Nihan KATAYIFÇI, Muzaffer SİNDEL, Niyazi ACER, Güneş AYTAÇ, Fatma ÖZ, Kamil KARAALİ

The role of lateralisation and sex on insular cortex: 3D volumetric analysis

Background/aim: The insula has attracted the attention of many neuroimaging studies because of its key role between brain structures. However, the number of studies investigating the effect of sex and laterality on insular volume is insufficient. The aim of this study was to investigate the differences in insular volume between sexes and hemispheres. Materials and methods: A total of 47 healthy participants [24 males (20.08 ± 1.44 years) and 23 females (19.57 ± 0.90 years)] underwent magnetic resonance imaging (MRI). Imaging was performed using the 3T MRI scanner. The insular volume was measured using the Individual Brain Atlases using Statistical Parametric Mapping (IBASPM); total intracranial, cerebral, grey and white matter volumes were measured using volBrain. Results: The right insular volume was significantly higher than the left insular volume in the participants, and the left cerebral volume was significantly higher than the right cerebral volume (p < 0.05). The total brain, total cerebral, left and right insular, and cerebral volumes were significantly larger in males than in females (p < 0.001). Also, the ratios of the insular volume to total brain and cerebral volume were significantly higher in males than in females (p < 0.05). Conclusion: This study shows that insular volume differs with laterality and sex. This outcome may be explained by the anatomical relationship between the insula and behavioural functions and emotional reactions and the fact that the right side of the brain is best at expressive and creative tasks.Key words: Insula of reil, MRI, brain mapping, sex differences

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1. Acer N, Turgut M. Measurements of the insula volume using MRI. In: Turgut M, Yurttaş C, Tubbs RS (editors). Island of Reil (Insula) in the Human Brain. Cham: Springer; 2018. pp. 101- 111
2. Bauernfeind AL, De Sousa AA, Avasthi T, Dobson SD, Raghanti MA et al. A volumetric comparison of the insular cortex and its subregions in primates. Journal of Human Evolution 2013; 64 (4): 263-279. doi: 10.1016/j.jhevol.2012.12.003
3. Benarroch EE. Insular cortex: functional complexity and clinical correlations. Neurology 2019; 93 (21): 932-938. doi: 10.1212/WNL.0000000000008525
4. Stephani C, Fernandez-Baca Vaca G, Maciunas R, Koubeissi M, Lüders HO. Functional neuroanatomy of the insular lobe. Brain Structure & Function 2011; 216 (2): 137-149. doi: 10.1007/s00429-010-0296-3
5. Gogolla N. The insular cortex. Current Biology: CB 2017; 27 (12): 580-586. doi: 10.1016/j.cub.2017.05.010
6. Craig AD. How do you feel--now? The anterior insula and human awareness. Nature Reviews Neuroscience 2009; 10 (1): 59-70. doi: 10.1038/nrn2555
7. Nieuwenhuys R. The insular cortex: a review. Progress in Brain Research 2012; 195: 123-163. doi: 10.1016/B978-0-444-53860- 4.00007-6
8. Craig AD. Forebrain emotional asymmetry: a neuroanatomical basis? Trends in Cognitive Sciences 2005; 9 (12): 566-571. doi: 10.1016/j.tics.2005.10.005
9. Papagno C, Pisoni A, Mattavelli G, Casarotti A, Comi A et al. Specific disgust processing in the left insula: new evidence from direct electrical stimulation. Neuropsychologia 2016; 84: 29-35. doi: 10.1016/j.neuropsychologia.2016.01.036
10. Isnard J, Magnin M, Jung J, Mauguière F, Garcia-Larrea L. Does the insula tell our brain that we are in pain? Pain 2011; 152 (4): 946-951. doi: 10.1016/j.pain.2010.12.025
11. Karnath HO, Baier B. Right insula for our sense of limb ownership and self-awareness of actions. Brain Structure & Function 2010; 214 (5-6): 411-417. doi: 10.1007/s00429-010- 0250-4
12. Naidich TP, Kang E, Fatterpekar GM, Delman BN, Gultekin SH et al. The insula: anatomic study and MR imaging display at 1.5 T. American Journal of Neuroradiology 2004; 25 (2): 222- 232
13. Macey PM, Rieken NS, Kumar R, Ogren JA, Middlekauff HR et al. Sex differences in insular Cortex Gyri responses to the Valsalva Maneuver. Frontiers in Neurology 2016; 7: 87. doi: 10.3389/fneur.2016.00087
14. Cheng Y, Chou KH, Decety J, Chen IY, Hung D et al. Sex differences in the neuroanatomy of human mirrorneuron system: a voxel-based morphometric investigation. Neuroscience 2009; 158 (2): 713-720. doi: 10.1016/j. neuroscience.2008.10.026
15. Sowell ER, Peterson BS, Kan E, Woods RP, Yoshii J et al. Sex differences in cortical thickness mapped in 176 healthy individuals between 7 and 87 years of age. Cerebral Cortex 2007; 17 (7): 1550-1560. doi: 10.1093/cercor/bhl066
16. Mutlu AK, Schneider M, Debbané M, Badoud D, Eliez S et al. Sex differences in thickness, and folding developments throughout the cortex. Neuroimage 2013; 82 : 200-207. doi: 10.1016/j.neuroimage.2013.05.076
17. Koolschijn PC, Crone EA. Sex differences and structural brain maturation from childhood to early adulthood. Developmental Cognitive Neuroscience 2013; 5: 106-118. doi: 10.1016/j. dcn.2013.02.003
18. Ruigrok AN, Salimi-Khorshidi G, Lai MC, Baron-Cohen S, Lombardo MV et al. A meta-analysis of sex differences in human brain structure. Neuroscience and Biobehavioral Reviews 2014; 39 (100): 34-50. doi: 10.1016/j.neubiorev.2013.12.004
19. Westerhausen R, Huster RJ, Kreuder F, Wittling W, Schweiger E. Corticospinal tract asymmetries at the level of the internal capsule: is there an association with handedness? Neuroimage 2007; 37 (2): 379-386. doi:10.1016/j.neuroimage.2007.05.047
20. Manjón JV, Coupé P. volBrain: An online MRI brain volumetry system. Frontiers in Neuroinformatics 2016; 10: 30. doi: 10.3389/fninf.2016.00030
21. Coupé P, Manjón JV, Fonov V, Pruessner J, Robles M et al. Patch-based segmentation using expert priors: application to hippocampus and ventricle segmentation. Neuroimage 2011; 54 (2): 940-954. doi:10.1016/j.neuroimage.2010.09.018
22. Kim JH, Choi DS, Kim SH, Shin HS, Seo H et al. Evaluation of hippocampal volume based on various inversion time in normal adults by manual tracing and automated segmentation methods. Investigative Magnetic Resonance Imaging 2015; 19 (2): 67-75. doi: 10.13104/imri.2015.19.2.67
23. Tae WS, Kim SS, Lee KU, Nam EC, Kim KW. Validation of hippocampal volumes measured using a manual method and two automated methods (FreeSurfer and IBASPM) in chronic major depressive disorder. Neuroradiology 2008; 50 (7): 569- 581. doi: 10.1007/s00234-008-0383-9
24. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002; 15 (1): 273-289. doi: 10.1006/nimg.2001.0978
25. Fields A. Discovering statistics using SPSS. Beverly Hills: Sage Publications; 2005.
26. Wierenga LM. The development of brain structure and connectivity. PhD, Utrecht University, Utrecht, the Netherlands, 2016.
27. McCarthy MM, Arnold AP. Reframing sexual differentiation of the brain. Nature Neuroscience 2011; 14 (6): 677-683. doi: 10.1038/nn.2834
28. Kennedy DN, Lange N, Makris N, Bates J, Meyer J et al. Gyri of the human neocortex: an MRI-based analysis of volume and variance. Cerebral Cortex 1998; 8 (4): 372-384. doi: 10.1093/ cercor/8.4.372
29. Mavridis I, Boviatsis E, Anagnostopoulou S. Exploring the neurosurgical anatomy of the human insula: a combined and comparative anatomic-radiologic study. Surgical and Radiologic Anatomy: SRA 2011; 33 (4): 319-328. doi: 10.1007/ s00276-010-0699-0
30. Augustine JR. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Research Reviews 1996; 22 (3): 229-244. doi: 10.1016/s0165-0173(96)00011-2
31. Brooks JC, Zambreanu L, Godinez A, Craig AD, Tracey I. Somatotopic organisation of the human insula to painful heat studied with high resolution functional imaging. Neuroimage 2005; 27 (1): 201-209. doi: 10.1016/j.neuroimage.2005.03.041
32. Mesulam MM, Mufson EJ. Insula of the old world monkey. I. Architectonics in the insulo-orbito-temporal component of the paralimbic brain. The Journal of Comparative Neurology 1982; 212 (1): 1-22. doi: 10.1002/cne.902120102
33. Corballis MC. Left brain, right brain: facts and fantasies. Plos Biology 2014; 12 (1): e1001767. doi: 10.1371/journal. pbio.1001767
34. Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM. FSL. Neuroimage 2012; 62 (2): 782-790. doi: 10.1016/j. neuroimage.2011.09.015
35. Fischl B. FreeSurfer. Neuroimage 2012; 62 (2): 774-781. doi: 10.1016/j.neuroimage.2012.01.021
36. Ashburner J. SPM: a history. Neuroimage 2012; 62 (2): 791- 800. doi: 10.1016/j.neuroimage.2011.10.025
37. Li W, Yang C, Shi F, Wang Q, Wu S et al. Alterations in normal aging revealed by cortical brain network constructed using IBASPM. Brain Topography 2018; 31 (4): 577-590. doi:10.1007/ s10548-018-0642-y
38. Wang Y, Xu Q, Luo J, Hu M, Zuo C. Effects of age and sex on subcortical volumes. Frontiers in Aging Neuroscience 2019; 26 (11): 259. doi: 10.3389/fnagi.2019.00259
39. Dewey J, Hana G, Russell T, Price J, McCaffrey D et al. Reliability and validity of MRI-based automated volumetry software relative to auto-assisted manual measurement of subcortical structures in HIV-infected patients from a multisite study. Neuroimage 2010; 51 (4): 1334-1344. doi:10.1016/j. neuroimage.2010.03.033
40. Makris N, Goldstein JM, Kennedy D, Hodge SM, Caviness VS et al. Decreased volume of left and total anterior insular lobule in schizophrenia. Schizophrenia Research 2006; 83 (2-3): 155- 171. doi:10.1016/j.schres.2005.11.020
41. Saze T, Hirao K, Namiki C, Fukuyama H, Hayashi T et al. Insular volume reduction in schizophrenia. European Archives of Psychiatry and Clinical Neuroscience 2007; 257 (8): 473- 479. doi: 10.1007/s00406-007-0750-2
42. Hervey-Jumper SL, Berger MS. Insular glioma surgery: an evolution of thought and practice. Journal of Neurosurgery 2019; 130 (1): 9-16. doi: 10.3171/2018.10.JNS181519
43. Hameed NUF, Qiu T, Zhuang D, Lu J, Yu Zet al. Transcortical insular glioma resection: clinical outcome and predictors. Journal of Neurosurgery 2018; 131 (3): 706-716. doi: 10.3171/2018.4.JNS18424