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Cognitive Performance, Aerobic Fitness, Motor Proficiency, and Brain Function Among Children Newly Diagnosed With Craniopharyngioma

Published online by Cambridge University Press:  03 May 2019

Heather M. Conklin ,
Kirsten K. Ness ,
Jason M. Ashford ,
Matthew A. Scoggins ,
Robert J. Ogg ,
Yuanyuan Han ,
Yimei Li ,
Julie A. Bradley ,
Frederick A. Boop  and
Thomas E. Merchant
Heather M. Conklin*
Affiliation:
Department of Psychology, St. Jude Children’s Research Hospital, Memphis, Tennessee
Kirsten K. Ness
Affiliation:
Department of Epidemiology/Cancer Control, St. Jude Children’s Research Hospital, Memphis, Tennessee
Jason M. Ashford
Affiliation:
Department of Psychology, St. Jude Children’s Research Hospital, Memphis, Tennessee
Matthew A. Scoggins
Affiliation:
Division of Translational Imaging, St. Jude Children’s Research Hospital, Memphis, Tennessee
Robert J. Ogg
Affiliation:
Division of Translational Imaging, St. Jude Children’s Research Hospital, Memphis, Tennessee
Yuanyuan Han
Affiliation:
Department of Biostatistics, St. Jude Children’s Research Hospital, Memphis, Tennessee
Yimei Li
Affiliation:
Department of Biostatistics, St. Jude Children’s Research Hospital, Memphis, Tennessee
Julie A. Bradley
Affiliation:
Department of Radiation Oncology, University of Florida Health Proton Therapy Institute, Jacksonville, Florida
Frederick A. Boop
Affiliation:
Department of Surgery, St. Jude Children’s Research Hospital, Memphis, Tennessee
Thomas E. Merchant
Affiliation:
Department of Radiation Oncology, St. Jude Children’s Research Hospital, Memphis, Tennessee
*
Correspondence and reprint requests to: Heather M. Conklin, Department of Psychology, Mail Stop #740, St. Jude Children’s Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105-2794. E-mail: [email protected]
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Abstract

Objectives: Craniopharyngioma survivors experience cognitive deficits that negatively impact quality of life. Aerobic fitness is associated with cognitive benefits in typically developing children and physical exercise promotes recovery following brain injury. Accordingly, we investigated cognitive and neural correlates of aerobic fitness in a sample of craniopharyngioma patients. Methods: Patients treated for craniopharyngioma [N=104, 10.0±4.6 years, 48% male] participated in fitness, cognitive and fMRI (n=51) assessments following surgery but before proton radiation therapy. Results: Patients demonstrated impaired aerobic fitness [peak oxygen uptake (PKVO2)=23.9±7.1, 41% impaired (i.e., 1.5 SD<normative mean)], motor proficiency [Bruininks-Oseretsky (BOT2)=38.6±9.0, 28% impaired], and executive functions (e.g., WISC-IV Working Memory Index (WMI)=96.0±15.3, 11% impaired). PKVO2 correlated with better executive functions (e.g., WISC-IV WMI r=.27, p=.02) and academic performance (WJ-III Calculation r=.24, p=.04). BOT2 correlated with better attention (e.g., CPT-II omissions r=.26, p=.04) and executive functions (e.g., WISC-IV WMI r=.32, p=.01). Areas of robust neural activation during an n-back task included superior parietal lobule, dorsolateral prefrontal cortex, and middle and superior frontal gyri (p<.05, corrected). Higher network activation was associated with better working memory task performance and better BOT2 (p<.001). Conclusions: Before adjuvant therapy, children with craniopharyngioma demonstrate significantly reduced aerobic fitness, motor proficiency, and working memory. Better aerobic fitness and motor proficiency are associated with better attention and executive functions, as well as greater activation of a well-established working memory network. These findings may help explain differential risk/resiliency with respect to acute cognitive changes that may portend cognitive late effects. (JINS, 2019, 25, 413–425)

Keywords

PediatricBrain tumorCognitive late effectsfMRIAcquired brain injuryExercise
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 25 , Issue 4 , April 2019 , pp. 413 - 425
Copyright
Copyright © The International Neuropsychological Society, 2019. 

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References

REFERENCES

Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological), 57, 289–300.CrossRefGoogle Scholar
Bigler, E.D., & Stern, Y. (2015). Traumatic brain injury and reserve. Handbook of Clinical Neurology, 128, 691–710. doi:10.106/B978-0-444-63521-1.00043-1CrossRefGoogle ScholarPubMed
Bruininks, R.H., & Bruininks, B.D. (2005). BOT2 Bruiniks-Oseretsky Test of Motor Proficiency, Second Edition. Circle Pines, MN: AGS Publishing.Google Scholar
Castelli, D.M., Hillman, C.H., Hirsch, J., Hirsch, A., & Drollette, E. (2011). FIT Kids: Time in target heart zone and cognitive performance. Preventative Medicine, 1, S55–S59. doi:10.1016/j.ypmed.2011.01.019CrossRefGoogle Scholar
Castellino, S.M., Ullrich, N.J., Whelen, M.J., & Lange, B.J. (2014). Developing interventions for cancer-related cognitive dysfunction in childhood cancer survivors. Journal of the National Cancer Institute, 106(8), pii: dju186. http://doi.org/10.1093/jnci/dju186CrossRefGoogle ScholarPubMed
Chaddock, L., Erickson, K.I., Prakash, R.S., Kim, J.S., Voss, M.W., VanPatter, M., … Kramer, F. (2010). A neuroimaging investigation of the association between aerobic fitness, hippocampal volume, and memory performance in preadolescent children. Brain Research, 1358, 172–183. doi:10.1016/j.brainres.2010.08.049CrossRefGoogle ScholarPubMed
Chaddock, L., Erickson, K.I., Prakash, R.S., VanPatter, M., Voss, M.W., Pontifex, M.B., … Kramer, A.F. (2010). Basal ganglia volume is associated with aerobic fitness in preadolescent children. Developmental Neuroscience, 32, 249–256. doi:10.1159/000316648CrossRefGoogle ScholarPubMed
Chaddock, L., Erickson, K.I., Prakash, R.S., Voss, M.W.V., VanPatter, M., Pontifex, M.B., … Kramer, A.F. (2012). A functional MRI investigation of the association between childhood aerobic fitness and neurocognitive control. Biological Psychology, 89, 260–268. doi:10.1016/j.biopsycho.2011.10.017CrossRefGoogle ScholarPubMed
Chaddock, L., Hillman, C.H., Pontifex, M.B., Johnson, C.R., Raine, L.B., & Kramer, A.F. (2012). Childhood aerobic fitness predicts cognitive performance one year later. Journal of Sport Sciences, 30, 421–430. doi:10.1080/02640414.2011.647706CrossRefGoogle ScholarPubMed
Chaouloff, F. (1989). Physical exercise and brain monoamines: A review. Acta Physiologica Scandinavica, 137, 1–13. doi:10.1111/j.1748-1716.1989.tb08715.xCrossRefGoogle ScholarPubMed
Conklin, H.M., Ogg, R.J., Ashford, J.M., Scoggins, M.A., Zou, P., Clark, K.N., … Zhang, H. (2015). Computerized cognitive training for amelioration of cognitive late effects among childhood cancer survivors: A randomized controlled trial. Journal of Clinical Oncology, 33, 3894–3902. doi:10.1200/JCO.2015.61.6672CrossRefGoogle ScholarPubMed
Conklin, H.M., Reddick, W.E., Ashford, J., Ogg, S., Howard, S.C., Morris, E.B., … Khan, R.B. (2010). Long-term efficacy of methylphenidate in enhancing attention regulation, social skills, and academic abilities of childhood cancer survivors. Journal of Clinical Oncology, 28, 4465–4472. doi:10.1200/JCO.2010.28.4026CrossRefGoogle ScholarPubMed
Conners, C.K. (2004). Conners’ Continuous Performance Test II. San Antonio, TX: Pearson Corporation.Google Scholar
Davis, C.L., Tomporowski, P.D., Boyle, C.A., Waller, J.L., Miller, P.H., Naglieri, J.A., & Gregoski, M.E. (2007). Effects of aerobic exercise on overweight children’s cognitive functioning: A randomized controlled trial. Research Quarterly for Exercise and Sport, 78, 510–519. doi:10.1080/02701367.2007.105999450Google ScholarPubMed
Davis, C.L., Tomporowski, P.D., McDowell, J.E., Austin, B.P., Miller, P.H., Yanasak, N.E., … Naglieri, J.A. (2011). Exercise improves executive function and achievement and alters brain activation in overweight children: A randomized, controlled trial. Health Psychology, 30, 91–98. doi:10.1037/a0021766CrossRefGoogle ScholarPubMed
Delis, D.C., Kaplan, E., & Kramer, J.H. (2001). Delis-Kaplan Executive Function System. San Antonio, TX: Pearson.Google Scholar
Devine, J.M., & Zafonte, D.O. (2009). Physical exercise and cognitive recovery in acquired brain injury: A review of the literature. Physical Medicine and Rehabilitation, 1, 560–575. doi:10.1016/j.pmrj.2009.03.015Google ScholarPubMed
Di Pinto, M., Conklin, H.M., Li, C., & Merchant, T.E. (2012). Learning and memory following conformal radiation therapy for pediatric craniopharyngioma and low-grade glioma. International Journal of Radiation Oncology, Biology, Physics, 84, e363–e369. doi:10.1016/j.ijrobp.2012.03.066CrossRefGoogle ScholarPubMed
Donnelly, J.E., Greene, J.L., Gibson, C.A., Smith, B.K., Washburn, R.A., Sullivan, D.K., … Williams, S.L. (2009). Physical activity across the curriculum (PAAC): A randomized controlled trial to promote physical activity and diminish overweight and obesity in elementary school children. Preventative Medicine, 49, 336–341. doi:10.1016/j.ypmed.2009.07.022CrossRefGoogle ScholarPubMed
Farmer, J., Zhao, X., van Praag, H., Wodtke, K., Gage, F.H., & Christie, B.R. (2004). Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience, 124, 71–79. doi:10.1016/j.neuroscience.2003.09.029CrossRefGoogle ScholarPubMed
Fedewea, A.L., & Ahn, S. (2011). The effects of physical activity and physical fitness on children’s achievement and cognitive outcomes: A meta-analysis. Research Quarterly for Exercise and Sport, 82, 521–535. doi:10.1080/02701367.2011.10599785CrossRefGoogle Scholar
Fjalldal, S., Holmer, H., Rylander, L., Elfving, M., Ekman, B., Osterberg, K., & Erfurth, E.M. (2013). Hypothalamic involvement predicts cognitive performance and psychosocial health in long-term survivors of childhood craniopharyngioma. The Journal of Clinical Endocrinology and Metabolism, 98, 3253–3262. doi:10.1210/jc.2013-2000CrossRefGoogle ScholarPubMed
Fournier-Goodnight, A.S., Ashford, J.M., Merchant, T.E., Boop, R.A., Indelicato, D.J., Wang, L., … Conklin, H.M. (2017). Neurocognitive functioning in pediatric craniopharyngioma: Performance before treatment with proton therapy. Journal of Neuro-oncology, 134, 97–105. doi:10.1007/s11060-017-2492-yCrossRefGoogle ScholarPubMed
Friedland, R.P., Fritsch, T., Smyth, K.A., Koss, E., Lerner, A.J., Chen, C.H., … Debanne, S.M. (2001). Patients with Alzheimer’s disease have reduced activities in midlife compared with healthy control-group members. Proceedings of the National Academy of Sciences of the United States of America, 90, 3440–3445. doi:10.1073/pnas.061002998CrossRefGoogle Scholar
Gioia, G.A., Isquith, P.K., Guy, S.C., & Kenworthy, L. (2000). Behavior Rating Inventory of Executive Function. Odessa, FL: Psychological Assessment Resources, Inc.Google Scholar
Huang, T.T., & Ness, K.K. (2011). Exercise interventions in children with cancer: A review. International Journal of Pediatrics, 2011, 1–11. doi:10.1155/2011/461512CrossRefGoogle ScholarPubMed
Jacola, L.M., Willard, V.M., Ashford, J.M., Ogg, R.J., Scoggins, M.A., Jones, M.M., … Conklin, H.M. (2015). Clinical utility of the n-back task in functional neuroimaging studies of working memory. Journal of Clinical and Experimental Neuropsychology, 36, 875–886. doi:10.1080/13803395.2014.953039CrossRefGoogle Scholar
James, F.W., Kaplan, S., Gluek, C.J., Tsay, J.Y., Knight, M.J., & Sarwar, C.J. (1980). Responses of normal children and young adults to controlled bicycle exercise. Circulation, 61, 902–912.CrossRefGoogle Scholar
Krull, K.R., Hardy, K.K., Kahalley, L.S., Schuitema, I., & Kesler, S.R. (2018). Neurocognitive outcomes and interventions in long-term survivors of childhood cancer. Journal of Clinical Oncology, 36, 2181–2189. doi:10.1200/JCO.2017.76.4696CrossRefGoogle ScholarPubMed
Laurin, D., Verreault, R., Lindsay, J., MacPherson, K., & Rockwood, K. (2001). Physical activity and risk of cognitive impairment and dementia in elderly person. Archives of Neurology, 58, 498–504.CrossRefGoogle Scholar
Mathias, J.L., & Wheaton, P. (2015). Contribution of brain or biological reserve and cognitive or neural reserve to outcome after TBI: A meta-analysis (prior to 2015). Neuroscience and Biobehavioral Reviews, 55, 573–593. doi:10.1016/j.neubiorev.2015.06.001CrossRefGoogle Scholar
Merchant, T.E., Kiehna, E.N., Kun, L.E., Mulhern, R.K., Li, C., Xiong, X., … Sanford, R.A. (2006). Phase II trial of conformal radiation therapy for pediatric patients with craniopharyngioma and correlation of surgical factors and radiation dosimetry with change in cognitive function. Journal of Neurosurgery, 104, 94–102. doi:10.317/ped.2006.104.2.5Google ScholarPubMed
Ming, G.L., & Song, H. (2011). Adult neurogenesis in the mammalian brain: Significant answers and significant questions. Neuron, 70, 687–702. doi:10.1016/j.neuron.2011.05.001CrossRefGoogle ScholarPubMed
Mitby, P.A., Robison, L.L., Whitton, J.A., Zevon, M.A., Gibbs, I.C., Tersak, J.M., … Mertens, A.C. (2003). Utilization of special education services and educational attainment among long-term survivors of childhood cancer: A report from the Childhood Cancer Survivor Study. Cancer, 97, 115–126. doi:10.1002/cncr.11117CrossRefGoogle ScholarPubMed
Mostow, E.N., Byrne, J., Connelly, R.R., & Mulvihill, J.J. (1991). Quality of life in long-term survivors of CNS tumors of childhood and adolescence. Journal of Clinical Oncology, 9, 592–599. doi:10.1200/JCO.1991.9.4.592CrossRefGoogle ScholarPubMed
Mulhern, R.K., & Butler, R.W. (2004). Neurocognitive sequelae of childhood cancers and their treatment. Pediatric Rehabilitation, 1, 1–14. doi:10.1080/13638490310001655528CrossRefGoogle 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. Lancet Oncology, 5, 399–408. doi:10.1016/S1470-2045(04)01507-4CrossRefGoogle ScholarPubMed
Muller, H.L., Gebhardt, U., Teske, C., Faldum, A., Zwiener, I., Warmuth-Metz, M., … Calaminus, G. (2011). Post-operative hypothalamic lesions and obesity in childhood craniopharyngioma: Results of the multinational prospective trial KRANIOPHARYNGEOM 2000 after 3-year follow-up. European Journal of Endocrinology, 134, 97–105. doi:10.1530/EJE-11-0158Google Scholar
Muller, H.L. (2017). Diagnosis, treatment, clinical course, and prognosis of childhood-onset craniopharyngioma patients. Minerva Endocrinology, 42, 356–375. doi:10.23736/S0391-1977.17.02615-3Google ScholarPubMed
Nee, D.E., & Brown, J.W. (2013). Dissociable frontal-striatal and frontal-parietal networks involved in updating hierarchical contexts in working memory. Cerebral Cortex, 13, 2146–2158. doi:10.1093/cercor/bhs194CrossRefGoogle Scholar
Ombrellaro, K.J., Perumal, N., Zeiher, J., Hoebel, J., Ittermann, T., Ewert, R., … Finger, J.D. (2018). Socioeconomic correlates and determinants of cardiorespiratory fitness in the general adult population: As systematic review and meta-analysis. Sports Medicine - Open, 4, 1–19. doi:10.1186/s40798-018-0137-0CrossRefGoogle ScholarPubMed
Ogg, R.J., Zou, P., Allen, D.N., Hutchins, S.B., Dutkiewicz, R.M., & Mulhern, R.K. (2008). Neural correlates of a clinical continuous performance test. Magnetic Resonance Imaging, 26, 504–512. doi:10.1016/j.mri.2007.09.004CrossRefGoogle ScholarPubMed
Ondruch, A., Maryniak, A., Kropiwnicki, T., Roszkowski, M., & Daszkiewicz, P. (2011). Cognitive and social functioning in children and adolescents after the removal of craniopharyngioma. Child’s Nervous System, 27, 391–397. doi:10.1007/s00381-010-1301-0CrossRefGoogle ScholarPubMed
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, 46–59. doi:10.1002/hbm.20131CrossRefGoogle ScholarPubMed
Ozyurt, J., Thiel, C.M., Lorenzen, A., Gebhardt, U., Calaminus, G., Warmuth-Metz, M., & Muller, H.L. (2014). Neuropsychological outcome in patients with childhood craniopharyngioma and hypothalamic involvement. Journal of Pediatrics, 164, 876–881. doi:10.1016/j.peds.2013.12.010CrossRefGoogle ScholarPubMed
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, 2302–2308. doi:10.1200/JC.2001.19.8.2302CrossRefGoogle ScholarPubMed
Piquel, X., Abraham, P., Bouhours-Nouet, N., Gatlais, F., Durfesne, S., Rouleau, S., & Coutant, R. (2012). Impaired aerobic exercise adaptation in children and adolescents with craniopharyngioma is associated with hypothalamic involvement. European Journal of Endocrinology, 166, 215–222.CrossRefGoogle Scholar
Pontifex, M.B., Raine, L.B., Johnson, C.R., Chaddock, L., Voss, M.W., Cohen, N.J., … Hillman, C.H. (2011). Cardiorespiratory fitness and the flexible modulation of cognitive control in preadolescent children. Journal of Cognitive Neuroscience, 23, 1332–1345. doi:10.1162/jocn.2010.21528CrossRefGoogle ScholarPubMed
Poretti, A., Grotzer, M.A., Ribi, K., Schonle, E., & Boltshauser, E. (2004). Outcome of craniopharyngioma in children: Long-term complications and quality of life. Developmental Medicine & Child Neurology, 46, 220–229.CrossRefGoogle ScholarPubMed
Powell, K.E., & Blair, S.N. (1994). The public health burdens of sedentary living habits: theoretical but realistic estimates. Medicine and Science in Sports and Exercise, 26, 851–856.CrossRefGoogle ScholarPubMed
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, 12–19. doi:10.1215/S1152851704000079CrossRefGoogle ScholarPubMed
Riggs, L., Bouffet, E., Laughlin, S., Laperriere, N., Liu, F., Skocic, J., … Mabbott, D.J. (2014). Changes to memory structures in children treated for posterior fossa tumors. Journal of the International Neuropsychological Society, 20, 168–180. doi:10.1017/S135561771300129XCrossRefGoogle ScholarPubMed
Riggs, L., Piscione, J., Laughlin, S., Cunningham, T., Timmons, B.W., Courneya, K.S., … Mabbott, D.J. (2017). Exercise training for neural recovery in a restricted sample of pediatric brain tumor survivors: A controlled clinical trial with crossover of training versus no training. Neuro-oncology, 19, 440–450. doi:10.1093/neuonc/now177Google 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, 3470–3476. doi:10.1200/JCO.2001.19.15.3470CrossRefGoogle 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, 189–200.CrossRefGoogle ScholarPubMed
Ullrich, N.J., & Embry, L. (2012). Neurocognitive dysfunction in survivors of childhood brain tumors. Seminars in Pediatric Neurology, 19, 35–42. doi:10.1016/j.spen.2012.02.014CrossRefGoogle ScholarPubMed
van Praag, H., Christie, B.R., Sejnowski, T.J., & Gage, F.H. (1999). Running enhances neurogenesis, learning, and long-term potentiation in mice. Proceedings of the National Academy of Sciences of the United States of America, 96, 13427–13431CrossRefGoogle ScholarPubMed
Voss, M.W., Chaddock, L., Kim, J.S., Vanpatter, M., Pontifex, M.B., Raine, L.B., … Kramer, F. (2011). Aerobic fitness is associated with greater efficiency of the network underlying cognitive control in preadolescent children. Neuroscience, 199, 166–176. doi:10.1016/j.neuroscience.2011.10.009CrossRefGoogle 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, 13–19. doi:10.1016/j.pediatneurol.2005.06.002CrossRefGoogle ScholarPubMed
Wechsler, D. (2003). Wechsler Intelligence Scale for Children, Fourth Edition. San Antonio, TX: The Psychological Corporation.Google Scholar
Wechsler, D. (2008). Wechsler Adult Intelligence Scale, Fourth Edition. New York, NY: The Psychological Corporation.Google Scholar
Winter, B., Breitenstein, C., Mooren, F.C., Voelker, K., Fobker, M., Lechtermann, A., … Knecht, S. (2007). High impact running improves learning. Neurobiology of Learning and Memory, 87, 597–609. doi:10.1016/j.nlm.2006.11.003CrossRefGoogle ScholarPubMed
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 crania radiation therapy. Pediatric Blood Cancer, 60, 669–675. doi:10.1002/pbc.24331CrossRefGoogle Scholar
Woodcock, R.W., McGrew, K.S., & Mather, N. (2001a). Woodcock-Johnson III Tests of Cognitive Abilities. Itasca, IL: Riverside Publishing.Google Scholar
Woodcock, R.W., McGrew, K.S., & Mather, N. (2001b). Woodcock-Johnson III Tests of Achievement. Itasca, IL, Riverside Publishing.Google Scholar
Yeates, K.O., Levin, H.S., & Ponsford, J. (2017). The neuropsychology of traumatic brain injury: looking back, peering ahead. Journal of the International Neuropsychological Society, 23, 806–817. doi:10.1017/S1355617717000686CrossRefGoogle ScholarPubMed
Yeo, B.T., Krienen, F.M., Sepulcre, J., Sabuncu, M.R., Lashkari, D., Hollinshead, M., … Buckner, R.L. (2011). The organization of the human cerebral cortex estimated by intrinsic functional connectivity. Journal of Neurophysiology, 106, 1125–1165. doi:10.1152/jn.00338.2011Google ScholarPubMed
Zanchi, D., Depoorter, A., Egloff, L., Haller, S., Mahlmann, L., Lag, U.E., … Borgwardt, S. (2017). The impact of gut hormones on the neural circuit of appetite and satiety: A systematic review. Neuroscience and Biobehavioral Reviews, 80, 457–475. doi:10.1016/j.neubiorev.2017.06.013CrossRefGoogle ScholarPubMed
Zou, P., Helton, K.J., Smeltzer, M., Li, C., Conklin, H.M., Gajjar, A., … Ogg, R.J. (2011). Hemodynamic responses to visual stimulation in children with sickle cell anemia. Brain Imaging and Behavior, 5, 295–306. doi:10.1007/s11682-011-9133-4CrossRefGoogle ScholarPubMed