Hostname: page-component-76fb5796d-x4r87 Total loading time: 0 Render date: 2024-04-25T18:54:53.634Z Has data issue: false hasContentIssue false

Childhood maltreatment moderates the effect of combat exposure on cingulum structural integrity

Published online by Cambridge University Press:  22 November 2017

Layla Banihashemi*
Affiliation:
University of Pittsburgh
Meredith L. Wallace
Affiliation:
University of Pittsburgh
Lei K. Sheu
Affiliation:
University of Pittsburgh
Michael C. Lee
Affiliation:
University of Pittsburgh
Peter J. Gianaros
Affiliation:
University of Pittsburgh
Robert P. Mackenzie
Affiliation:
University of Pittsburgh
Salvatore P. Insana
Affiliation:
University of Pittsburgh
Anne Germain
Affiliation:
University of Pittsburgh
Ryan J. Herringa
Affiliation:
University of Pittsburgh University of Wisconsin School of Medicine and Public Health
*
Address correspondence and reprint requests to: Layla Banihashemi, Department of Psychiatry, University of Pittsburgh, 3811 O'Hara Street, Pittsburgh, PA 15213; E-mail: layla.banihashemi@pitt.edu.

Abstract

Limbic white matter pathways link emotion, cognition, and behavior and are potentially malleable to the influences of traumatic events throughout development. However, the impact of interactions between childhood and later life trauma on limbic white matter pathways has yet to be examined. Here, we examined whether childhood maltreatment moderated the effect of combat exposure on diffusion tensor imaging measures within a sample of military veterans (N = 28). We examined five limbic tracts of interest: two components of the cingulum (cingulum, cingulate gyrus, and cingulum hippocampus [CGH]), the uncinate fasciculus, the fornix/stria terminalis, and the anterior limb of the internal capsule. Using effect sizes, clinically meaningful moderator effects were found only within the CGH. Greater combat exposure was associated with decreased CGH fractional anisotropy (overall structural integrity) and increased CGH radial diffusivity (perpendicular water diffusivity) among individuals with more severe childhood maltreatment. Our findings provide preliminary evidence of the moderating effect of childhood maltreatment on the relationship between combat exposure and CGH structural integrity. These differences in CGH structural integrity could have maladaptive implications for emotion and memory, as well as provide a potential mechanism by which childhood maltreatment induces vulnerability to later life trauma exposure.

Type
Special Issue Articles
Copyright
Copyright © Cambridge University Press 2017 

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

The authors thank Benjamin Paul, Ashlee McKeon, Ryan Stocker, and Noelle Rode for their assistance with participant screening, MRI procedures, and data organization. This work was supported by the American Academy of Child & Adolescent Psychiatry (AACAP) Pilot Research Award (to R.J.H.); National Institute of Mental Health Grants MH102406-01 (to L.B.), MH096944 (to M.L.W.), MH080696 and MH083035 (to A.G.), and MH100267 (to R.J.H.); and Department of Defense Congressionally Directed Medical Research Program Grants PT073961 and PR054093 (to A.G.).

References

Adelmann, G., Deller, T., & Frotscher, M. (1996). Organization of identified fiber tracts in the rat fimbria-fornix: An anterograde tracing and electron microscopic study. Anatomy and Embryology, 193, 481493. doi:10.1007/BF00185879 Google Scholar
Adler, A. B., Bliese, P. D., McGurk, D., Hoge, C. W., & Castro, C. A. (2009). Battlemind debriefing and battlemind training as early interventions with soldiers returning from Iraq: Randomization by platoon. Journal of Consulting and Clinical Psychology, 77, 928.Google Scholar
Adler, A. B., Castro, C. A., & McGurk, D. (2009). Time-driven battlemind psychological debriefing: A group-level early intervention in combat. Military Medicine, 174, 21.Google Scholar
Aiken, L. S., West, S. G., & Reno, R. R. (1991). Multiple regression: Testing and interpreting interactions. Thousand Oaks, CA: Sage.Google Scholar
Axer, H., & Keyserlingk, D. G. (2000). Mapping of fiber orientation in human internal capsule by means of polarized light and confocal scanning laser microscopy. Journal of Neuroscience Methods, 94, 165175.Google Scholar
Baker, L. M., Williams, L. M., Korgaonkar, M. S., Cohen, R. A., Heaps, J. M., & Paul, R. H. (2013). Impact of early vs. late childhood early life stress on brain morphometrics. Brain imaging and Behavior, 7, 196203. doi:10.1007/s11682-012-9215-y Google Scholar
Beck, A. T., Steer, R. A., & Carbin, M. G. (1988). Psychometric properties of the Beck Depression Inventory: Twenty-five years of evaluation. Clinical Psychology Review, 8, 77100.Google Scholar
Beckmann, M., Johansen-Berg, H., & Rushworth, M. F. S. (2009). Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. Journal of Neuroscience, 29, 11751190.Google Scholar
Bernstein, D. P., & Fink, L. (1998). Childhood Trauma Questionnaire: A retrospective self-report: Manual. Orlando, FL: Psychological Corporation.Google Scholar
Bernstein, D. P., Fink, L., Handelsman, L., Foote, J., Lovejoy, M., Wenzel, K., … Ruggiero, J. (1994). Initial reliability and validity of a new retrospective measure of child abuse and neglect. American Journal of Psychiatry, 151, 1132.Google Scholar
Berntsein, D., Johannessen, K. B., Thomsen, Y. D., Bertelsen, M., Hoyle, R. H., & Rubin, D. C. (2012). Peace and war: Trajectories of posttraumatic stress disorder symptoms before, during, and after military deployment in Afghanistan. Psychological Science, 23, 15571565.Google Scholar
Bifulco, A., Brown, G. W., & Harris, T. (1994). Childhood Experience of Care and Abuse (CECA): A retrospective interview measure. Journal of Child Psychology and Psychiatry, 35, 14191435.Google Scholar
Bifulco, A., Brown, G., Lillie, A., & Jarvis, J. (1997). Memories of childhood neglect and abuse: Corroboration in a series of sisters. Journal of Child Psychology and Psychiatry, 38, 365374.Google Scholar
Birn, R. M., Patriat, R., Phillips, M. L., Germain, A., & Herringa, R. J. (2014). Childhood maltreatment and combat posttraumatic stress differentially predict fear-related fronto-subcortical connectivity. Depression and Anxiety, 31, 880892. doi:10.1002/da.22291 Google Scholar
Blake, D. D., Weathers, F. W., Nagy, L. M., Kaloupek, D. G., Gusman, F. D., Charney, D. S., & Keane, T. M. (1995). The development of a clinician-administered PTSD scale. Journal of Traumatic Stress, 8, 7590.Google Scholar
Bremner, J. D., Randall, P., Vermetten, E., Staib, L., Bronen, R. A., Mazure, C., … Charney, D. S. (1997). Magnetic resonance imaging-based measurement of hippocampal volume in posttraumatic stress disorder related to childhood physical and sexual abuse—A preliminary report. Biological Psychiatry, 41, 2332.Google Scholar
Briere, J., & Scott, C. (2015). Complex trauma in adolescents and adults: Effects and treatment. Psychiatric Clinics of North America, 38, 515527. doi:10.1016/j.psc.2015.05.004 CrossRefGoogle ScholarPubMed
Cabrera, O. A., Hoge, C. W., Bliese, P. D., Castro, C. A., & Messer, S. C. (2007). Childhood adversity and combat as predictors of depression and post-traumatic stress in deployed troops. American Journal of Preventive Medicine, 33, 7782. doi:10.1016/j.amepre.2007.03.019 Google Scholar
Carrion, V. G., Weems, C. F., Eliez, S., Patwardhan, A., Brown, W., Ray, R. D., & Reiss, A. L. (2001). Attenuation of frontal asymmetry in pediatric posttraumatic stress disorder. Biological Psychiatry, 50, 943951.Google Scholar
Castro, C. A., Adler, A. B., McGurk, D., & Bliese, P. D. (2012). Mental health training with soldiers four months after returning from Iraq: Randomization by platoon. Journal of Traumatic Stress, 25, 376383.Google Scholar
Catani, M., & De Schotten, M. T. (2008). A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex, 44, 11051132.Google Scholar
Catani, M., Dell'Acqua, F., & Thiebaut de Schotten, M. (2013). A revised limbic system model for memory, emotion and behaviour. Neuroscience & Biobehavioral Reviews, 37, 17241737. doi:10.1016/j.neubiorev.2013.07.001 Google 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, 227234. doi:10.1016/j.biopsych.2008.06.022 CrossRefGoogle ScholarPubMed
Cicchetti, D. (2016). Socioemotional, personality, and biological development: Illustrations from a multilevel developmental psychopathology perspective on child maltreatment. Annual Review of Psychology, 67, 187211.Google Scholar
Cohen, J., Cohen, P., West, S. G., & Aiken, L. S. (2003). Applied multiple regression/correlation analysis for the behavioral sciences (3rd ed.). Mahwah, NJ: Erlbaum.Google Scholar
Cragg, B. G., & Hamlyn, L. H. (1959). Histologic connections and electrical and autonomic responses evoked by stimulation of the dorsal fornix in the rabbit. Experimental Neurology, 1, 187213.Google Scholar
Danese, A., Moffitt, T. E., Harrington, H. L., Milne, B. J., Polanczyk, G., Pariante, C. M., … Caspi, A. (2009). Adverse childhood experiences and adult risk factors for age-related disease: Depression, inflammation, and clustering of metabolic risk markers. Archives of Pediatrics and Adolescent Medicine, 163, 1135.Google 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, 286293. doi:10.1016/j.biopsych.2011.10.021 Google Scholar
De Bellis, M. D., Keshavan, M. S., Clark, D. B., Casey, B. J., Giedd, J. N., Boring, A. M., … Ryan, N. D. (1999). Developmental traumatology: Part II. Brain development. Biological Psychiatry, 45, 12711284.Google Scholar
De Olmos, J. S., & Ingram, W. (1972). The projection field of the stria terminalis in the rat brain: An experimental study. Journal of Comparative Neurology, 146, 303333.Google Scholar
Dong, H.-W., Petrovich, G. D., & Swanson, L. W. (2001). Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Research Reviews, 38, 192246.Google Scholar
Eluvathingal, T. J., Chugani, H. T., Behen, M. E., Juhász, C., Muzik, O., Maqbool, M., … Makki, M. (2006). Abnormal brain connectivity in children after early severe socioemotional deprivation: A diffusion tensor imaging study. Pediatrics, 117, 20932100.Google Scholar
Feldman, S., & Conforti, N. (1980). Inhibition of adrenocortical responses following olfactory stimulation in rats with stria terminalis lesions. Neuroscience, 5, 13231329. doi:10.1016/0306-4522(80)90204-3 Google Scholar
Flood, J. F., Merbaum, M. O., & Morley, J. E. (1995). The memory enhancing effects of cholecystokinin octapeptide are dependent on an intact stria terminalis. Neurobiology of Learning and Memory, 64, 139145.Google Scholar
First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. W. (2002). Structured Clinical Interview for DSM-IV-TR Axis I Disorders, research version, patient edition (SCID-I/P). New York: New York State Psychiatric Institute Biometrics Research.Google Scholar
French, L., McCrea, M., & Baggett, M. (2008). The military acute concussion evaluation (MACE). Journal of Special Operations Medicine, 8, 6877.Google Scholar
Gorka, A. X., Hanson, J. L., Radtke, S. R., & Hariri, A. R. (2014). Reduced hippocampal and medial prefrontal gray matter mediate the association between reported childhood maltreatment and trait anxiety in adulthood and predict sensitivity to future life stress. Biology of Mood and Anxiety Disorders, 4, 110. doi:10.1186/2045-5380-4-12 Google Scholar
Hagmann, P., Jonasson, L., Maeder, P., Thiran, J. P., Wedeen, V. J., & Meuli, R. (2006). Understanding diffusion MR imaging techniques: From scalar diffusion-weighted imaging to diffusion tensor imaging and beyond. Radiographics, 26(Suppl. 1), S205S223.Google 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, 15661578.Google Scholar
Hardt, J., & Rutter, M. (2004). Validity of adult retrospective reports of adverse childhood experiences: Review of the evidence. Journal of Child Psychology and Psychiatry, 45, 260273.Google Scholar
Heilbronner, S. R., & Haber, S. N. (2014). Frontal cortical and subcortical projections provide a basis for segmenting the cingulum bundle: Implications for neuroimaging and psychiatric disorders. Journal of Neuroscience, 34, 1004110054.Google Scholar
Herringa, R. J., Phillips, M. L., Fournier, J. C., Kronhaus, D. M., & Germain, A. (2013). Childhood and adult trauma both correlate with dorsal anterior cingulate activation to threat in combat veterans. Psychological Medicine, 43, 15331542.Google Scholar
Hildyard, K. L., & Wolfe, D. A. (2002). Child neglect: Developmental issues and outcomes. Child Abuse & Neglect, 26, 679695. doi:10.1016/S0145-2134(02)00341-1 Google Scholar
Huang, H., Gundapuneedi, T., & Rao, U. (2012). White matter disruptions in adolescents exposed to childhood maltreatment and vulnerability to psychopathology. Neuropsychopharmacology, 37, 26932701.Google Scholar
Johansen-Berg, H., & Behrens, T. E. J. (2009). Diffusion MRI: From quantitative measurement to in-vivo neuroanatomy (1st ed.). New York: Elsevier Science.Google Scholar
Jones, D. K., Christiansen, K. F., Chapman, R. J., & Aggleton, J. P. (2013). Distinct subdivisions of the cingulum bundle revealed by diffusion MRI fibre tracking: Implications for neuropsychological investigations. Neuropsychologia, 51, 6778.Google Scholar
Keane, T. M., Fairbank, J. A., Caddell, J. M., Zimering, R. T., Taylor, K. L., & Mora, C. A. (1989). Clinical evaluation of a measure to assess combat exposure. Journal of Consulting and Clinical Psychology, 1, 53.Google Scholar
Keding, T. J., & Herringa, R. J. (2015). Abnormal structure of fear circuitry in pediatric post-traumatic stress disorder. Neuropsychopharmacology, 40, 537545. doi:10.1038/npp.2014.239 Google Scholar
King, B. M., Rollins, B. L., Grundmann, S. J., & Olivier, L. G. (2003). Excessive weight gains in female rats with transections of the stria terminalis. Physiology & Behavior, 78, 563568. doi:10.1016/S0031-9384(03)00042-8 Google Scholar
Koenen, K. C., Moffitt, T. E., Poulton, R., Martin, J., & Caspi, A. (2007). Early childhood factors associated with the development of post-traumatic stress disorder: Results from a longitudinal birth cohort. Psychological Medicine, 37, 181192. doi:10.1017/S0033291706009019 Google Scholar
Korgaonkar, M. S., Grieve, S. M., Koslow, S. H., Gabrieli, J. D. E., Gordon, E., & Williams, L. M. (2011). Loss of white matter integrity in major depressive disorder: Evidence using tract-based spatial statistical analysis of diffusion tensor imaging. Human Brain Mapping, 32, 21612171.CrossRefGoogle Scholar
Korgaonkar, M. S., Rekshan, W., Gordon, E., Rush, A. J., Williams, L. M., Blasey, C., & Grieve, S. M. (2015). Magnetic resonance imaging measures of brain structure to predict antidepressant treatment outcome in major depressive disorder. EBioMedicine, 2, 3745. doi:10.1016/j.ebiom.2014.12.002 Google Scholar
Kraus, M. F., Susmaras, T., Caughlin, B. P., Walker, C. J., Sweeney, J. A., & Little, D. M. (2007). White matter integrity and cognition in chronic traumatic brain injury: A diffusion tensor imaging study. Brain, 130, 2508.Google Scholar
Kuo, J. R., Kaloupek, D. G., & Woodward, S. H. (2012). Amygdala volume in combat-exposed veterans with and without posttraumatic stress disorder: A cross-sectional study. Archives of General Psychiatry, 69, 10801086. doi:10.1001/archgenpsychiatry.2012.73 Google 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, 340352.Google Scholar
Levine, T. R., & Hullett, C. R. (2002). Eta squared, partial eta squared, and misreporting of effect size in communication research. Human Communication Research, 28, 612625.Google Scholar
Long, Z., Duan, X., Xie, B., Du, H., Li, R., Xu, Q., … Chen, H. (2013). Altered brain structural connectivity in post-traumatic stress disorder: A diffusion tensor imaging tractography study. Journal of Affective Disorders, 150, 798806. doi:10.1016/j.jad.2013.03.004 Google Scholar
Luders, E., Clark, K., Narr, K. L., & Toga, A. W. (2011). Enhanced brain connectivity in long-term meditation practitioners. NeuroImage, 57, 13081316. doi:10.1016/j.neuroimage.2011.05.075 Google Scholar
Lyden, H., Espinoza, R. T., Pirnia, T., Clark, K., Joshi, S. H., Leaver, A. M., … Narr, K. L. (2014). Electroconvulsive therapy mediates neuroplasticity of white matter microstructure in major depression. Translational Psychiatry, 4, e380. doi:10.1038/tp.2014.21 Google Scholar
McLaughlin, K. A., Conron, K. J., Koenen, K. C., & Gilman, S. E. (2010). Childhood adversity, adult stressful life events, and risk of past-year psychiatric disorder: A test of the stress sensitization hypothesis in a population-based sample of adults. Psychological Medicine, 40, 16471658.Google Scholar
Mori, S., Wakana, S., Van Zijl, P. C. M., & Nagae-Poetscher, L. M. (2005). MRI atlas of human white matter. Amsterdam: Elsevier.Google Scholar
Mori, S., & Zhang, J. (2006). Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron, 51, 527539. doi:10.1016/j.neuron.2006.08.012 Google Scholar
Nemeroff, C. B. (2016). Paradise lost: The neurobiological and clinical consequences of child abuse and neglect. Neuron, 89, 892909. doi:10.1016/j.neuron.2016.01.019 Google Scholar
Nieuwenhuys, R., Voogd, J., & van Huijzen, C. (2008). The human central nervous system: A synopsis and atlas (4th ed.). Berlin: Springer.Google Scholar
Osborne, B., Sivakumaran, T., & Black, A. H. (1979). Effects of fornix lesions on adrenocortical responses to changes in environmental stimulation. Behavioral and Neural Biology, 25, 227241. doi:10.1016/S0163-1047(79)90584-3 Google Scholar
Packard, M. G., Hirsh, R., & White, N. M. (1989). Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: Evidence for multiple memory systems. Journal of Neuroscience, 9, 14651472.Google Scholar
Scott, K. M., McLaughlin, K. A., Smith, D. A. R., & Ellis, P. M. (2012). Childhood maltreatment and DSM-IV adult mental disorders: Comparison of prospective and retrospective findings. British Journal of Psychiatry, 200, 469.Google Scholar
Shenton, M. E., Hamoda, H. M., Schneiderman, J. S., Bouix, S., Pasternak, O., Rathi, Y., … Koerte, I. (2012). A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury. Brain Imaging and Behavior, 6, 137192.Google Scholar
Smith, S. M., Johansen-Berg, H., Jenkinson, M., Rueckert, D., Nichols, T. E., Miller, K. L., … Bartsch, A. J. (2007). Acquisition and voxelwise analysis of multi-subject diffusion data with tract-based spatial statistics. Nature Protocols, 2, 499503.Google Scholar
Song, S. K., Sun, S. W., Ramsbottom, M. J., Chang, C., Russell, J., & Cross, A. H. (2002). Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. NeuroImage, 17, 14291436.Google Scholar
Stein, M. B., Koverola, C., Hanna, C., Torchia, M. G., & McClarty, B. (1997). Hippocampal volume in women victimized by childhood sexual abuse. Psychological Medicine, 27, 951959.Google Scholar
Tang, Y.-Y., Holzel, B. K., & Posner, M. I. (2015). The neuroscience of mindfulness meditation. Nature Reviews Neuroscience, 16, 213225. doi:10.1038/nrn3916 Google Scholar
Tang, Y.-Y., Tang, R., & Posner, M. I. (2016). Mindfulness meditation improves emotion regulation and reduces drug abuse. Drug and Alcohol Dependence, 163(Suppl. 1), S13S18. doi:10.1016/j.drugalcdep.2015.11.041 Google Scholar
Teicher, M. H., & Samson, J. A. (2016). Annual Research Review: Enduring neurobiological effects of childhood abuse and neglect. Journal of Child Psychology and Psychiatry, 57, 241266. doi:10.1111/jcpp.12507 Google Scholar
Ugwu, I. D., Amico, F., Carballedo, A., Fagan, A. J., & Frodl, T. (2015). Childhood adversity, depression, age and gender effects on white matter microstructure: A DTI study. Brain Structure and Function, 220, 19972009.CrossRefGoogle ScholarPubMed
Vogt, B. A. (2005). Pain and emotion interactions in subregions of the cingulate gyrus. Nature Reviews Neuroscience, 6, 533544.Google Scholar
Von Der Heide, R. J., Skipper, L. M., Klobusicky, E., & Olson, I. R. (2013). Dissecting the uncinate fasciculus: Disorders, controversies and a hypothesis. Brain, 136, 16921707.Google Scholar
Wasserstein, R. L., & Lazar, N. A. (2016). The ASA's statement on p-values: Context, process, and purpose. American Statistician. Advance online publication.Google Scholar
Weathers, F. W., Keane, T. M., & Davidson, J. R. T. (2001). Clinician-Administered PTSD Scale: A review of the first ten years of research. Depression and Anxiety, 13, 132156.Google Scholar
Woodward, S. H., Kuo, J. R., Schaer, M., Kaloupek, D. G., & Eliez, S. (2013). Early adversity and combat exposure interact to influence anterior cingulate cortex volume in combat veterans. NeuroImage, 2, 670674. doi:10.1016/j.nicl.2013.04.016 Google Scholar