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New-Onset Psychosis Associated with a Lesion Localized in the Rostral Tectum: Insights Into Pathway-Specific Connectivity Disrupted in Psychosis

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New-Onset Psychosis Associated with a Lesion Localized in the Rostral Tectum: Insights Into Pathway-Specific Connectivity Disrupted in Psychosis Downloaded from https://academic.oup.com/schizophreniabulletin/advance-article-abstract/doi/10.1093/schbul/sbaa018/5760704 by Access provided HEAL-Link (National Technical University of Athens) user on 22 June 2020 applyparastyle "fig//caption/p[1]" parastyle "FigCapt" applyparastyle "fig" parastyle "Figure" Schizophrenia Bulletin doi:10.1093/schbul/sbaa018 New-Onset Psychosis Associated With a Lesion Localized in the Rostral Tectum: Insights Into Pathway-Specific Connectivity Disrupted in Psychosis Eleftheria Koropouli*,1,2, Nikos Melanitis3, Vasileios I. Dimitriou1, Asimina Grigoriou1, Efstratios Karavasilis4, Konstantina S. Nikita3, Elias Tzavellas1, and Thomas Paparrigopoulos1 1First Department of Psychiatry, Aiginition Hospital, National and Kapodistrian University of Athens School of Medicine, Athens, Greece; 2Present address: First Department of Neurology, Aiginition Hospital, National and Kapodistrian University of Athens School of Medicine, Athens, Greece; 3School of Electrical and Computer Engineering, National Technical University of Athens, Athens, Greece; 4Second Department of Radiology, Attikon Hospital, National and Kapodistrian University of Athens School of Medicine, Athens, Greece *To whom correspondence should be addressed; First Department of Neurology, Aiginition Hospital, National and Kapodistrian University of Athens, Vasilissis Sofias Avenue 72–74, Athens, Attica 11528, Greece, e-mail: [email protected]. Objective: To investigate pathway-specific connectivity dis- primary and higher-order brain areas serving distinct rupted in psychosis. Methods: We carried out a case study of functions.1,2 This dysregulation has been substantiated a middle-aged patient who presented with new-onset psychosis on the basis of resting-state activity of broadly distrib- associated with a space-occupying lesion localized in the right uted functional networks in schizophrenic individuals.2 superior colliculus/periaqueductal gray. The study sought to Despite the advances in elucidating such networks, two investigate potential connectivity deficits related to the lesion major questions remain unanswered. First, functional by the use of diffusion tensor imaging and resting-state func- connectivity aberrations that occur in prodromal stages tional magnetic resonance imaging. To this aim, we generated of psychosis remain occult. Second, the precise neural a functional connectivity map of the patient’s brain, centered pathways underlying psychosis have yet to be identified; on the lesion area, and compared this map with the corre- despite that certain structures, such as the hippocampus, sponding map of 10 sex- and age-matched control individuals exhibit profound structural and functional abnormalities identified from the Max Planck Institute–Leipzig Mind– in psychosis,3 it is unknown whether these deficits un- Brain–Body database. Results: Our analysis revealed a dis- derlie psychosis or they constitute the sequela of general- crete area in the right rostral tectum, in the immediate vicinity ized and lasting brain dysfunction. of the lesion, whose activity is inversely correlated with the It is well known that in both prodromal and clinically activity of left amygdala, whereas left amygdala is function- overt psychosis, there is impairment of saccadic eye move- ally associated with select areas of the temporal, parietal, and ments4–6; the latter are controlled cortically by the frontal occipital lobes. Based on a comparative analysis of the patient eye field and subcortically by the superior colliculus (SC).7 with 10 control individuals, the lesion has impacted on the con- The SC consists of multiple layers, each with distinct in- nectivity of rostral tectum (superior colliculus/periaqueductal puts and outputs.8,9 The SC receives inputs from retinal gray) with left amygdala as well as on the connectivity of left ganglion cells,10 cortical areas (visual, auditory, motor, amygdala with subcortical and cortical areas. Conclusions: prefrontal),9,11,12 locus coeruleus13 and its efferents project The superior colliculus/periaqueductal gray might play impor- to cortex,8 substantia nigra pars compacta,14 amygdala tant roles in the initiation and perpetuation of psychosis, at through the pulvinar,15 parabigeminal nucleus,9,16,17 lat- least partially through dysregulation of left amygdala activity. eral posterior thalamic nucleus,9,17,18 and brainstem nu- clei.9 The SC, besides being an integral part of the visual Key words: psychosis/schizophrenia/neural connectivity/ pathway,7 constitutes a cross-modal integration center resting-state functional MRI/superior colliculus/ capable of guiding motor behaviors in response to ex- periaqueductal gray/amygdala ternal stimuli.19–21 In particular, SC excitation can drive fear, anxiety, and defensive behaviors8,9,11,16–18,22–25; this is largely mediated by excitatory collicular projections Introduction to amygdala through the parabigeminal nucleus9,16,17 or In schizophrenia, there is severe dysregulation of ana- through the thalamus.18 In addition, the closely associated tomical and functional neuronal connectivity among periaqueductal gray (PAG), which is directly connected © The Author(s) 2020. Published by Oxford University Press on behalf of the Maryland Psychiatric Research Center. All rights reserved. For permissions, please email: [email protected] Page 1 of 10 Downloaded from https://academic.oup.com/schizophreniabulletin/advance-article-abstract/doi/10.1093/schbul/sbaa018/5760704 by Access provided HEAL-Link (National Technical University of Athens) user on 22 June 2020 E. Koropouli et al to SC,9 plays essential roles in fear expression and defen- (affine) transformation with 12 degrees of freedom.37 We sive behavior26–28 and is also connected to amygdala.28–30 then selected manually, using fsleyes tool, a seed region Of note, amygdala is indispensable for escape from around superior colliculus in the T1 sequence and used impending threats.31 However, despite elegant research in PROBTRACKX tool on BEDPOSTX output to recon- animal models, schizophrenic phenotypes cannot be fully struct fiber bundles. reproduced with the existing behavioral paradigms.32,33 In figure 3B, the principal direction of diffusion is dis- Herein, we report a case study of a middle-aged indi- played at each voxel. Fractional anisotropy is a good vidual who presented with subacute psychosis associated marker of white matter integrity and fractional anisot- with a space-occupying lesion localized in the rostral ropy values modulate the brightness of the vectors. When tectum, within the right SC and PAG. Our functional white matter is intact anisotropic voxels appear bright, connectivity analysis implicates the SC, PAG and left whereas loss of white matter structure gives low frac- amygdala in psychosis. Although our case study cannot tional anisotropy values and thus low brightness vectors. test causality, it is the first study to provide compelling evidence for an association of SC/PAG with a psychotic Resting-State Functional Magnetic Resonance Imaging behavioral phenotype in the absence of any neurologic Analysis disability. It is, however, the second study that reports an association of a tectal lesion with psychosis, with the first Resting-state functional magnetic resonance imaging 38 one described in a young woman who presented with psy- (rs-fMRI) analysis was conducted using CONN toolbox chosis as a result of a quadrigeminal plate lipoma.34 and SPM12 (https://www.fil.ion.ucl.ac.uk/spm/), un- less otherwise stated. The structural T1 scan was brain- extracted using FSL and then coregistered to functional Methods images. Structural and functional images were mapped to Magnetic Resonance Imaging Acquisition Parameters the standardized Montreal Neurological Institute (MNI) Magnetic resonance data from the patient were ac- space. FMRI data were preprocessed to apply motion quired using Philips Medical Systems Achieva-3T. T1 estimation and correction, slice timing correction, out- weighted images were acquired with the following param- lier detection, and spatial Gaussian smoothing. FMRI eters: field of view (FoV) = 24.0 cm, voxel size = 0.94 × data denoising was performed with high-pass filtering 0.94 × 1.20 mm3, slice thickness = 1.20 mm, flip angle to remove low-frequency noise. First-level seed-based (FA) = 10°, time repetition (TR) = 6.23 s, time echo connectivity analysis was performed using correlation (TE) = 3.00 s. Images of diffusion tensor imaging (DTI) coefficient,r . The seed regions, which are the left or right were acquired using echo-planar imaging (EPI) with amygdala and intracalcarine cortex (ICC), were selected 39 parameters: FoV = 22.4 cm, voxel size = 1.75 × 1.75 × on Harvard–Oxford atlas. For each seed region, a cor- 2.0 mm3, slice thickness = 2.00 mm, FA = 90°, TR = 7.39 s, relation map was evaluated by computing r between the TE = 71 ms, number of averages = 1, b = 1000 s/mm2, seed Blood Oxygen Level Dependent (BOLD) signal and number of directions = 30. Functional images were ac- the BOLD signal of all brain voxels. quired using EPI sensitive to blood oxygenation with To identify brain regions with significantly altered func- parameters: FoV = 24.0 cm, voxel size = 3 × 3 × 3 mm3, tional connectivity in the patient, we performed a seed- slice thickness = 3.00 mm, FA = 90°, TR = 2.49 s, to-voxel second-level analysis. We compared our patient TE = 30 ms, and 6-minute scan time length. In the con- (60 years old) with a group of 10 sex- and age-matched trol group, data were acquired
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