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Neuroimaging auditory verbal hallucinations in schizophrenia patient and healthy populations

Published online by Cambridge University Press:  14 February 2019

Maria Angelique Di Biase Open the ORCID record for Maria Angelique Di Biase [Opens in a new window] ,
Fan Zhang ,
Amanda Lyall ,
Marek Kubicki ,
René C. W. Mandl ,
Iris E. Sommer  and
Ofer Pasternak
Maria Angelique Di Biase*
Affiliation:
Department of Psychiatry, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA
Fan Zhang
Affiliation:
Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA
Amanda Lyall
Affiliation:
Department of Psychiatry, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts, USA
Marek Kubicki
Affiliation:
Department of Psychiatry, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts, USA
René C. W. Mandl
Affiliation:
Department of Psychiatry, UMC Utrecht Brain Center, Utrecht, The Netherlands CNSR, Mental Health Center Glostrup, Glostrup, Denmark
Iris E. Sommer
Affiliation:
Department of Neuroscience, Rijksuniversiteit Groningen (RUG), University Medical Center Groningen, Antonie Deusinglaan 2 Groningen, The Netherlands
Ofer Pasternak
Affiliation:
Department of Psychiatry, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA
*
Author for correspondence: Maria Angelique Di Biase, E-mail: mdibiase1@bwh.harvard.edu
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Abstract

Background

Auditory verbal hallucinations (AVH) are a cardinal feature of schizophrenia, but they can also appear in otherwise healthy individuals. Imaging studies implicate language networks in the generation of AVH; however, it remains unclear if alterations reflect biologic substrates of AVH, irrespective of diagnostic status, age, or illness-related factors. We applied multimodal imaging to identify AVH-specific pathology, evidenced by overlapping gray or white matter deficits between schizophrenia patients and healthy voice-hearers.

Methods

Diffusion-weighted and T1-weighted magnetic resonance images were acquired in 35 schizophrenia patients with AVH (SCZ-AVH), 32 healthy voice-hearers (H-AVH), and 40 age- and sex-matched controls without AVH. White matter fractional anisotropy (FA) and gray matter thickness (GMT) were computed for each region comprising ICBM-DTI and Desikan–Killiany atlases, respectively. Regions were tested for significant alterations affecting both SCZ-AVH and H-AVH groups, relative to controls.

Results

Compared with controls, the SCZ-AVH showed widespread FA and GMT reductions; but no significant differences emerged between H-AVH and control groups. While no overlapping pathology appeared in the overall study groups, younger (<40 years) H-AVH and SCZ-AVH subjects displayed overlapping FA deficits across four regions (p < 0.05): the genu and splenium of the corpus callosum, as well as the anterior limbs of the internal capsule. Analyzing these regions with free-water imaging ascribed overlapping FA abnormalities to tissue-specific anisotropy changes.

Conclusions

We identified white matter pathology associated with the presence of AVH, independent of diagnostic status. However, commonalities were constrained to younger and more homogenous groups, after reducing pathologic variance associated with advancing age and chronicity effects.

Keywords

Agechronicitycortical thicknessdiffusion MRIfree-watergray matter thicknesspsychosissymptom dimensionstissue-specific fractional anisotropy
Type
Original Articles
Information
Psychological Medicine , Volume 50 , Issue 3 , February 2020 , pp. 403 - 412
Copyright
Copyright © Cambridge University Press 2019

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Footnotes

*

These authors contributed equally and share senior authorship

References

Agerbo, E, Sullivan, PF, Vilhjalmsson, BJ, Pedersen, CB, Mors, O, Børglum, AD, Hougaard, DM, Hollegaard, MV, Meier, S and Mattheisen, M (2015) Polygenic risk score, parental socioeconomic status, family history of psychiatric disorders, and the risk for schizophrenia: a Danish population-based study and meta-analysis. JAMA Psychiatry 72, 635–641.CrossRefGoogle ScholarPubMed
Allen, P, Larøi, F, McGuire, PK and Aleman, A (2008) The hallucinating brain: a review of structural and functional neuroimaging studies of hallucinations. Neuroscience & Biobehavioral Reviews 32, 175–191.CrossRefGoogle ScholarPubMed
Andersson, J, Jenkinson, M and Smith, S (2007) Non-Linear Optimisation. FMRIB Technical Report. Available at http://www.fmrib.ox.ac.uk/analysis/techrep (Accessed 15 August 2018).Google Scholar
Andersson, J, Jenkinson, M and Smith, S (2010) Non-Linear Registration, Aka Spatial Normalisation. Available at http://www.fmrib.ox.ac.uk/analysis/techrep (Accessed 15 August 2018).Google Scholar
Andreasen, NC, Flaum, M and Arndt, S (1992) The comprehensive assessment of symptoms and history (CASH): an instrument for assessing diagnosis and psychopathology. Archives of General Psychiatry 49, 615–623.CrossRefGoogle ScholarPubMed
Baumeister, D, Sedgwick, O, Howes, O and Peters, E (2017) Auditory verbal hallucinations and continuum models of psychosis: a systematic review of the healthy voice-hearer literature. Clinical Psychology Review 51, 125–141.CrossRefGoogle ScholarPubMed
Bellebaum, C, Daum, I, Koch, B, Schwarz, M and Hoffmann, K-P (2005) The role of the human thalamus in processing corollary discharge. Brain 128, 1139–1154.CrossRefGoogle ScholarPubMed
Benjamini, Y and Heller, R (2007) False discovery rates for spatial signals. Journal of the American Statistical Association 102, 1272–1281.CrossRefGoogle Scholar
Catani, M and Ffytche, DH (2005) The rises and falls of disconnection syndromes. Brain 128, 2224–2239.CrossRefGoogle ScholarPubMed
Catani, M, Craig, MC, Forkel, SJ, Kanaan, R, Picchioni, M, Toulopoulou, T, Shergill, S, Williams, S, Murphy, DG and McGuire, P (2011) Altered integrity of perisylvian language pathways in schizophrenia: relationship to auditory hallucinations. Biological Psychiatry 70, 1143–1150.CrossRefGoogle ScholarPubMed
Claridge, G and Beech, T (1995) Fully and quasi-dimensional constructions of schizotypy. In Raine, A, Lencz, T and Mednick, SA (eds), Schizotypal Personality. Melbourne: Press Syndicate of the University of Cambridge, pp. 192–216.CrossRefGoogle Scholar
Colby, CL, Berman, RA, Heiser, LM and Saunders, RC (2005) Corollary discharge and spatial updating: when the brain is split, is space still unified? Progress in Brain Research 149, 187–205.CrossRefGoogle ScholarPubMed
Cropley, VL, Klauser, P, Lenroot, RK, Bruggemann, J, Sundram, S, Bousman, C, Pereira, A, Di Biase, MA, Weickert, TW, Weickert, CS, Pantelis, C and Zalesky, A (2016) Accelerated gray and white matter deterioration with age in schizophrenia. American Journal of Psychiatry 174, 286–295.CrossRefGoogle Scholar
Ćurčić-Blake, B, Nanetti, L, van der Meer, L, Cerliani, L, Renken, R, Pijnenborg, GH and Aleman, A (2015) Not on speaking terms: hallucinations and structural network disconnectivity in schizophrenia. Brain Structure and Function 220, 407–418.CrossRefGoogle Scholar
Daalman, K, Boks, M, Diederen, K, de Weijer, AD, Blom, JD, Kahn, RS and Sommer, I (2011) The same or different? A phenomenological comparison of auditory verbal hallucinations in healthy and psychotic individuals. Journal of Clinical Psychiatry 72, 320–325.CrossRefGoogle ScholarPubMed
Daalman, K, Diederen, K, Derks, EM, van Lutterveld, R, Kahn, RS and Sommer, IE (2012) Childhood trauma and auditory verbal hallucinations. Psychological Medicine 42, 2475–2484.CrossRefGoogle ScholarPubMed
Dale, AM, Fischl, B and Sereno, MI (1999) Cortical surface-based analysis: I. Segmentation and surface reconstruction. NeuroImage 9, 179–194.CrossRefGoogle ScholarPubMed
Desikan, RS, Ségonne, F, Fischl, B, Quinn, BT, Dickerson, BC, Blacker, D, Buckner, RL, Dale, AM, Maguire, RP and Hyman, BT (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31, 968–980.CrossRefGoogle ScholarPubMed
de Weijer, A, Mandl, R, Diederen, K, Neggers, S, Kahn, R, Pol, HH and Sommer, I (2011) Microstructural alterations of the arcuate fasciculus in schizophrenia patients with frequent auditory verbal hallucinations. Schizophrenia Research 130, 68–77.CrossRefGoogle ScholarPubMed
de Weijer, AD, Neggers, SF, Diederen, K, Mandl, RC, Kahn, RS, Pol, H, Hilleke, E and Sommer, IE (2013) Aberrations in the arcuate fasciculus are associated with auditory verbal hallucinations in psychotic and in non-psychotic individuals. Human Brain Mapping 34, 626–634.Google ScholarPubMed
Di Biase, MA, Cropley, VL, Baune, BT, Olver, J, Amminger, GP, Phassouliotis, C, Bousman, C, McGorry, PD, Everall, I, Pantelis, C and Zalesky, A (2017) White matter connectivity disruptions in early and chronic schizophrenia. Psychological Medicine 1–14.Google ScholarPubMed
Di Biase, MA, Cropley, VL, Cocchi, L, Fornito, A, Calamante, F, Ganella, EP, Pantelis, C and Zalesky, A (2018) Linking cortical and connectional pathology in schizophrenia. Schizophrenia Bulletin sby121.CrossRefGoogle Scholar
Edwards, TJ, Sherr, EH, Barkovich, AJ and Richards, LJ (2014) Clinical, genetic and imaging findings identify new causes for corpus callosum development syndromes. Brain 137, 1579–1613.CrossRefGoogle ScholarPubMed
First, MB and Gibbon, M (2004) The structured clinical interview for DSM-IV axis I disorders (SCID-I) and the structured clinical interview for DSM-IV axis II disorders (SCID-II). In Hersen, M, Haynes, SN, Goldstein, G, Heiby, EM, Hilsenroth, MJ, Beers, SR, Segal, DL and Thomas, JC (eds), Comprehensive Handbook of Psychological Assessment. New Jersey: John Wiley & Sons Inc., pp. 134–143.Google Scholar
Fischl, B and Dale, AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences 97, 11050–11055.CrossRefGoogle ScholarPubMed
Fischl, B, Sereno, MI and Dale, AM (1999) Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. NeuroImage 9, 195–207.CrossRefGoogle Scholar
Fischl, B, Salat, DH, Busa, E, Albert, M, Dieterich, M, Haselgrove, C, Van Der Kouwe, A, Killiany, R, Kennedy, D and Klaveness, S (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341–355.CrossRefGoogle ScholarPubMed
Fischl, B, van der Kouwe, A, Destrieux, C, Halgren, E, Ségonne, F, Salat, DH, Busa, E, Seidman, LJ, Goldstein, J and Kennedy, D (2004) Automatically parcellating the human cerebral cortex. Cerebral Cortex 14, 11–22.CrossRefGoogle ScholarPubMed
Ford, JM, Morris, SE, Hoffman, RE, Sommer, I, Waters, F, McCarthy-Jones, S, Thoma, RJ, Turner, JA, Keedy, SK and Badcock, JC (2014) Studying hallucinations within the NIMH RDoC framework. Schizophrenia Bulletin 40, S295–S304.CrossRefGoogle ScholarPubMed
Friederici, AD, von Cramon, DY and Kotz, SA (2007) Role of the corpus callosum in speech comprehension: interfacing syntax and prosody. Neuron 53, 135–145.CrossRefGoogle ScholarPubMed
Fusar-Poli, P, Tantardini, M, De Simone, S, Ramella-Cravaro, V, Oliver, D, Kingdon, J, Kotlicka-Antczak, M, Valmaggia, L, Lee, J, Millan, MJ, Galderisi, S, Balottin, U, Ricca, V and McGuire, P (2017) Deconstructing vulnerability for psychosis: meta-analysis of environmental risk factors for psychosis in subjects at ultra high-risk. European Psychiatry 40, 65–75.CrossRefGoogle ScholarPubMed
Haddock, G, McCarron, J, Tarrier, N and Faragher, E (1999) Scales to measure dimensions of hallucinations and delusions: the psychotic symptom rating scales (PSYRATS). Psychological Medicine 29, 879–889.CrossRefGoogle Scholar
Hinkley, LBN, Marco, EJ, Findlay, AM, Honma, S, Jeremy, RJ, Strominger, Z, Bukshpun, P, Wakahiro, M, Brown, WS, Paul, LK, Barkovich, AJ, Mukherjee, P, Nagarajan, SS and Sherr, EH (2012) The role of corpus callosum development in functional connectivity and cognitive processing. PLoS ONE 7, e39804.CrossRefGoogle ScholarPubMed
Hubl, D, Koenig, T, Strik, W, Federspiel, A, Kreis, R, Boesch, C, Maier, SE, Schroth, G, Lovblad, K and Dierks, T (2004) Pathways that make voices: white matter changes in auditory hallucinations. Archives of General Psychiatry 61, 658–668.CrossRefGoogle ScholarPubMed
Hugdahl, K, Løberg, E-M, Specht, K, Steen, VM, van Wageningen, H and Jørgensen, HA (2008) Auditory hallucinations in schizophrenia: the role of cognitive, brain structural and genetic disturbances in the left temporal lobe. Frontiers in Human Neuroscience 1, 6–6.CrossRefGoogle ScholarPubMed
Iacobucci, D, Posavac, SS, Kardes, FR, Schneider, MJ and Popovich, DL (2015) The median split: robust, refined, and revived. Journal of Consumer Psychology 25, 690–704.CrossRefGoogle Scholar
Jackowski, AP, Douglas-Palumberi, H, Jackowski, M, Win, L, Schultz, RT, Staib, LW, Krystal, JH and Kaufman, J (2008) Corpus callosum in maltreated children with posttraumatic stress disorder: a diffusion tensor imaging study. Psychiatry Research: Neuroimaging 162, 256–261.CrossRefGoogle ScholarPubMed
Jahanshad, N, Kochunov, PV, Sprooten, E, Mandl, RC, Nichols, TE, Almasy, L, Blangero, J, Brouwer, RM, Curran, JE, de Zubicaray, GI, Duggirala, R, Fox, PT, Hong, LE, Landman, BA, Martin, NG, McMahon, KL, Medland, SE, Mitchell, BD, Olvera, RL, Peterson, CP, Starr, JM, Sussmann, JE, Toga, AW, Wardlaw, JM, Wright, MJ, Hulshoff Pol, HE, Bastin, ME, McIntosh, AM, Deary, IJ, Thompson, PM and Glahn, DC (2013) Multi-site genetic analysis of diffusion images and voxelwise heritability analysis: a pilot project of the ENIGMA-DTI working group. NeuroImage 81, 455–469.CrossRefGoogle ScholarPubMed
Jenkinson, M, Beckmann, CF, Behrens, TE, Woolrich, MW and Smith, SM (2012) FSL. NeuroImage 62, 782–790.CrossRefGoogle ScholarPubMed
Jones, DK, Catani, M, Pierpaoli, C, Reeves, SJ, Shergill, SS, O'sullivan, M, Golesworthy, P, McGuire, P, Horsfield, MA and Simmons, A (2006) Age effects on diffusion tensor magnetic resonance imaging tractography measures of frontal cortex connections in schizophrenia. Human Brain Mapping 27, 230–238.CrossRefGoogle Scholar
Kay, SR, Flszbein, A and Opfer, LA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276.CrossRefGoogle Scholar
Kubicki, M, Alvarado, JL, Westin, C-F, Tate, DF, Markant, D, Terry, DP, Whitford, TJ, De Siebenthal, J, Bouix, S, McCarley, RW, Kikinis, R and Shenton, ME (2011) Stochastic tractography study of inferior frontal gyrus anatomical connectivity in schizophrenia. NeuroImage 55, 1657–1664.CrossRefGoogle Scholar
Kühn, S and Gallinat, J (2012) Quantitative meta-analysis on state and trait aspects of auditory verbal hallucinations in schizophrenia. Schizophrenia Bulletin 38, 779–786.CrossRefGoogle Scholar
Larøi, F (2012) How do auditory verbal hallucinations in patients differ from those in non-patients? Frontiers in Human Neuroscience 6, 1–9.CrossRefGoogle ScholarPubMed
Larøi, F, Marczewski, P and Van der Linden, M (2004) Further evidence of the multi-dimensionality of hallucinatory predisposition: factor structure of a modified version of the Launay-Slade Hallucinations Scale in a normal sample. European Psychiatry 19, 15–20.CrossRefGoogle Scholar
Lyall, A, Pasternak, O, Robinson, D, Newell, D, Trampush, J, Gallego, J, Fava, M, Malhotra, A, Karlsgodt, K and Kubicki, M (2017) Greater extracellular free-water in first-episode psychosis predicts better neurocognitive functioning. Molecular Psychiatry 23, 701–707.CrossRefGoogle ScholarPubMed
Mathalon, DH and Ford, JM (2008) Corollary discharge dysfunction in schizophrenia: evidence for an elemental deficit. Clinical EEG and Neuroscience 39, 82–86.CrossRefGoogle ScholarPubMed
McGrath, JJ, Saha, S, Al-Hamzawi, AO, Alonso, J, Andrade, L, Borges, G, Bromet, EJ, Oakley Browne, M, Bruffaerts, R, Caldas de Almeida, JM, Fayyad, J, Florescu, S, de Girolamo, G, Gureje, O, Hu, C, de Jonge, P, Kovess-Masfety, V, Lepine, JP, Lim, CCW, Navarro-Mateu, F, Piazza, M, Sampson, N, Posada-Villa, J, Kendler, KS and Kessler, RC (2016) Age of onset and lifetime projected risk of psychotic experiences: cross-national data from the world mental health survey. Schizophrenia Bulletin 42, 933–941.CrossRefGoogle ScholarPubMed
Mori, S, Wakana, S, Van Zijl, PC and Nagae-Poetscher, L (2005) MRI Atlas of Human White Matter. Amsterdam: Elsevier.Google Scholar
Mulert, C, Kirsch, V, Whitford, TJ, Alvarado, J, Pelavin, P, McCarley, RW, Kubicki, M, Salisbury, DF and Shenton, ME (2012) Hearing voices: a role of interhemispheric auditory connectivity? The World Journal of Biological Psychiatry 13, 153–158.CrossRefGoogle ScholarPubMed
O'Donnell, LJ and Pasternak, O (2015) Does diffusion MRI tell us anything about the white matter? An overview of methods and pitfalls. Schizophrenia Research 161, 133–141.CrossRefGoogle ScholarPubMed
Oestreich, LK, McCarthy-Jones, S and Whitford, TJ (2016) Decreased integrity of the fronto-temporal fibers of the left inferior occipito-frontal fasciculus associated with auditory verbal hallucinations in schizophrenia. Brain Imaging and Behavior 10, 445–454.CrossRefGoogle Scholar
Oestreich, LK, Lyall, AE, Pasternak, O, Kikinis, Z, Newell, DT, Savadjiev, P, Bouix, S, Shenton, ME, Kubicki, M, Whitford, TJ and McCarthy-Jones, S (2017) Characterizing white matter changes in chronic schizophrenia: a free-water imaging multi-site study. Schizophrenia Research 189, 153–161.CrossRefGoogle ScholarPubMed
Palaniyappan, L, Balain, V, Radua, J and Liddle, PF (2012) Structural correlates of auditory hallucinations in schizophrenia: a meta-analysis. Schizophrenia Research 137, 169–173.CrossRefGoogle ScholarPubMed
Pasternak, O, Sochen, N, Gur, Y, Intrator, N and Assaf, Y (2009) Free water elimination and mapping from diffusion MRI. Magnetic Resonance in Medicine 62, 717–730.CrossRefGoogle ScholarPubMed
Pasternak, O, Westin, C-F, Bouix, S, Seidman, LJ, Goldstein, JM, Woo, T-UW, Petryshen, TL, Mesholam-Gately, RI, McCarley, RW, Kikinis, R, Shenton, ME and Kubicki, M (2012) Excessive extracellular volume reveals a neurodegenerative pattern in schizophrenia onset. The Journal of Neuroscience 32, 17365–17372.CrossRefGoogle ScholarPubMed
Pasternak, O, Westin, CF, Dahlben, B, Bouix, S and Kubicki, M (2015) The extent of diffusion MRI markers of neuroinflammation and white matter deterioration in chronic schizophrenia. Schizophrenia Research 161, 113–118.CrossRefGoogle ScholarPubMed
Pasternak, O, Kubicki, M and Shenton, ME (2016) In vivo imaging of neuroinflammation in schizophrenia. Schizophrenia Research 173, 200–212.CrossRefGoogle Scholar
Penfield, W and Perot, P (1963) The brain's record of auditory and visual experience: a final summary and discussion. Brain 86, 595–696.CrossRefGoogle ScholarPubMed
Psomiades, M, Fonteneau, C, Mondino, M, Luck, D, Haesebaert, F, Suaud-Chagny, M-F and Brunelin, J (2016) Integrity of the arcuate fasciculus in patients with schizophrenia with auditory verbal hallucinations: a DTI-tractography study. NeuroImage: Clinical 12, 970–975.CrossRefGoogle ScholarPubMed
Schnack, HG, van Haren, NEM, Nieuwenhuis, M, Hulshoff Pol, HE, Cahn, W and Kahn, RS (2016) Accelerated brain aging in schizophrenia: a longitudinal pattern recognition study. American Journal of Psychiatry 173, 607–616.CrossRefGoogle ScholarPubMed
Seok, J-H, Park, H-J, Chun, J-W, Lee, S-K, Cho, HS, Kwon, JS and Kim, J-J (2007) White matter abnormalities associated with auditory hallucinations in schizophrenia: a combined study of voxel-based analyses of diffusion tensor imaging and structural magnetic resonance imaging. Psychiatry Research: Neuroimaging 156, 93–104.CrossRefGoogle ScholarPubMed
Smith, SM, Jenkinson, M, Johansen-Berg, H, Rueckert, D, Nichols, TE, Mackay, CE, Watkins, KE, Ciccarelli, O, Cader, MZ, Matthews, PM and Behrens, TE (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 31, 1487–1505.CrossRefGoogle ScholarPubMed
Sommer, IE, Daalman, K, Rietkerk, T, Diederen, KM, Bakker, S, Wijkstra, J and Boks, MP (2010) Healthy individuals with auditory verbal hallucinations; who are they? Psychiatric assessments of a selected sample of 103 subjects. Schizophrenia Bulletin 36, 633–641.CrossRefGoogle ScholarPubMed
Stephan, KE, Friston, KJ and Frith, D (2009) Disconnection in schizophrenia: from abnormal synaptic plasticity to failures of self-monitoring. Schizophrenia Bulletin 35, 509–527.CrossRefGoogle Scholar
Uranova, NA, Vikhreva, OV, Rachmanova, VI and Orlovskaya, DD (2011) Ultrastructural alterations of myelinated fibers and oligodendrocytes in the prefrontal cortex in schizophrenia: a postmortem morphometric study. Schizophrenia Research and Treatment 2011, 1–13.CrossRefGoogle ScholarPubMed
Uranova, NA, Vikhreva, OV, Rachmanova, VI and Orlovskaya, DD (2014) Microglial activation in white matter in schizophrenia: findings from a postmortem electron microscopic morphometric study. Neurology, Psychiatry and Brain Research 20, 25.CrossRefGoogle Scholar
van Swam, C, Federspiel, A, Hubl, D, Wiest, R, Boesch, C, Vermathen, P, Kreis, R, Strik, W and Dierks, T (2012) Possible dysregulation of cortical plasticity in auditory verbal hallucinations – a cortical thickness study in schizophrenia. Journal of Psychiatric Research 46, 1015–1023.CrossRefGoogle Scholar
Westerhausen, R and Hugdahl, K (2008) The corpus callosum in dichotic listening studies of hemispheric asymmetry: a review of clinical and experimental evidence. Neuroscience & Biobehavioral Reviews 32, 1044–1054.CrossRefGoogle ScholarPubMed
Westlye, LT, Walhovd, KB, Dale, AM, Bjørnerud, A, Due-Tønnessen, P, Engvig, A, Grydeland, H, Tamnes, CK, Østby, Y and Fjell, AM (2009) Life-span changes of the human brain white matter: diffusion tensor imaging (DTI) and volumetry. Cerebral Cortex 20, 2055–2068.CrossRefGoogle ScholarPubMed
Whitford, TJ, Ford, JM, Mathalon, DH, Kubicki, M and Shenton, ME (2010 a) Schizophrenia, myelination, and delayed corollary discharges: a hypothesis. Schizophrenia Bulletin 38, 486–494.CrossRefGoogle ScholarPubMed
Whitford, TJ, Kubicki, M, Schneiderman, JS, O'Donnell, LJ, King, R, Alvarado, JL, Khan, U, Markant, D, Nestor, PG, Niznikiewicz, M, McCarley, RW, Westin, C-F and Shenton, ME (2010 b) Corpus callosum abnormalities and their association with psychotic symptoms in patients with schizophrenia. Biological Psychiatry 68, 70–77.CrossRefGoogle ScholarPubMed
Whitford, TJ, Mathalon, DH, Shenton, ME, Roach, BJ, Bammer, R, Adcock, RA, Bouix, S, Kubicki, M, De Siebenthal, J, Rausch, AC, Schneiderman, JS and Ford, JM (2011) Electrophysiological and diffusion tensor imaging evidence of delayed corollary discharges in patients with schizophrenia. Psychological Medicine 41, 959–969.CrossRefGoogle ScholarPubMed
Woodward, TS, Jung, K, Hwang, H, Yin, J, Taylor, L, Menon, M, Peters, E, Kuipers, E, Waters, F and Lecomte, T (2014) Symptom dimensions of the psychotic symptom rating scales in psychosis: a multisite study. Schizophrenia Bulletin 40, S265–S274.CrossRefGoogle ScholarPubMed
Xi, Y-B, Guo, F, Li, H, Chang, X, Sun, J-B, Zhu, Y-Q, Liu, W-M, Cui, L-B, Chen, G and Wang, H-N (2016) The structural connectivity pathology of first-episode schizophrenia based on the cardinal symptom of auditory verbal hallucinations. Psychiatry Research: Neuroimaging 257, 25–30.CrossRefGoogle ScholarPubMed
Yung, AR, Buckby, JA, Cotton, SM, Cosgrave, EM, Killackey, EJ, Stanford, C, Godfrey, K and McGorry, PD (2005) Psychotic-like experiences in nonpsychotic help-seekers: associations with distress, depression, and disability. Schizophrenia Bulletin 32, 352–359.CrossRefGoogle ScholarPubMed
Zhang, X, Gao, J, Zhu, F, Wang, W, Fan, Y, Ma, Q, Ma, X and Yang, J (2018) Reduced white matter connectivity associated with auditory verbal hallucinations in first-episode and chronic schizophrenia: a diffusion tensor imaging study. Psychiatry Research: Neuroimaging 273, 63–70.CrossRefGoogle ScholarPubMed
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