1994). A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. Archives of Neurology, 51(9), 874–887.Google Scholar
Pfluger, T., Weil, S., Weis, S., Vollmar, C., Heiss, D., Egger, J., Hahn, K. (1999). Normative volumetric data of the developing hippocampus in children based on magnetic resonance imaging. Epilepsia, 40(4), 414–423.Google Scholar
Pruessner, J.C., Li, L.M., Serles, W., Pruessner, M., Collins, D.L., Kabani, N., Evans, A.C. (2000). Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: minimizing the discrepancies between laboratories. Cerebral cortex, 10(4), 433–442.Google Scholar
Qiu, D., Leung, L.H., Kwong, D.L., Chan, G.C., Khong, P.L. (2006). Mapping radiation dose distribution on the fractional anisotropy map: Applications in the assessment of treatment-induced white matter injury. Neuroimage, 31(1), 109–115. doi:10.1016/j.neuroimage.2005.12.007 Google Scholar
Raber, J., Fan, Y., Matsumori, Y., Liu, Z., Weinstein, P.R., Fike, J.R., Liu, J. (2004). Irradiation attenuates neurogenesis and exacerbates ischemia-induced deficits. Annals of Neurology, 55(3), 381–389 doi:10.1002/ana.10853 Google Scholar
Reddick, W.E., Glass, J.O., Palmer, S.L., Wu, S., Gajjar, A., Langston, J.W., Mulhern, R.K. (2005). Atypical white matter volume development in children following craniospinal irradiation. Neuro-Oncology, 7(1), 12–19. doi:10.1215/S1152851704000079 CrossRefGoogle ScholarPubMed
Reddick, W.E., Russell, J.M., Glass, J.O., Xiong, X., Mulhern, R.K., Langston, J.W., Gajjar, A. (2000). Subtle white matter volume differences in children treated for medulloblastoma with conventional or reduced dose craniospinal irradiation. Magnetic Resonance Imaging, 18(7), 787–793.CrossRefGoogle ScholarPubMed
Reddick, W.E., White, H.A., Glass, J.O., Wheeler, G.C., Thompson, S.J., Gajjar, A., Mulhern, R.K. (2003). Developmental model relating white matter volume to neurocognitive deficits in pediatric brain tumor survivors. Cancer, 97(10), 2512–2519. doi:10.1002/cncr.11355 Google Scholar
Ris, M.D., Packer, R., Goldwein, J., Jones-Wallace, D., Boyett, J.M. (2001). Intellectual outcome after reduced-dose radiation therapy plus adjuvant chemotherapy for medulloblastoma: A Children's Cancer Group study. Journal of Clinical Oncology, 19(15), 3470–3476.Google Scholar
Rutkowski, S., Bode, U., Deinlein, F., Ottensmeier, H., Warmuth-Metz, M., Soerensen, N., Kuehl, J. (2005). Treatment of early childhood medulloblastoma by postoperative chemotherapy alone. The New England Journal of Medicine, 352(10), 978–986. doi:10.1056/NEJMoa042176 Google Scholar
Saxe, M.D., Battaglia, F., Wang, J.W., Malleret, G., David, D.J., Monckton, J.E., Drew, M.R. (2006). Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proceedings of the National Academy of Sciences of the United States of America, 103(46), 17501–17506. doi:10.1073/pnas.0607207103 Google Scholar
Shabani, M., Larizadeh, M.H., Parsania, S., Asadi Shekaari, M., Shahrokhi, N. (2012). Profound destructive effects of adolescent exposure to vincristine accompanied with some sex differences in motor and memory performance. Canadian Journal of Physiology and Pharmacology, 90(4), 379–386. doi:10.1139/Y11-132 Google Scholar
Shabani, M., Larizadeh, M.H., Parsania, S., Hajali, V., Shojaei, A. (2012). Evaluation of destructive effects of exposure to cisplatin during developmental stage: No profound evidence for sex differences in impaired motor and memory performance. The International Journal of Neuroscience, 122(8), 439–448. doi:10.3109/00207454.2012.673515 Google Scholar
Shan, Z.Y., Liu, J.Z., Glass, J.O., Gajjar, A., Li, C.S., Reddick, W.E. (2006). Quantitative morphologic evaluation of white matter in survivors of childhood medulloblastoma. [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't]. Magn Reson Imaging, 24(8), 1015–1022. doi:10.1016/j.mri.2006.04.015 Google Scholar
Shors, T.J., Townsend, D.A., Zhao, M., Kozorovitskiy, Y., Gould, E. (2002). Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus, 12(5), 578–584. doi:10.1002/hipo.10103 Google Scholar
Smith, S.M., Jenkinson, M., Woolrich, M.W., Beckmann, C.F., Behrens, T.E., Johansen-Berg, H., Matthews, P.M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage, 23(Suppl 1), S208–S219. doi:10.1016/j.neuroimage.2004.07.051 Google Scholar
Spiegler, B.J., Bouffet, E., Greenberg, M.L., Rutka, J.T., Mabbott, D.J. (2004). Change in neurocognitive functioning after treatment with cranial radiation in childhood. Journal of Clinical Oncology, 22(4), 706–713. doi:10.1200/JCO.2004.05.186 Google Scholar
Squire, L.R. (1992). Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychological Review, 99(2), 195–231.Google Scholar
Thatcher, R.W., Walker, R.A., Giudice, S. (1987). Human cerebral hemispheres develop at different rates and ages. Science, 236(4805), 1110–1113.Google Scholar
Van Petten, C. (2004). Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: Review and meta-analysis. Neuropsychologia, 42(10), 1394–1413. doi:0.1016/j.neuropsychologia.2004.04.006 Google Scholar
Winocur, G., Wojtowicz, J.M., Sekeres, M., Snyder, J.S., Wang, S. (2006). Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus, 16(3), 296–304. doi:10.1002/hipo.20163 Google Scholar
Wong-Goodrich, S.J., Pfau, M.L., Flores, C.T., Fraser, J.A., Williams, C.L., Jones, L.W. (2010). Voluntary running prevents progressive memory decline and increases adult hippocampal neurogenesis and growth factor expression after whole-brain irradiation. Cancer Research, 70(22), 9329–9338. doi:10.1158/0008-5472.CAN-10-1854 Google Scholar
Woolrich, M.W., Jbabdi, S., Patenaude, B., Chappell, M., Makni, S., Behrens, T., Smith, S.M. (2009). Bayesian analysis of neuroimaging data in FSL. Neuroimage, 45(1 Suppl), S173–S186. doi:10.1016/j.neuroimage.2008.10.055 Google Scholar