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Cortical thickness and sulcal depth: insights on development and psychopathology in paediatric epilepsy

Published online by Cambridge University Press:  02 January 2018

Duygu Tosun*
Affiliation:
Department of Radiology and Biomedical Imaging, University of California – San Francisco, California, and Center for Imaging of Neurodegenerative Diseases, San Francisco Veterans Affairs Medical Center, San Francisco, California, USA
Prabha Siddarth
Affiliation:
Department of Psychiatry, Semel Institute for Neuroscience and Human Behavior, UCLA David Geffen School of Medicine, Los Angeles, California, USA
Jennifer Levitt
Affiliation:
Department of Psychiatry, Semel Institute for Neuroscience and Human Behavior, UCLA David Geffen School of Medicine, Los Angeles, California, USA
Rochelle Caplan
Affiliation:
Department of Psychiatry, Semel Institute for Neuroscience and Human Behavior, UCLA David Geffen School of Medicine, Los Angeles, California, USA
*
Duygu Tosun, Centre for Imaging of Neurodegenerative Diseases, VA Medical Center, Bldg 13, 114M, San Francisco, CA 94121, USA. Email: duygu.tosun@ucsf.edu
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Abstract

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Background

The relationship between cortical thickness (CThick) and sulcal depth (SDepth) changes across brain regions during development. Epilepsy youth have CThick and SDepth abnormalities and prevalent psychiatric disorders.

Aims

This study compared the CThick–SDepth relationship in children with focal epilepsy with typically developing children (TDC) and the role played by seizure and psychopathology variables.

Method

A surface-based, computational high-resolution three-dimesional (3D) magnetic resonance image analytic technique compared regional CThick–SDepth relationships in 42 participants with focal epilepsy and 46 TDC (6–16 years) imaged in a 1.5 Tesla scanner. Psychiatric interviews administered to each participant yielded psychiatric diagnoses. Parents provided seizure-related information.

Results

The TDC group alone demonstrated a significant negative medial fronto-orbital CThick–SDepth correlation. Focal epilepsy participants with but not without psychiatric diagnoses showed significant positive pre-central and post-central CThick–SDepth associations not found in TDC. Although the history of prolonged seizures was significantly associated with the postcentral CThick–SDepth correlation, it was unrelated to the presence/absence of psychiatric diagnoses.

Conclusions

Abnormal CThick–SDepth pre-central and post-central associations might be a psychopathology biomarker in paediatric focal epilepsy.

Type
Research Article
Creative Commons
Creative Common License - CCCreative Common License - BYCreative Common License - NCCreative Common License - ND
This is an open access article distributed under the terms of the Creative Commons Non-Commercial, No Derivatives (CC BY-NC-ND) licence (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Copyright
Copyright © The Royal College of Psychiatrists 2015

Footnotes

Declaration of interest

None.

References

1 Raznahan, A, Shaw, P, Lalonde, F, Stockman, M, Wallace, GL, Greenstein, D, et al. How does your cortex grow? J Neurosci 2011; 31: 7174–7.CrossRefGoogle ScholarPubMed
2 Shaw, P, Kabani, NJ, Lerch, JP, Eckstrand, K, Lenroot, R, Gogtay, N, et al. Neurodevelopmental trajectories of the human cerebral cortex. J Neurosci 2008; 28: 3586–94.CrossRefGoogle ScholarPubMed
3 Alemán-Gómez, Y, Janssen, J, Schnack, H, Balaban, E, Pina-Camacho, L, Alfaro-Almagro, F, et al. The human cerebral cortex flattens during adolescence. J Neurosci 2013; 33: 15004–10.CrossRefGoogle ScholarPubMed
4 Vandekar, SN, Shinohara, RT, Raznahan, A, Roalf, DR, Ross, M, DeLeo, N, et al. Topologically dissociable patterns of development of the human cerebral cortex. J Neurosci 2015; 35: 599609.CrossRefGoogle ScholarPubMed
5 Tosun, D, Caplan, R, Siddarth, P, Seidenberg, M, Gurbani, S, Toga, AW, et al. Intelligence and cortical thickness in children with complex partial seizures. Neuroimage 2011; 15: 337–46.Google Scholar
6 Tosun, D, Siddarth, P, Toga, AW, Hermann, B, Caplan, R. Effects of childhood absence epilepsy on associations between regional cortical morphometry and aging and cognitive abilities. Hum Brain Mapp 2010; 32: 580–91.Google Scholar
7 Lin, JJ, Dabbs, K, Riley, JD, Jones, JE, Jackson, DC, Hsu, DA, et al. Neurodevelopment in new-onset juvenile myoclonic epilepsy over the first 2 years. Ann Neurol 2014; 76: 660–8.CrossRefGoogle ScholarPubMed
8 Widjaja, E, Mahmoodabadi, SZ, Snead, OC, Almehdar, A, Smith, ML. Widespread cortical thinning in children with frontal lobe epilepsy. Epilepsia 2011; 52: 1685–91.CrossRefGoogle ScholarPubMed
9 Duerden, EG, Tannock, R, Dockstader, C. Altered cortical morphology in sensorimotor processing regions in adolescents and adults with attention-deficit/hyperactivity disorder. Brain Res 2012; 1445:8291.CrossRefGoogle ScholarPubMed
10 Reynolds, S, Carrey, N, Jaworska, N, Langevin, LM, Yang, XR, Macmaster, FP. Cortical thickness in youth with major depressive disorder. BMC Psychiatry 2014; 14: 83.CrossRefGoogle ScholarPubMed
11 Strawn, JR, Wegman, CJ, Dominick, KC, Swartz, MS, Wehry, AM, Patino, LR, et al. Cortical surface anatomy in pediatric patients with generalized anxiety disorder. J Anxiety Disord 2014; 28: 717–23.CrossRefGoogle ScholarPubMed
12 Ducharme, S, Hudziak, JJ, Botteron, KN, Albaugh, MD, Nguyen, TV, Karama, S, et al. Decreased regional cortical thickness and thinning rate are associated with inattention symptoms in healthy children. J Am Acad Child Adolesc Psychiatry 2012; 51: 18–27.e2.CrossRefGoogle ScholarPubMed
13 Ducharme, S, Albaugh, MD, Hudziak, JJ, Botteron, KN, Nguyen, TV, Truong, C, et al. Anxious/depressed symptoms are linked to right ventromedial prefrontal cortical thickness maturation in healthy children and young adults. Cereb Cortex 2014; 24: 2941–50.CrossRefGoogle ScholarPubMed
14 Levan, A, Baxter, L, Kirwan, CB, Black, G, Gale, SD. Right frontal pole cortical thickness and social competence in children with chronic traumatic brain injury: Cognitive proficiency as a mediator. J Head Trauma Rehabil 2015; 30: E2431.CrossRefGoogle ScholarPubMed
15 Hesdorffer, DC, Lúdvígsson, P, Hauser, WA, Olafsson, E, Kjartansson, O. Cooccurrence of major depression or suicide attempt with migraine with aura and risk for unprovoked seizure. Epilepsy Res 2007; 75: 220–3.CrossRefGoogle ScholarPubMed
16 Hesdorffer, DC, Ludvigsson, P, Olafsson, E, Gudmundsson, G, Kjartansson, O, Hauser, WA. ADHD as a risk factor for incident unprovoked seizures and epilepsy in children. Arch Gen Psychiatry 2004; 61: 731–6.CrossRefGoogle ScholarPubMed
17 Austin, JK, Perkins, SM, Johnson, CS, Fastenau, PS, Byars, AW, desGrauw, TJ, et al. Behavior problems in children at time of first recognized seizure and changes over the following 3 years. Epilepsy Behav 2011; 21: 373–81.CrossRefGoogle ScholarPubMed
18 Caplan, R, Siddarth, P, Gurbani, S, Ott, D, Sankar, R, Shields, WD. Psychopathology and pediatric complex partial seizures: seizure-related, cognitive, and linguistic variables. Epilepsia 2004; 45: 1273–81.CrossRefGoogle ScholarPubMed
19 Jones, JE, Watson, R, Sheth, R, Caplan, R, Koehn, M, Seidenberg, M, et al. Psychiatric comorbidity in children with new onset epilepsy. Dev Med Child Neurol 2007; 49: 493–7.CrossRefGoogle ScholarPubMed
20 Dabbs, K, Jones, JE, Jackson, DC, Seidenberg, M, Hermann, BP. Patterns of cortical thickness and the child behavior checklist in childhood epilepsy. Epilepsy Behav 2013; 29: 198204.CrossRefGoogle ScholarPubMed
21 Saute, R, Dabbs, K, Jones, JE, Jackson, DC, Seidenberg, M, Hermann, BP. Brain morphology in children with epilepsy and ADHD. PLoS One 2014; 9: e95269.CrossRefGoogle ScholarPubMed
22 Jones, JE, Jackson, DC, Chambers, KL, Dabbs, K, Hsu, DA, Stafstrom, CE, et al. Children with epilepsy and anxiety: subcortical and cortical differences. Epilepsia 2015; 56: 283–90.CrossRefGoogle ScholarPubMed
23 Engel, J Jr, International League Against Epilepsy (ILAE). A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE task force on classification and terminology. Epilepsia 2001; 42: 796803.CrossRefGoogle Scholar
24 Hollingshead, AB. Medical sociology: a brief review. Milbank Mem Fund Q Health Soc 1973; 51: 531–42.CrossRefGoogle ScholarPubMed
25 Kaufman, J, Birmaher, B, Brent, D, Rao, U, Flynn, C, Moreci, P, et al. Schedule for affective disorders and schizophrenia for school age children present and lifetime version (K SADS PL): initial reliability and validity data. J Am Acad Child Adolesc Psychiatry 1997; 36: 980–8.CrossRefGoogle ScholarPubMed
26 American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th edn (DMS-IV) ed. APA, 1994.Google Scholar
27 Wechsler, D. Wechsler Intelligence Scale for Children, 3rd edn. The Psychological Corporation, 1991.Google Scholar
28 Shattuck, DW, Leahy, RM. BrainSuite: an automated cortical surface identification tool. Med Image Anal 2002; 6: 129–42.CrossRefGoogle ScholarPubMed
29 Sled, JG, Pike, GB. Standing-wave and RF penetration artifacts caused by elliptic geometry: an electrodynamic analysis of MRI. IEEE Trans Med Imaging 1998; 17: 653–62.CrossRefGoogle ScholarPubMed
30 Han, X, Pham, DL, Tosun, D, Rettmann, ME, Xu, C, Prince, JL. Cruise: cortical reconstruction using implicit surface evolution. Neuroimage 2004; 23: 9971012.CrossRefGoogle ScholarPubMed
31 Tosun, D, Rettmann, ME, Naiman, DQ, Resnick, SM, Kraut, MA, Prince, JL. Cortical reconstruction using implicit surface evolution: accuracy and precision analysis. Neuroimage 2006; 29: 838–52.CrossRefGoogle ScholarPubMed
32 Tosun, D, Duchesne, S, Rolland, Y, Toga, AW, Vérin, M, Barillot, C. 3-D analysis of cortical morphometry in differential diagnosis of Parkinson's plus syndromes: mapping frontal lobe cortical atrophy in progressive supranuclear palsy patients. Med Image Comput Comput Assist Interv 2007; 10: 891–9.Google ScholarPubMed
33 Yezzi, AJ Jr, Prince, JL. An Eulerian PDE approach for computing tissue thickness. IEEE Trans Med Imaging 2003; 22: 1332–9.CrossRefGoogle ScholarPubMed
34 Tosun, D, Prince, JL. A geometry-driven optical flow warping for spatial normalization of cortical surfaces. IEEE Trans Med Imaging 2008; 27: 1739–53.CrossRefGoogle ScholarPubMed
35 Holmes, CJ, Hoge, R, Collins, L, Woods, R, Toga, AW, Evans, AC. Enhancement of MR images using registration for signal averaging. J Comput Assist Tomogr 1998; 22: 324–33.CrossRefGoogle ScholarPubMed
36 Tosun, D, Dabbs, K, Caplan, R, Siddarth, P, Toga, A, Seidenberg, M, et al. Deformation-based morphometry of prospective neurodevelopmental changes in new onset paediatric epilepsy. Brain 2011; 134: 1003–14.CrossRefGoogle ScholarPubMed
37 Ciumas, C, Saignavongs, M, Ilski, F, Herbillon, V, Laurent, A, Lothe, A, et al. White matter development in children with benign childhood epilepsy with centrotemporal spikes. Brain 2014; 137: 1095–106.CrossRefGoogle Scholar
38 Amft, M, Bzdok, D, Laird, AR, Fox, PT, Schilbach, L, Eickhoff, SB. Definition and characterization of an extended social-affective default network. Brain Struct Funct 2015; 220: 1031–49.CrossRefGoogle ScholarPubMed
39 Powell, JL, Lewis, PA, Dunbar, RI, García-Fiñana, M, Roberts, N. Orbital prefrontal cortex volume correlates with social cognitive competence. Neuropsychologia 2010; 48: 3554–62.CrossRefGoogle ScholarPubMed
40 Lewis, PA, Rezaie, R, Brown, R, Roberts, N, Dunbar, RI. Ventromedial prefrontal volume predicts understanding of others and social network size. Neuroimage 2011; 57: 1624–9.CrossRefGoogle ScholarPubMed
41 McNamee, D, Rangel, A, O'Doherty, JP. Category-dependent and category-independent goal-value codes in human ventromedial prefrontal cortex. Nat Neurosci 2013; 16: 479–85.CrossRefGoogle ScholarPubMed
42 Happaney, K, Zelazo, PD, Stuss, DT. Development of orbitofrontal function: current themes and future directions. Brain Cogn 2004; 55:110.CrossRefGoogle ScholarPubMed
43 Gansler, DA, McLaughlin, NCR, Iguchi, L, Jerram, M, Moore, DW, Bhadelia, R, et al. A multivariate approach to aggression and the orbital frontal cortex in psychiatric patients. Psychiatry Res 2009; 171: 145–54.CrossRefGoogle ScholarPubMed
44 Hoptman, MJ, D'Angelo, D, Catalano, D, Mauro, CJ, Shehzad, ZE, Kelly, AM, et al. Amygdalofrontal functional disconnectivity and aggression in schizophrenia. Schizophr Bull 2010; 36: 1020–8.CrossRefGoogle ScholarPubMed
45 Caplan, R, Siddarth, P, Levitt, J, Gurbani, S, Shields, WD, Sankar, R. Suicidality and brain volumes in pediatric epilepsy. Epilepsy Behav 2010; 18: 286–90.CrossRefGoogle ScholarPubMed
46 Mak, A, Wong, MM, Han, SH, Lee, TM. Gray matter reduction associated with emotion regulation in female outpatients with major depressive disorder: a voxel-based morphometry study. Progr Neuro-Psychopharmacol Biol Psychiatry 2009; 33: 1184–90.CrossRefGoogle ScholarPubMed
47 Najt, P, Nicoletti, M, Chen, HH, Hatch, JP, Caetano, SC, Sassi, RB, et al. Anatomical measurements of the orbitofrontal cortex in child and adolescent patients with bipolar disorder. Neurosci Lett 2007; 413: 183–6.CrossRefGoogle ScholarPubMed
48 Hoptman, MJ, Volavka, J, Weiss, EM, Czobor, P, Szeszko, PR, Gerig, G, et al. Quantitative MRI measures of orbitofrontal cortex in patients with chronic schizophrenia or schizoaffective disorder. Psychiatry Res 2005; 140: 133–45.CrossRefGoogle ScholarPubMed
49 Verdejo-García, A, Bechara, A. A somatic marker theory of addiction. Neuropharmacology 2009; 56: 4862.CrossRefGoogle ScholarPubMed
50 Ko, CH, Liu, G-C, Hsiao, S, Yen, JY, Yang, MJ, Lin, WC, et al. Brain activities associated with gaming urge of online gaming addiction. J Psychiatr Res 2009; 43: 739–47.CrossRefGoogle ScholarPubMed
51 Caplan, R, Levitt, J, Siddarth, P, Taylor, J, Daley, M, Wu, KN, et al. Thought disorder and frontotemporal volumes in pediatric epilepsy. Epilepsy Behav 2008; 13: 593–9.CrossRefGoogle ScholarPubMed
52 Daley, M, Levitt, J, Siddarth, P, Mormino, E, Hojatkashani, C, Gurbani, S, et al. Frontal and temporal volumes in children with epilepsy. Epilepsy Behav 2007; 10: 470–6.CrossRefGoogle ScholarPubMed
53 Hamiwka, L, Jones, JE, Salpekar, J, Caplan, R. Child psychiatry: special edition on the future of clinical epilepsy research. Epilepsy Behav 2011; 22: 3846.CrossRefGoogle Scholar
54 Khundrakpam, BS, Tohka, J, Evans, AC. Prediction of brain maturity based on cortical thickness at different spatial resolutions. Neuroimage 2015; 111: 350–9.CrossRefGoogle ScholarPubMed
55 Mankinen, K, Jalovaara, P, Paakki, JJ, Harila, M, Rytky, S, Tervonen, O, et al. Connectivity disruptions in resting-state functional brain networks in children with temporal lobe epilepsy. Epilepsy Res 2012; 100: 168–78.CrossRefGoogle ScholarPubMed
56 Widjaja, E, Zamyadi, M, Raybaud, C, Snead, OC, Smith, ML. Abnormal functional network connectivity among resting-state networks in children with frontal lobe epilepsy. AJNR Am J Neuroradiol 2013; 34: 2386–92.CrossRefGoogle ScholarPubMed
57 Haneef, Z, Lenartowicz, A, Yeh, HJ, Levin, HS, Engel, J Jr, Stern, JM. Functional connectivity of hippocampal networks in temporal lobe epilepsy. Epilepsia 2014; 55: 137–45.CrossRefGoogle ScholarPubMed
58 Voets, NL, Beckmann, CF, Cole, DM, Hong, S, Bernasconi, A, Bernasconi, N, et al. Structural substrates for resting network disruption in temporal lobe epilepsy. Brain 2012; 135: 2350–7.CrossRefGoogle ScholarPubMed
59 McDonald, CR, Hagler, DJ, Ahmadi, ME, Tecoma, E, Iragui, V, Gharapetian, L, et al. Regional neocortical thinning in mesial temporal lobe epilepsy. Epilepsia 2008; 49: 794803.CrossRefGoogle ScholarPubMed
60 Lin, JJ, Salamon, N, Lee, AD, Dutton, RA, Geaga, JA, Hayashi, KM, et al. Reduced neocortical thickness and complexity mapped in mesial temporal lobe epilepsy with hippocampal sclerosis. Cereb Cortex 2007; 17: 2007–18.CrossRefGoogle ScholarPubMed
61 Lin, JJ, Mula, M, Hermann, BP. Uncovering the neurobehavioural comorbidities of epilepsy over the lifespan. Lancet 2012; 380: 1180–92.CrossRefGoogle ScholarPubMed
62 Shaw, P, Malek, M, Watson, B, Sharp, W, Evans, A, Greenstein, D. Development of of cortical surface area and gyrification in attention-deficit/hyperactivity disorder. Biol Psychiatry 2012; 72: 191–7.CrossRefGoogle ScholarPubMed
63 Caplan, R, Siddarth, P, Stahl, L, Lanphier, E, Vona, P, Gurbani, S, et al. Childhood absence epilepsy: behavioral, cognitive, and linguistic comorbidities. Epilepsia 2008; 49: 1838–46.CrossRefGoogle ScholarPubMed
64 Austin, JK, Dunn, DW, Caffrey, HM, Perkins, SM, Harezlak, J, Rose, DF. Recurrent seizures and behavior problems in children with first recognized seizures: a prospective study. Epilepsia 2002; 43: 1564–73.CrossRefGoogle ScholarPubMed
65 Hermann, BP, Jones, JE, Sheth, R, Koehn, M, Becker, T, Fine, J, et al. Growing up with epilepsy: a two-year investigation of cognitive development in children with new onset epilepsy. Epilepsia 2008; 49: 1847–58.CrossRefGoogle ScholarPubMed
66 Noble, KG, Houston, SM, Kan, E, Sowell, ER. Neural correlates of socioeconomic status in the developing human brain. Dev Sci 2012; 15: 516–27.CrossRefGoogle ScholarPubMed
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