Ganglion Cell Layer, Inner Plexiform Layer, and Choroidal Layer Correlate Better with Disorder Severity in ADHD Patients than Retinal Nerve Fiber Layer: An Optical Coherence Tomography Study

Abstract

Aim: To assess the thickness of the choroidal layer, inner plexiform layer (IPL), ganglion cell layer (GCL), and retinal nerve fiber layer (RNFL) in individuals with attention-deficit/hyperactivity disorder (ADHD). Material and Methods: In this retrospective study, we used a spectral optical coherence tomography (OCT) device. The CPRS-48 was performed to the ADHD group. Results: Both groups consisted of 60 subjects. There were significant differences in NS segment of RNFL (right p=0.039; left p=0.035). The mean right choroidal thickness of ADHD group was significantly lower than the control group (p=0.015). The left GCL and IPL volumes of ADHD group were significantly lower than the control group (p<0.05). In ADHD group, a significant correlation was found between right choroid and opposition (r=0.278, p<0.05) and conduct (r=0.373, p<0.01) subscales of CPRS-48; between age and right choroid (r=0.248, p<0.05). In control group, a significant correlation was found between age and right NS (r=-0.370, p<0.05), right TS (r=-0.381, p<0.05), right mean RNFL (r=-0.352, p<0.05), left NS (r=-0.397, p<0.05), right choroid (r=0.422, p<0.01), left choroid (r=0.443, p<0.01), right GCL (r=0.425, p<0.01), right IPL (r=0.446, p<0.01). Conclusion: This study demonstrated that there is an association between disorder severity, duration of disorder, choroidal layer thickness, GCL, IPL and ADHD.

Keywords

• Ganglion cell layer
• inner plexiform layer
• retinal nerve fiber layer
• attention-deficit/hyperactivity disorder
• optical coherence tomography

References

1. 1. Hu HF, Chou WJ, Yen CF. Anxiety and depression among adolescents with attention-deficit/hyperactivity disorder: the roles of behavioral temperamental traits, comorbid autism spectrum disorder, and bullying involvement. Kaohsiung J Med Sci. 2016;32:103-9.
2. 2. Bijlenga D, Vollebregt MA, Kooij JJS, Arns M. The role of the circadian system in the etiology and pathophysiology of ADHD: time to redefine ADHD?. Atten Defic Hyperact Disord. 2019;11:5-19.
3. 3. Weyandt L, Swentosky A, Gudmundsdottir BG. Neuroimaging and ADHD: fMRI, PET, DTI findings, and methodological limitations. Dev Neuropsychol. 2013;38:211-25.
4. 4. Karadag AS, Kalenderoglu A, Orum MH. Optical coherence tomography findings in conversion disorder: are there any differences in the etiopathogenesis of subtypes?. Arch Clin Psychiatry. 2018;45:154-60.
5. 5. Hergüner A, Alpfidan İ, Yar A, et al. Retinal nerve fiber layer thickness in children with ADHD. J Atten Disord. 2018;22:619-26.
6. 6. Ulucan Atas PB, Ceylan OM, Dönmez YE, Ozel Ozcan O. Ocular findings in patients with attention deficit and hyperactivity. Int Ophthalmol. 2020;40:3105-13.
7. 7. Işik Ü, Kaygisiz M. Assessment of intraocular pressure, macular thickness, retinal nerve fiber layer, and ganglion cell layer thicknesses: ocular parameters and optical coherence tomography findings in attention-deficit/hyperactivity disorder. Braz J Psychiatry. 2020;42:309-13.
8. 8. Akkaya S, Ulusoy DM, Dogan H, Arslan ME. Assessment of the effect of attention-deficit hyperactivity disorder on choroidal thickness using spectral domain optical coherence tomography. Beyoglu Eye J. 2021;6:161-5.

9. 9. Bodur Ş, Kara H, Açıkel B, Yaşar E. Evaluation of the ganglion cell layer thickness in children with attention deficit hyperactivity disorder and comorbid oppositional defiant disorder. Turkish J Clinical Psychiatry. 2018;21:222-30.
10. 10. Ayyildiz T, Ayyildiz D. Retinal nerve fiber layer, macular thickness and anterior segment measurements in attention deficit and hyperactivity disorder. Psychiatr Clin Psychopharmacol. 2019;29:760-4.
11. 11. Tosun ZS, Vural Ozec A, Erdogan H, et al. Examination of retinal and choroidal structural changes in children with attention deficit/hyperactivity disorder. Research Square. https://doi.org/10.21203/rs.3.rs-341702/v1.
12. 12. American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 5th edition. American Psychiatric Publishing, Washington DC, 2013.
13. 13. Celik C, Yigit I, Erden G. Wechsler Çocuklar İçin Zeka Ölçeği Geliştirilmiş Formunun (WISC-R) doğrulayıcı faktör analizi: Normal zihinsel gelişim gösteren çocukların oluşturduğu bir örneklem. Türk Psikoloji Yazıları. 2015;18:21-9.
14. 14. Goyette CH, Conners CK, Ulrich RE. Normative data on the revised Conners’ parent and teacher rating scales. J Abnorm Child Psychol. 1978;6:221-36.
15. 15. Conners CK, Wells KC, Parker JD, et al. A new self- report scale for assessment of adolescent psychopathology: Factor structure, reliability, validity and diagnostic sensitivity. J Abnorm Child Psychol. 1997;25:487-97.
16. 16. Dereboy Ç, Şenol S, Şener Ş, Dereboy F. Conners kısa form öğretmen ve ana baba derecelendirme ölçeklerinin geçerliği. Türk Psikiyatri Dergisi. 2007;18:48-58.
17. 17. Berger I, Slobodin O, Aboud M, et al. Maturational delay in ADHD: evidence from CPT. Front Hum Neurosci. 2013;7:691.
18. 18. Vaidya CJ. Neurodevelopmental abnormalities in ADHD. Curr Top Behav Neurosci. 2012;9:49-66.
19. 19. Altemir I, Oros D, Elía N, et al. Retinal asymmetry in children measured with optical coherence tomography. Am J Ophthalmol. 2013;156:1238-43.
20. 20. Pekel G, Acer S, Ozbakis F, et al. Macular asymmetry analysis in sighting ocular dominance. Kaohsiung J Med Sci. 2014;30:531-6.
21. 21. Douglas PK, Gutman B, Anderson A, et al. Hemispheric brain asymmetry differences in youths with attention-deficit/hyperactivity disorder. Neuroimage Clin. 2018;18:744-52.
22. 22. Silk TJ, Vilgis V, Adamson C, et al. Abnormal asymmetry in frontostriatal white matter in children with attention deficit hyperactivitydisorder. Brain Imaging Behav. 2016;10:1080-9.
23. 23. Hale TS, Loo SK, Zaidel E, et al. Rethinking a right hemisphere deficit in ADHD. J Atten Disord. 2009;13:3-17.
24. 24. Rennie B, Beebe-Frankenberger M, Swanson HL. A longitudinal study of neuropsychological functioning and academic achievement in children with and without signs of attention-deficit/ hyperactivity disorder. J Clin Exp Neuropsychol. 2014;36:621-35.
25. 25. Almeida Montes LG, Prado Alcántara H, Martínez García RB, et al. Brain cortical thickness in ADHD: age, sex, and clinical correlations. J Atten Disord. 2013;17:641-54.
26. 26. Frodl T, Skokauskas N. Meta-analysis of structural MRI studies in children and adults with attention deficit hyperactivity disorder indicates treatment effects. Acta Psychiatr Scand. 2012;125:114-26.
27. 27. Nakao T, Radua J, Rubia K, Mataix-Cols D. Gray matter volume abnormalities in ADHD: voxelbased meta-analysis exploring the effects of age and stimulant medication. Am J Psychiatry. 2011;168:1154-63.
28. 28. Cepko CL, Austin CP, Yang X, Alexiades M, Ezzeddine D. Cell fate determination in the vertebrate retina. Proc Natl Acad Sci U S A. 1996;93:589-95.
29. 29. Coombs JL, Van Der List D, Chalupa LM. Morphological properties of mouse retinal ganglion cells during postnatal development. J Comp Neurol. 2007;503:803-14.
30. 30. Popova E. Role of Dopamine in Retinal Function. In: The Organization of the Retina and Visual System. University of Utah Health Sciences Center, Salt Lake City,1995.
31. 31. Huemer KH, Garhofer G, Zawinka C, et al. Effects of dopamine on human retinal vessel diameter and its modulation during flicker stimulation. Am J Physiol Heart Circ Physiol. 2003;284:H358-63.
32. 32. Huemer KH, Zawinka C, Garhöfer G, et al. Effects of dopamine on retinal and choroidal blood flow parameters in humans. Br J Ophthalmol. 2007;91:1194-8.