Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-22T18:46:10.108Z Has data issue: false hasContentIssue false
  • English
  • Français

Early life stress, cortisol, frontolimbic connectivity, and depressive symptoms during puberty

Published online by Cambridge University Press:  08 May 2019

Katharina Kircanski ,
Lucinda M. Sisk ,
Tiffany C. Ho ,
Kathryn L. Humphreys ,
Lucy S. King ,
Natalie L. Colich ,
Sarah J. Ordaz  and
Ian H. Gotlib
Katharina Kircanski*
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Lucinda M. Sisk
Affiliation:
Department of Psychology, Stanford University, Stanford, CA, USA
Tiffany C. Ho
Affiliation:
Department of Psychology, Stanford University, Stanford, CA, USA
Kathryn L. Humphreys
Affiliation:
Department of Psychology and Human Development, Vanderbilt University, Nashville, TN, USA
Lucy S. King
Affiliation:
Department of Psychology, Stanford University, Stanford, CA, USA
Natalie L. Colich
Affiliation:
Department of Psychology, University of Washington, Seattle, WA, USA
Sarah J. Ordaz
Affiliation:
Department of Psychology, Stanford University, Stanford, CA, USA
Ian H. Gotlib
Affiliation:
Department of Psychology, Stanford University, Stanford, CA, USA
*
Author for correspondence: Katharina Kircanski, Emotion and Development Branch, National Institute of Mental Health, 9000 Rockville Pike, Building 15K, MSC-2670, Bethesda, MD 20892-2670; E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

Early life stress (ELS) is a risk factor for the development of depression in adolescence; the mediating neurobiological mechanisms, however, are unknown. In this study, we examined in early pubertal youth the associations among ELS, cortisol stress responsivity, and white matter microstructure of the uncinate fasciculus and the fornix, two key frontolimbic tracts; we also tested whether and how these variables predicted depressive symptoms in later puberty. A total of 208 participants (117 females; M age = 11.37 years; M Tanner stage = 2.03) provided data across two or more assessment modalities: ELS; salivary cortisol levels during a psychosocial stress task; diffusion magnetic resonance imaging; and depressive symptoms. In early puberty there were significant associations between higher ELS and decreased cortisol production, and between decreased cortisol production and increased fractional anisotropy in the uncinate fasciculus. Further, increased fractional anisotropy in the uncinate fasciculus predicted higher depressive symptoms in later puberty, above and beyond earlier symptoms. In post hoc analyses, we found that sex moderated several additional associations. We discuss these findings within a broader conceptual model linking ELS, emotion dysregulation, and depression across the transition through puberty, and contend that brain circuits implicated in the control of hypothalamic–pituitary–adrenal axis function should be a focus of continued research.

Keywords

cortisoldepressiondiffusion tensor imagingemotion dysregulationearly life stresspuberty
Type
Special Issue Articles
Information
Development and Psychopathology , Volume 31 , Special Issue 3: Emotion Dysregulation and Emerging Psychopathology , August 2019 , pp. 1011 - 1022
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Authors Katharina Kircanski and Lucinda M. Sisk contributed equally to the article.

References

Adrian, M., Zeman, J., & Veits, G. (2011). Methodological implications of the affect revolution: A 35-year review of emotion regulation assessment in children. Journal of Experimental Child Psychology, 110, 171–197. doi:10.1016/j.jecp.2011.03.009Google Scholar
Aghajani, M., Veer, I. M., Van Lang, N. D. J., Meens, P. H. F., Van Den Bulk, B. G., Rombouts, S. A. R. B., … Van Der Wee, N. J. (2014). Altered white-matter architecture in treatment-naive adolescents with clinical depression. Psychological Medicine, 44, 2287–2298. doi:10.1017/S0033291713003000Google Scholar
Alink, L. R. A., Cicchetti, D., Kim, J., & Rogosch, F. A. (2012). Longitudinal associations among child maltreatment, social functioning, and cortisol regulation. Developmental Psychology, 48, 224–236. doi:10.1037/a0024892Google Scholar
Basser, P. J., Pajevic, S., Pierpaoli, C., Duda, J., & Aldroubi, A. (2000). In vivo fiber tractography using DT-MRI data. Magnetic Resonance in Medicine, 141, C4014005. doi:10.1061/(ASCE)EI.1943-5541.0000225Google Scholar
Beauchaine, T. P. (2015). Future directions in emotion dysregulation and youth psychopathology. Journal of Clinical Child and Adolescent Psychology, 44, 875–896. doi:10.1080/15374416.2015.1038827Google Scholar
Beauchaine, T. P., & Gatzke-Kopp, L. M. (2012). Instantiating the multiple levels of analysis perspective in a program of study on externalizing behavior. Development and Psychopathology, 24, 1003–1018. doi:10.1017/S0954579412000508Google Scholar
Bracht, T., Linden, D., & Keedwell, P. (2015). A review of white matter microstructure alterations of pathways of the reward circuit in depression. Journal of Affective Disorders, 187, 45–53. doi:10.1016/j.jad.2015.06.041Google Scholar
Bunea, I. M., Szentágotai-Tǎtar, A., & Miu, A. C. (2017). Early-life adversity and cortisol response to social stress: A meta-analysis. Translational Psychiatry, 7, 1274. doi:10.1038/s41398-017-0032-3Google Scholar
Burke, H. M., Davis, M. C., Otte, C., & Mohr, D. C. (2005). Depression and cortisol responses to psychological stress: A meta-analysis. Psychoneuroendocrinology, 30, 846–856. doi:10.1016/j.psyneuen.2005.02.010Google Scholar
Callaghan, B. L., & Tottenham, N. (2016). The stress acceleration hypothesis: Effects of early-life adversity on emotion circuits and behavior. Current Opinion in Behavioral Sciences, 7, 76–81. doi:10.1016/j.cobeha.2015.11.018Google Scholar
Choi, J., Jeong, B., Rohan, M. L., Polcari, A. M., & Teicher, M. H. (2009). Preliminary evidence for white matter tract abnormalities in young adults exposed to parental verbal abuse. Biological Psychiatry, 65, 227–234. doi:10.1016/j.biopsych.2008.06.022Google Scholar
Cicchetti, D., Rogosch, F. A., Gunnar, M. R., & Toth, S. L. (2010). The differential impacts of early physical and sexual abuse and internalizing problems on daytime cortisol rhythm in school-aged children. Child Development, 81, 252–269. doi:10.1111/j.1467-8624.2009.01393.xGoogle Scholar
Coleman, L., & Coleman, J. (2002). The measurement of puberty: A review. Journal of Adolescence, 25, 535–550. doi:10.1207/S15327949PAC0804_03Google Scholar
Colich, N. L., Kircanski, K., Foland-Ross, L. C., & Gotlib, I. H. (2015). HPA-axis reactivity interacts with stage of pubertal development to predict the onset of depression. Psychoneuroendocrinology, 55, 94–101.Google Scholar
Colich, N. L., Williams, E. S., Ho, T. C., King, L. S., Humphreys, K. L., Price, A. N., Ordaz, S. J., & Gotlib, I. H. (2017). The association between early life stress and prefrontal cortex activation during implicit emotion regulation is moderated by sex in early adolescence. Development and Psychopathology, 29, 1851–1864.Google Scholar
Conturo, T. E., Lori, N. F., Cull, T. S., Akbudak, E., Snyder, A. Z., Shimony, J. S., … Raichle, M. E. (1999). Tracking neuronal fiber pathways in the living human brain. Applied Physical Sciences: Neurobiology, 96, 10422–10427. doi:10.1073/pnas.96.18.10422Google Scholar
Dahl, R. E. (2001). Affect regulation, brain development, and behavioral/emotional health in adolescence. CNS Spectrums, 6, 60–72. doi:10.1017/S1092852900022884Google Scholar
Dannlowski, U., Stuhrmann, A., Beutelmann, V., Zwanzger, P., Lenzen, T., Grotegerd, D., … Kugel, H. (2012). Limbic scars: Long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging. Biological Psychiatry, 71, 286–293. doi:10.1016/j.biopsych.2011.10.021Google Scholar
DePasquale, C. E., Donzella, B., & Gunnar, M. R. (in press). Pubertal recalibration of cortisol reactivity following early life stress: A cross-sectional analysis. Journal of Child Psychology and Psychiatry. doi:10.1111/jcpp.12992Google Scholar
Desmangles, J. C., Lappe, J. M., Lipaczewski, G., & Haynatzki, G. (2006). Accuracy of pubertal Tanner staging self-reporting. Journal of Pediatric Endocrinology and Metabolism, 19, 213–222. doi:10.1515/JPEM.2006.19.3.213Google Scholar
Destrieux, C., Fischl, B., Dale, A., & Halgren, E. (2010). Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. NeuroImage, 53, 1–15. doi:10.1016/j.neuroimage.2010.06.010Google Scholar
Doom, J. R., & Gunnar, M. R. (2013). Stress physiology and developmental psychopathology: Past, present and future. Development and Psychopathology, 25, 1359–1373. doi:10.1017/S0954579413000667Google Scholar
Eluvathingal, T. J. (2006). Abnormal brain connectivity in children after early severe socioemotional deprivation: A diffusion tensor imaging study. Pediatrics, 117, 2093–2100. doi:10.1542/peds.2005-1727Google Scholar
Fischl, B., Salat, D. H., Van Der Kouwe, A. J. W., Makris, N., Ségonne, F., Quinn, B. T., & Dale, A. M. (2004). Sequence-independent segmentation of magnetic resonance images. NeuroImage, 23, 69–84. doi:10.1016/j.neuroimage.2004.07.016Google Scholar
Fries, E., Hesse, J., Hellhammer, J., & Hellhammer, D. H. (2005). A new view on hypocortisolism. Psychoneuroendocrinology, 30, 1010–1016. doi:10.1016/j.psyneuen.2005.04.006Google Scholar
Fuhrmann, D., Knoll, L. J., & Blakemore, S. J. (2015). Adolescence as a sensitive period of brain development. Trends in Cognitive Sciences, 19, 558–566. doi:10.1016/j.tics.2015.07.008Google Scholar
Green, J. G., Mclaughlin, K. A., Berglund, P. A., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., & Kessler, R. C. (2010). Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I. American Medical Association, 67, 113–123. doi:10.1001/archgenpsychiatry.2009.186Google Scholar
Haber, S. N., & Knutson, B. (2010). The reward circuit: Linking primate anatomy and human imaging. Neuropsychopharmacology, 35, 4–26. doi:10.1038/npp.2009.129Google Scholar
Hanson, J. L., Adluru, N., Chung, M. K., Alexander, A. L., Davidson, R. J., & Pollak, S. D. (2013). Early neglect is associated with alterations in white matter integrity and cognitive functioning. Child Development, 84, 1566–1578. doi:10.1111/cdev.12069Google Scholar
Hanson, J. L., Knodt, A. R., Brigidi, B. D., & Hariri, A. R. (2015). Lower structural integrity of the uncinate fasciculus is associated with a history of child maltreatment and future psychological vulnerability to stress. Development and Psychopathology, 27, 1611–1619. doi:10.1017/S0954579415000978Google Scholar
Hanson, J. L., Nacewicz, B. M., Sutterer, M. J., Cayo, A. A., Schaefer, S. M., Rudolph, K. D., … Davidson, R. J. (2015). Behavioral problems after early life stress: Contributions of the hippocampus and amygdala. Biological Psychiatry, 77, 314–323. doi:10.1016/j.biopsych.2014.04.020Google Scholar
Harkness, K. L., Stewart, J. G., & Wynne-Edwards, K. E. (2011). Cortisol reactivity to social stress in adolescents: Role of depression severity and child maltreatment. Psychoneuroendocrinology, 36, 173–181. doi:10.1016/j.psyneuen.2010.07.006Google Scholar
Ho, T. C., King, L. S., Leong, J. K., Colich, N. L., Humphreys, K. L., Ordaz, S. J., & Gotlib, I. H. (2017). Effects of sensitivity to life stress on uncinate fasciculus segments in early adolescence. Social Cognitive and Affective Neuroscience, 12, 1460–1469. doi:10.1093/scan/nsx065Google Scholar
Hua, K., Zhang, J., Wakana, S., Jiang, H., Li, X., Reich, D. S., … Mori, S. (2008). Tract probability maps in stereotaxic spaces: Analyses of white matter anatomy and tract-specific quantification. NeuroImage, 39, 336–347. doi:10.1371/journal.pone.0128887Google Scholar
Huang, H., Gundapuneedi, T., & Rao, U. (2012). White matter disruptions in adolescents exposed to childhood maltreatment and vulnerability to psychopathology. Neuropsychopharmacology, 37, 2693–2701. doi:10.1038/npp.2012.133Google Scholar
Kessler, R. C. (2003). Epidemiology of women and depression. Journal of Affective Disorders, 74, 5–13. doi:10.1016/S0165-0327(02)00426-3Google Scholar
King, L. S., Colich, N. L., LeMoult, J., Humphreys, K. L., Ordaz, S. J., Price, A. N., & Gotlib, I. H. (2017). The impact of the severity of early life stress on diurnal cortisol: The role of puberty. Psychoneuroendocrinology, 77, 68–74. doi:10.1016/j.psyneuen.2016.11.024Google Scholar
Kirschbaum, C., Pirke, K.-M., & Hellhammer, D. H. (1993). The Trier Social Stress Test—A tool for investigating psychobiological stress responses in a laboratory setting. Neuropychobiology, 28, 76–81.Google Scholar
Koss, K. J., & Gunnar, M. R. (2018). Annual Research Review: Early adversity, the hypothalamic-pituitary-adrenocortical axis, and child psychopathology. Journal of Child Psychology and Psychiatry and Allied Disciplines, 4, 327–346. doi:10.1111/jcpp.12784Google Scholar
Kovacs, M. (1985). The Children's Depression Inventory (CDI). Psychopharmocological Bulletin, 21, 995–998.Google Scholar
Kovacs, M. (1992). The Children's Depression Inventory (CDI). Toronto, ON: Multi-Health Systems.Google Scholar
Kwong, A. S., Manley, D., Timpson, N. J., Pearson, R. M., Heron, J., Sallis, H., … Leckie, G. (in press). Identifying critical points of trajectories of depressive symptoms from childhood to young adulthood. Journal of Youth and Adolescence. doi:10.1007/s10964-018-0976-5Google Scholar
Lebel, C., Gee, M., Camicioli, R., Wieler, M., Martin, W., & Beaulieu, C. (2012). Diffusion tensor imaging of white matter tract evolution over the lifespan. NeuroImage, 60, 340–352. doi:10.1016/j.neuroimage.2011.11.094Google Scholar
Leong, J. K., MacNiven, K. H., Samanez-Larkin, G. R., & Knutson, B. (2018). Distinct neural circuits support incentivized inhibition. NeuroImage, 178, 435–444. doi:10.1016/j.neuroimage.2018.05.055Google Scholar
Leong, J., Pestilli, F., Wu, C., Samanez-Larkin, G., & Knutson, B. (2016). White-matter tract connecting anterior insula to nucleus accumbens correlates with reduced preference for positively skewed gambles. Neuron, 89, 63–69. doi:10.1161/CIRCULATIONAHA.114.010270.Google Scholar
Lewinn, K. Z., Connolly, C. G., Wu, J., Drahos, M., Hoeft, F., Ho, T. C., … Yang, T. T. (2014). White matter correlates of adolescent depression: Structural evidence for frontolimbic disconnectivity. Journal of the American Academy of Child & Adolescent Psychiatry, 53, 899–909. doi:10.1016/j.jaac.2014.04.021Google Scholar
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. M. (2009). Effects of stress throughout the lifespan on the brain and behavior. In Pfaff, D. W. (Ed.), Hormones, brain and behavior (3rd ed., pp. 434–445). San Diego, CA: Academic Press.Google Scholar
Marshall, W. A., & Tanner, J. M. (1968). Growth and physiological development during adolescence. Annual Review of Medicine, 19, 283–300.Google Scholar
McEwen, B. S. (1998). Stress, adaptation, and disease: Allostasis and allostatic load. Annals of the New York Academy of Sciences, 840, 33–44.Google Scholar
McEwen, B. S. (2004). Protection and damage from acute and chronic stress. Annals of the New York Academy of Sciences, 1032, 1–7.Google Scholar
McEwen, B. S., & Milner, T. (2007). Hippocampal formation: Shedding light on the influence of sex and stress on the brain. Brain Research Review, 55, 343–355.Google Scholar
McLaughlin, K. A., Green, J. G., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., & Kessler, R. C. (2012). Childhood adversities and first onset of psychiatric disorders in a national sample of US adolescents. Archives of General Psychiatry, 69, 1151–1160. doi:10.1001/archgenpsychiatry.2011.2277Google Scholar
Messman-Moore, T. L., & Bhuptani, P. H. (2017). A review of the long-term impact of child maltreatment on posttraumatic stress disorder and its comorbidities: An emotion dysregulation perspective. Clinical Psychology Science and Practice, 24, 154–169. doi:10.1111/cpsp.12193Google Scholar
Morris, M. C., Kouros, C. D., Mielock, A. S., & Rao, U. (2017). Depressive symptom composites associated with cortisol stress reactivity in adolescents. Journal of Affective Disorders, 210, 181–188. doi:10.1016/j.jad.2016.12.023Google Scholar
Negriff, S., & Susman, E. J. (2011). Pubertal timing, depression, and externalizing problems: A framework, review, and examination of gender differences. Journal of Research on Adolescence, 21, 717–746. doi:10.1111/j.1532-7795.2010.00708.xGoogle Scholar
Olson, I. R., Von der Heide, R. J., Alm, K. H., & Vyas, G. (2015). Development of the uncinate fasciculus: Implications for theory and developmental disorders. Developmental Cognitive Neuroscience, 14, 50–61. doi:10.1016/j.dcn.2015.06.003Google Scholar
O'Mahen, H. A., Karl, A., Moberly, N., & Fedock, G. (2015). The association between childhood maltreatment and emotion regulation: Two different mechanisms contributing to depression? Journal of Affective Disorders, 174, 287–295. doi:10.1016/j.jad.2014.11.028Google Scholar
Ordaz, S. J., & Luna, B. (2012). Sex differences in physiological reactivity to acute psychosocial stress in adolescence. Psychoneuroendocrinology, 37, 1135–1157. doi:10.1016/j.psyneuen.2012.01.002Google Scholar
Palacios-Barrios, E. E., & Hanson, J. (2019). Poverty and self-regulation: Integrating psychosocial processes and neurobiology to understand risk for psychopathology. Comprehensive Psychiatry, 90, 52–64. doi:10.1016/j.comppsych.2018.12.012Google Scholar
Powell, D. J., & Schlotz, W. (2012). Daily life stress and the cortisol awakening response: testing the anticipation hypothesis. PLOS ONE, 7. doi:10.1371/journal.pone.0052067Google Scholar
Pruessner, J. C., Kirschbaum, C., Meinlschmid, G., & Hellhammer, D. H. (2003). Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology, 28, 916–931. doi:10.1016/S0306-4530(02)00108-7Google Scholar
Quevedo, K., Johnson, A., Loman, M., Lafavor, T., & Gunnar, M. (2012). The confluence of adverse early experience and puberty on the cortisol awakening response. International Journal of Behavioral Development, 36, 19–28. doi:10.1177/0165025411406860Google Scholar
Rao, U., Hammen, C., Ortiz, L. R., Chen, L. A., & Poland, R. E. (2008). Effects of early and recent adverse experiences on adrenal response to psychosocial stress in depressed adolescents. Biological Psychiatry, 64, 521–526. doi:10.1016/j.biopsych.2008.05.012Google Scholar
Raymond, C., Marin, M. F., Majeur, D., & Lupien, S. (2018). Early child adversity and psychopathology in adulthood: HPA axis and cognitive dysregulations as potential mechanisms. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 85, 152–160. doi:10.1016/j.pnpbp.2017.07.015Google Scholar
R Core Team. (2017). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.orgGoogle Scholar
Ribbe, D. (1996). Psychometric review of Traumatic Event Screening Instrument for Children (TESI-C). In Stamm, B. H. (Ed.), Measurement of stress, trauma, and adaptation (pp. 386–387). Lutherville, MD: Sidran Press.Google Scholar
Rohde, G. K., Barnett, A. S., Basser, P. J., Marenco, S., & Pierpaoli, C. (2004). Comprehensive approach for correction of motion and distortion in diffusion-weighted MRI. Magnetic Resonance in Medicine, 51, 103–114. doi:10.1002/mrm.10677Google Scholar
Romeo, R. D. (2010). Adolescence: A central event in shaping stress reactivity. Developmental Psychobiology, 52, 244–253. doi:10.1002/dev.20437Google Scholar
Romeo, R. D., & McEwen, B. S. (2006). Stress and the adolescent brain. Annals of the New York Academy of Sciences, 1094, 202–214. doi:10.1196/annals.1376.022Google Scholar
Rudolph, K. D., Hammen, C., Burge, D., Lindberg, N., Herzberg, D., & Daley, S. E. (2000). Toward an interpersonal life-stress model of depression: The developmental context of stress generation. Development and Psychopathology, 12, 215–234Google Scholar
Sheikh, H. I., Joanisse, M. F., Mackrell, S. M., Kryski, K. R., Smith, H. J., Singh, S. M., & Hayden, E. P. (2014). Links between white matter microstructure and cortisol reactivity to stress in early childhood: Evidence for moderation by parenting. NeuroImage: Clinical, 6, 77–85. doi:10.1016/j.nicl.2014.08.013Google Scholar
Shirtcliff, E. A., Dahl, R. E., & Pollak, S. D. (2009). Pubertal development: Correspondence between hormonal and physical development. Child Development, 80, 327–337. doi:10.1111/j.1467-8624.2009.01263.x.PubertalGoogle Scholar
Simmonds, D. J., Hallquist, M. N., Asato, M., & Luna, B. (2014). Developmental stages and sex differences of white matter and behavioral development through adolescence: A longitudinal diffusion tensor imaging (DTI) study. Neuroimage, 92, 356–368. doi:10.1038/jid.2014.371Google Scholar
Stalder, T., Kirschbaum, C., Kudielka, B. M., Adam, E. K., Pruessner, J. C., Wüst, S., … Clow, A. (2016). Assessment of the cortisol awakening response: Expert consensus guidelines. Psychoneuroendocrinology, 63, 414–432. doi:10.1016/j.psyneuen.2015.10.010Google Scholar
Teicher, M. H., Samson, J. A., Anderson, C. M., & Ohashi, K. (2016). The effects of childhood maltreatment on brain structure, function and connectivity. Nature Reviews Neuroscience, 17, 652–666. doi:10.1038/nrn.2016.111Google Scholar
Teicher, M. H., Tomoda, A., & Andersen, S. E. (2006). Neurobiological consequences of early stress and childhood maltreatment: Are results from human and animal studies comparable? Annals of the New York Academy of Sciences, 1071, 313–323. doi:10.1196/annals.1364.024Google Scholar
Tournier, J. D., Calamante, F., & Connelly, A. (2007). Robust determination of the fibre orientation distribution in diffusion MRI: Non-negativity constrained super-resolved spherical deconvolution. NeuroImage, 35, 1459–1472. doi:10.1016/j.neuroimage.2007.02.016Google Scholar
Trickett, P. K., Gordis, E., Peckins, M. K., & Susman, E. J. (2014). Stress reactivity in maltreated and comparison male and female young adolescents. Child Maltreatment, 19, 27–37. doi:10.1177/1077559513520466Google Scholar
Ursache, A., Noble, K., & Blair, C. (2015). Socioeconomic status, subjective social status, and perceived stress: Associations with stress physiology and executive functioning. Journal of Behavioral Medicine, 41, 145–154. doi:10.1161/CIRCULATIONAHA.114.010270.HospitalGoogle Scholar
Wakana, S., Jiang, H., & van Zijl, P. C. M. (2004). Fiber tract–based atlas of human white matter anatomy. Radiology, 230, 77–87. doi:10.1148/radiol.2301021640Google Scholar
Yeatman, J. D., Dougherty, R. F., Myall, N. J., Wandell, B. A., & Feldman, H. M. (2012). Tract profiles of white matter properties: Automating fiber-tract quantification. PLOS ONE, 7. doi:10.1371/journal.pone.0049790Google Scholar
Zhang, W., Olivi, A., Hertig, S. J., van Zijl, P., & Mori, S. (2008). Automated fiber tracking of human brain white matter using diffusion tensor imaging. NeuroImage, 42, 771–777. doi:10.1016/j.neuroimage.2008.04.241Google Scholar