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Insular Volume Reductions in Patients with Major Depressive Disorder Insular volume reductions in patients with major depressive disorder Item Type Article Authors Mutschler, Isabella; Hänggi, Jürgen; Frei, Manuela; Lieb, Roselind; grosse Holforth, Martin; Seifritz, Erich; Spinelli, Simona Citation Mutschler, I., Hänggi, J., Frei, M., Lieb, R., grosse Holforth, M., Seifritz, E., & Spinelli, S. (2019). Insular volume reductions in patients with major depressive disorder. Neurology, Psychiatry and Brain Research, 33, 39–47. doi:10.1016/j.npbr.2019.06.002 Eprint version Post-print DOI 10.1016/j.npbr.2019.06.002 Publisher Elsevier BV Journal Neurology Psychiatry and Brain Research Rights NOTICE: this is the author’s version of a work that was accepted for publication in Neurology Psychiatry and Brain Research. Changes resulting from the publishing process, such as peer review, editing, corrections, structural formatting, and other quality control mechanisms may not be reflected in this document. Changes may have been made to this work since it was submitted for publication. A definitive version was subsequently published in Neurology Psychiatry and Brain Research, [[Volume], [Issue], (2019-06-22)] DOI: 10.1016/ j.npbr.2019.06.002 . © 2019. This manuscript version is made available under the CC-BY-NC-ND 4.0 license http:// creativecommons.org/licenses/by-nc-nd/4.0/ Download date 23/09/2021 13:26:26 Item License http://creativecommons.org/licenses/by-nc-nd/4.0/ Link to Item http://hdl.handle.net/10754/656271 Neurology, Psychiatry and Brain Research 33 (2019) 39–47 Contents lists available at ScienceDirect Neurology, Psychiatry and Brain Research journal homepage: www.elsevier.com/locate/npbr Insular volume reductions in patients with major depressive disorder T ⁎ Isabella Mutschlera, , Jürgen Hänggib, Manuela Freia, Roselind Lieba, Martin grosse Holforthc,d, Erich Seifritze, Simona Spinellif a Department of Psychology, Clinical Psychology and Epidemiology, University of Basel, Basel, Switzerland b Division Neuropsychology, Department of Psychology, University of Zurich, Zurich, Switzerland c Department of Psychology, University of Bern, Switzerland d Psychosomatic Competence Center, Department of Neurology, Inselspital, Bern, Switzerland e Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Switzerland f King Abdullah University of Science and Technology, Animal Resources Core Lab, Thuwal, Saudi Arabia ARTICLE INFO ABSTRACT Keywords: Background: Major Depressive Disorder (MDD) is one of the most common mental disorders. Converging evi- Major depressive disorder dence suggests that the insula plays an important role in the pathophysiology of MDD. Little is known regarding Insula in which insula subregion volume alterations occur in patients with MDD. Voxel-based morphometry Methods: We analyzed voxel-based morphometry in T1-weighted MRI scans of unmedicated DSM-IV MDD pa- Meta-analysis tients (n = 26) and in age, education, and sex matched healthy controls (HC, n = 26). Furthermore, we per- Interoception formed a quantitative meta-analysis across 14 structural MRI MDD studies by applying the anatomical likelihood Grey matter volume estimation technique to identify concordant volume reductions in MDD in the insula cortex. Results: We found significantly reduced grey matter volumes (GMV) in patients with MDD compared to HCs in the left mid-insula and in the right and left caudate nucleus. The left mid-insular volume reduction in our sample was consistent with the coordinate-based meta-analysis results. Conclusions: The findings highlight the role of the mid-insula in the psychopathology of MDD. The mid-insula subregion might be associated with reduced interoceptive abilities in patients with MDD that is the ability to process information of “how the body feels”. In addition, the caudate nucleus has been described as being part of a network that mediates emotional and motivational processes which seems to be affected in MDD. 1. Introduction thalamus, caudate nucleus, putamen and globus pallidus (Delaveau et al., 2011). Another meta-analysis focused on the insular cortex and Major depressive disorder (MDD) is among the most prevalent showed that during emotional processing in depressed individuals, in- mental disorders worldwide with a lifetime prevalence ranging from sula activation may be topographically shifted toward insula subregions 6.6 to 21% across cultures (Kessler & Bromet, 2013). According to DSM- typically associated with the experience of pain (Mutschler, Ball, 5, MDD is characterized by depressed mood, diminished interests, im- Wankerl, & Strigo, 2012). More recently, Li and colleagues reported paired cognitive function and vegetative symptoms (American abnormalities in resting-state brain activity in medication-free MDD Psychiatric Association, 2013). MDD profoundly impacts individuals’ patients in meta-analyses of ALFF (amplitude of low-frequency fluc- lifes (Otte et al., 2016) and has been associated with medical co- tuations) studies and rCBF (regional cerebral blood flow) studies in morbidity such as chronic pain (Kessler & Bromet, 2013) and increased different brain regions including the left insula, anterior cingulate risk for cardiovascular disorders (Whooley & Wong, 2013). cortex, inferior frontal gyrus, right caudate nucleus, supplementary In the last decades, a large number of neuroimaging studies have motor area and hippocampus (Li et al., 2017). Furthermore, a meta- investigated functional brain characteristics in depression. A meta- analysis on structural MRI studies found reduced grey matter volume in analysis of functional neuroimaging studies showed that responses to the insula in MDD samples (Peng, Chen, Yin, Jia, & Gong, 2016). To- emotional stimuli in depression involve the insula, prefrontal cortices, gether these findings provide strong support for the assumption that the hippocampus, amygdala, anterior cingulate cortex, cerebellum, insula plays a pivotal role in the pathophysiology of MDD. The insula ― ⁎ Corresponding author at: University of Basel, Department of Psychology, Division of Clinical Psychology & Epidemiology, Missionsstrasse 62a, 4055 Basel, Switzerland. E-mail address: [email protected] (I. Mutschler). https://doi.org/10.1016/j.npbr.2019.06.002 Received 31 October 2018; Received in revised form 12 June 2019; Accepted 14 June 2019 0941-9500/ © 2019 Published by Elsevier GmbH. I. Mutschler, et al. Neurology, Psychiatry and Brain Research 33 (2019) 39–47 a brain structure that is situated in the depth of the Sylvian fissure ― is Table 1 anatomically connected to many other brain regions (Nieuwenhuys, Demographics, symptom severity and other clinical characteristics for 2012). The insula is pyramid-shaped and anatomically divided by the patients with MDD and healthy controls (HC) investigated in the MRI central insular sulcus into an anterior and posterior part (Ture, Yasargil, study. Individuals with MDD and HCs completed the Hopelessness Scale (H- Al-Mefty, & Yasargil, 1999). It is thought that the insular cortex might Scale) (Krampen, 1994) and the State-Trait Anxiety Inventory (STAI) (Laux et al., 1981). Individuals with MDD were also assessed with the Inventory for underlie a wide range of functions in humans such as processing in- Depressive Symptomatology (IDS) (Helmreich et al., 2011; Rush et al., 1996), formation related to the state of the body as well self-awareness, cog- and the Beck Depression Inventory II (BDI-II) (Beck et al., 1996). Statistics: Last nitive and emotional functioning, somatomotor control, and language column shows statistical analysis of two-sample t-test comparing the MDD (Christopher, Koshimori, Lang, Criaud, & Strafella, 2014; Craig, 2002; group and the HC group (a based on n = 25; b based on n = 24; SD = Standard Kelly et al., 2012a; Mutschler et al., 2009; Uyanikgil, Cavusoglu, Celik, deviation). & Kilic, 2018). Subjects MDD HCs Statistics Little is known, however, regarding in which insula subregion vo- lume alterations occur in individuals with MDD. There is growing Number of subjects n = 26 n = 26 evidence that there is a functional organization in the insula and that Sex different insula subregions may serve different functions (Deen, Pitskel, male/female n = 17/9 n = 17/9 Age & Pelphrey, 2011; Kelly et al., 2012b; Mutschler et al., 2009). The mean (range) 40.19 (22-63) 35.92 (20-60) p = 0.25 dorsal anterior insula may be involved in perception of vocalizations Years of education and language (Mutschler et al., 2009), cognition (Deen et al., 2011) and mean (SD) 15.64 (3.60) 15.5 (2.44) p = 0.21 the ventral anterior insula may be involved in peripheral physiological Episodes: processing resulting from emotional experiences (Mutschler et al., First n = 9 Recurrent n = 17 2009). The mid insula has been associated with interoception (see Fig. 5 BDI score 25.26 (8.34) in reference (Kelly et al., 2012a). Hence, knowing in which insula mean (SD) subregion grey matter volume reductions in MDD occur may shed light IDS (SD) 34.54 (8.51) on functional impairments in MDD. On this background, we performed STAI Trait (SD) 56.0 (9.85) 33.1 (8.01) p = 2.5E-12 STAI State (SD) 43.62 (5.92)a 32.4 (5.29)b p = 8.5E-09 two studies. In the first study, T1-weighted MRI scans were analyzed in H-Scale (SD) 75.1 (12.90) 45.7 (11.01) p = 8.5E-12 unmedicated DSM-IV MDD patients (n = 26) and in age, education, and sex matched healthy controls (HC, n = 26) using voxel-based mor- phometry (VBM). We hypothesized that GM volumes within the insula 2.1.2. Psychometric measures would be significantly
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