Advertisement

Neural correlates of binocular depth inversion illusion in antipsychotic-naïve first-episode schizophrenia patients

  • Cathrin Rohleder
  • Dagmar Koethe
  • Stefan Fritze
  • Cristina E. Topor
  • F. Markus Leweke
  • Dusan HirjakEmail author
Original Paper

Abstract

Objectives

Binocular depth inversion illusion (BDII), a visual, ‘top–down’-driven information process, is impaired in schizophrenia and particularly in its early stages. BDII is a sensitive measure of impaired visual information processing and represents a valid diagnostic tool for schizophrenia and other psychotic disorders. However, neurobiological underpinnings of aberrant BDII in first-episode schizophrenia are largely unknown at present.

Methods

In this study, 22 right-handed, first-episode, antipsychotic-naïve schizophrenia patients underwent BDII assessment and MRI scanning at 1.5 T. The surface-based analysis via new version of Freesurfer (6.0) enabled calculation of cortical thickness and surface area. BDII total and faces scores were related to the two distinct cortical measurements.

Results

We found a significant correlation between BDII performance and cortical thickness in the inferior frontal gyrus and middle temporal gyrus (p < 0.003, Bonferroni corr.), as well as superior parietal gyrus, postcentral gyrus, supramarginal gyrus, and precentral gyrus (p < 0.05, CWP corr.), respectively. BDII performance was significantly correlated with surface area in the superior parietal gyrus and right postcentral gyrus (p < 0.003, Bonferroni corr.).

Conclusion

BDII performance may be linked to cortical thickness and surface area variations in regions involved in “adaptive” or “top–down” modulation and stimulus processing, i.e., frontal and parietal lobes. Our results suggest that cortical features of distinct evolutionary and genetic origin differently contribute to BDII performance in first-episode, antipsychotic-naïve schizophrenia patients.

Keywords

Depth inversion illusion (DII) MRI Schizophrenia Perception Cortex FreeSurfer 

Notes

Acknowledgements

We thank Kristina Gawlik for technical support. We are grateful to all the participants and their families for their time and interest in this study.

Funding

The authors have declared that there is no funding of this study.

Compliance with ethical standards

Conflict of interest

The authors have declared that there are no conflicts of interest in relation to the subject of this study.

Ethical standards

This study has been approved by the appropriate ethics committee and has, therefore, been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

References

  1. 1.
    Adolphs R (2002) Neural systems for recognizing emotion. Curr Opin Neurobiol 12:169–177PubMedCrossRefGoogle Scholar
  2. 2.
    Adolphs R (2002) Recognizing emotion from facial expressions: psychological and neurological mechanisms. Behav Cogn Neurosci Rev 1:21–62CrossRefGoogle Scholar
  3. 3.
    Andreasen NC, Flashman L, Flaum M, Arndt S, Swayze V 2nd, O’Leary DS, Ehrhardt JC, Yuh WT (1994) Regional brain abnormalities in schizophrenia measured with magnetic resonance imaging. JAMA 272:1763–1769PubMedCrossRefGoogle Scholar
  4. 4.
    Bernard JA, Orr JM, Mittal VA (2017) Cerebello-thalamo-cortical networks predict positive symptom progression in individuals at ultra-high risk for psychosis. NeuroImage Clin 14:622–628PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Binder J (1997) Functional magnetic resonance imaging. Language mapping. Neurosurg Clin N Am 8:383–392PubMedCrossRefGoogle Scholar
  6. 6.
    Bridge H, Parker AJ (2007) Topographical representation of binocular depth in the human visual cortex using FMRI. J Vis 7(14):15.1–15.14.  https://doi.org/10.1167/7.14.15 CrossRefGoogle Scholar
  7. 7.
    Buchy L, Barbato M, Makowski C, Bray S, MacMaster FP, Deighton S, Addington J (2017) Mapping structural covariance networks of facial emotion recognition in early psychosis: a pilot study. Schizophr Res 189:146–152.  https://doi.org/10.1016/j.schres.2017.01.054 CrossRefPubMedGoogle Scholar
  8. 8.
    Calderone DJ, Hoptman MJ, Martinez A, Nair-Collins S, Mauro CJ, Bar M, Javitt DC, Butler PD (2013) Contributions of low and high spatial frequency processing to impaired object recognition circuitry in schizophrenia. Cereb Cortex 23:1849–1858PubMedCrossRefGoogle Scholar
  9. 9.
    Cao H, Dixson L, Meyer-Lindenberg A, Tost H (2016) Functional connectivity measures as schizophrenia intermediate phenotypes: advances, limitations, and future directions. Curr Opin Neurobiol 36:7–14PubMedCrossRefGoogle Scholar
  10. 10.
    Chung MK, Robbins SM, Dalton KM, Davidson RJ, Alexander AL, Evans AC (2005) Cortical thickness analysis in autism with heat kernel smoothing. NeuroImage 25:1256–1265PubMedCrossRefGoogle Scholar
  11. 11.
    Chung MK, Worsley KJ, Robbins S, Paus T, Taylor J, Giedd JN, Rapoport JL, Evans AC (2003) Deformation-based surface morphometry applied to gray matter deformation. NeuroImage 18:198–213PubMedCrossRefGoogle Scholar
  12. 12.
    Collin G, de Reus MA, Cahn W, Hulshoff Pol HE, Kahn RS, van den Heuvel MP (2013) Disturbed grey matter coupling in schizophrenia. Eur Neuropsychopharmacol 23:46–54PubMedCrossRefGoogle Scholar
  13. 13.
    Corbetta M, Miezin FM, Shulman GL, Petersen SE (1993) A pet study of visuospatial attention. J Neurosci 13:1202–1226PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Culham JC, Valyear KF (2006) Human parietal cortex in action. Curr Opin Neurobiol 16:205–212PubMedCrossRefGoogle Scholar
  15. 15.
    Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage 9:179–194PubMedCrossRefGoogle Scholar
  16. 16.
    Davatzikos C, Shen D, Gur RC, Wu X, Liu D, Fan Y, Hughett P, Turetsky BI, Gur RE (2005) Whole-brain morphometric study of schizophrenia revealing a spatially complex set of focal abnormalities. Arch Gen Psychiatry 62:1218–1227PubMedCrossRefGoogle Scholar
  17. 17.
    Dean K, Fearon P, Morgan K, Hutchinson G, Orr K, Chitnis X, Suckling J, Mallet R, Leff J, Jones PB, Murray RM, Dazzan P (2006) Grey matter correlates of minor physical anomalies in the aesop first-episode psychosis study. Br J Psychiatry 189:221–228PubMedCrossRefGoogle Scholar
  18. 18.
    Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on mri scans into gyral based regions of interest. NeuroImage 31:968–980CrossRefGoogle Scholar
  19. 19.
    Dima D, Roiser JP, Dietrich DE, Bonnemann C, Lanfermann H, Emrich HM, Dillo W (2009) Understanding why patients with schizophrenia do not perceive the hollow-mask illusion using dynamic causal modelling. Neuroimage 46:1180–1186PubMedCrossRefGoogle Scholar
  20. 20.
    Dobias JJ, Papathomas TV (2013) Recovering 3-D shape: roles of absolute and relative disparity, retinal size, and viewing distance as studied with reverse-perspective stimuli. Perception 42:430–446PubMedCrossRefGoogle Scholar
  21. 21.
    Doniger GM, Foxe JJ, Murray MM, Higgins BA, Javitt DC (2002) Impaired visual object recognition and dorsal/ventral stream interaction in schizophrenia. Arch Gen Psychiatry 59:1011–1020PubMedCrossRefGoogle Scholar
  22. 22.
    Emrich HM, Weber MM, Wendl A, Zihl J, Von Meyer L, Hanisch W (1991) Reduced binocular depth inversion as an indicator of cannabis-induced censorship impairment. Pharmacol Biochem Behav 40:689–690PubMedCrossRefGoogle Scholar
  23. 23.
    Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97:11050–11055PubMedCrossRefGoogle Scholar
  24. 24.
    Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. NeuroImage 9:195–207PubMedCrossRefGoogle Scholar
  25. 25.
    Fischl B, van der Kouwe A, Destrieux C, Halgren E, Segonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D, Caviness V, Makris N, Rosen B, Dale AM (2004) Automatically parcellating the human cerebral cortex. Cereb Cortex 14:11–22PubMedCrossRefGoogle Scholar
  26. 26.
    Fitzsimmons J, Kubicki M, Shenton ME (2013) Review of functional and anatomical brain connectivity findings in schizophrenia. Curr Opin Psychiatry 26(2):172–187.  https://doi.org/10.1097/YCO.0b013e32835d9e6a CrossRefPubMedGoogle Scholar
  27. 27.
    Friston KJ, Worsley KJ, Frackowiak RS, Mazziotta JC, Evans AC (1994) Assessing the significance of focal activations using their spatial extent. Hum Brain Mapp 1:210–220PubMedCrossRefGoogle Scholar
  28. 28.
    Fusar-Poli P, Bhattacharyya S, Allen P, Crippa JA, Borgwardt S, Martin-Santos R, Seal M, O’Carroll C, Atakan Z, Zuardi AW, McGuire P (2010) Effect of image analysis software on neurofunctional activation during processing of emotional human faces. J Clin Neurosci 17:311–314PubMedCrossRefGoogle Scholar
  29. 29.
    Gharabaghi A, Fruhmann Berger M, Tatagiba M, Karnath HO (2006) The role of the right superior temporal gyrus in visual search-insights from intraoperative electrical stimulation. Neuropsychologia 44:2578–2581PubMedCrossRefGoogle Scholar
  30. 30.
    Gong Q, Lui S, Sweeney JA (2016) A selective review of cerebral abnormalities in patients with first-episode schizophrenia before and after treatment. Am J Psychiatry 173(3):232–243PubMedCrossRefGoogle Scholar
  31. 31.
    Gregory RL (1998) Eye and brain. The psychology of seeing. Oxford University Press, OxfordCrossRefGoogle Scholar
  32. 32.
    Gupta T, Silverstein SM, Bernard JA, Keane BP, Papathomas TV, Pelletier-Baldelli A, Dean DJ, Newberry RE, Ristanovic I, Mittal VA (2016) Disruptions in neural connectivity associated with reduced susceptibility to a depth inversion illusion in youth at ultra high risk for psychosis. NeuroImage Clin 12:681–690PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Hagler DJ Jr, Saygin AP, Sereno MI (2006) Smoothing and cluster thresholding for cortical surface-based group analysis of FMRI data. NeuroImage 33:1093–1103PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Hayasaka S, Nichols TE (2003) Validating cluster size inference: random field and permutation methods. NeuroImage 20:2343–2356PubMedCrossRefGoogle Scholar
  35. 35.
    Hirjak D, Huber M, Kirchler E, Kubera KM, Karner M, Sambataro F, Freudenmann RW, Wolf RC (2017) Cortical features of distinct developmental trajectories in patients with delusional infestation. Progress Neuro Psychopharmacol Biol Psychiatry 76:72–79CrossRefGoogle Scholar
  36. 36.
    Hirjak D, Kubera KM, Wolf RC, Thomann AK, Hell SK, Seidl U, Thomann PA (2015) Local brain gyrification as a marker of neurological soft signs in schizophrenia. Behav Brain Res 292:19–25PubMedCrossRefGoogle Scholar
  37. 37.
    Hirjak D, Thomann PA, Wolf RC, Kubera KM, Goch C, Hering J, Maier-Hein KH (2017) White matter microstructure variations contribute to neurological soft signs in healthy adults. Hum Brain Mapp 38:3552–3565PubMedGoogle Scholar
  38. 38.
    Hirjak D, Wolf RC, Kubera KM, Stieltjes B, Thomann PA (2016) Multiparametric mapping of neurological soft signs in healthy adults. Brain Struct Funct 221:1209–1221PubMedCrossRefGoogle Scholar
  39. 39.
    Hirjak D, Wolf RC, Pfeifer B, Kubera KM, Thomann AK, Seidl U, Maier-Hein KH, Schroder J, Thomann PA (2017) Cortical signature of clock drawing performance in alzheimer’s disease and mild cognitive impairment. J Psychiatr Res 90:133–142PubMedCrossRefGoogle Scholar
  40. 40.
    Hirjak D, Wolf RC, Stieltjes B, Hauser T, Seidl U, Schroder J, Thomann PA (2014) Cortical signature of neurological soft signs in recent onset schizophrenia. Brain Topogr 27:296–306PubMedCrossRefGoogle Scholar
  41. 41.
    Hogstrom LJ, Westlye LT, Walhovd KB, Fjell AM (2013) The structure of the cerebral cortex across adult life: age-related patterns of surface area, thickness, and gyrification. Cereb Cortex 23:2521–2530PubMedCrossRefGoogle Scholar
  42. 42.
    Knöchel C, Reuter J, Reinke B, Stäblein M, Marbach K, Feddern R, Kuhlmann K, Alves G, Prvulovic D, Wenzler S, Linden DEJ, Oertel-Knöchel V (2016) Cortical thinning in bipolar disorder and schizophrenia. Schizophr Res 172(1–3):78–85PubMedCrossRefGoogle Scholar
  43. 43.
    Iacoboni M, Molnar-Szakacs I, Gallese V, Buccino G, Mazziotta JC, Rizzolatti G (2005) Grasping the intentions of others with one’s own mirror neuron system. PLoS Biol 3:e79PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Janssen J, Aleman-Gomez Y, Schnack H, Balaban E, Pina-Camacho L, Alfaro-Almagro F, Castro-Fornieles J, Otero S, Baeza I, Moreno D, Bargallo N, Parellada M, Arango C, Desco M (2014) Cortical morphology of adolescents with bipolar disorder and with schizophrenia. Schizophr Res 158:91–99PubMedCrossRefGoogle Scholar
  45. 45.
    Jung WH, Kim JS, Jang JH, Choi JS, Jung MH, Park JY, Han JY, Choi CH, Kang DH, Chung CK, Kwon JS (2011) Cortical thickness reduction in individuals at ultra-high-risk for psychosis. Schizophr Bull 37:839–849PubMedCrossRefGoogle Scholar
  46. 46.
    Karnath HO (2001) New insights into the functions of the superior temporal cortex. Nat Rev Neurosci 2:568–576PubMedCrossRefGoogle Scholar
  47. 47.
    Keane BP, Silverstein SM, Wang Y, Papathomas TV (2013) Reduced depth inversion illusions in schizophrenia are state-specific and occur for multiple object types and viewing conditions. J Abnormal Psychol 122:506–512CrossRefGoogle Scholar
  48. 48.
    Keri S, Janka Z (2004) Critical evaluation of cognitive dysfunctions as endophenotypes of schizophrenia. Acta Psychiatr Scand 110:83–91PubMedCrossRefGoogle Scholar
  49. 49.
    Khan AR, Wang L, Beg MF (2008) Freesurfer-initiated fully-automated subcortical brain segmentation in mri using large deformation diffeomorphic metric mapping. NeuroImage 41:735–746PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Koenigs M, Barbey AK, Postle BR, Grafman J (2009) Superior parietal cortex is critical for the manipulation of information in working memory. J Neurosci 29:14980–14986PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Koethe D, Gerth CW, Neatby MA, Haensel A, Thies M, Schneider U, Emrich HM, Klosterkötter J, Schultze-Lutter F, Leweke FM (2006) Disturbances of visual information processing in early states of psychosis and experimental delta-9-tetrahydrocannabinol altered states of consciousness. Schizophr Res 88:142–150PubMedCrossRefGoogle Scholar
  52. 52.
    Koethe D, Kranaster L, Hoyer C, Gross S, Neatby MA, Schultze-Lutter F, Ruhrmann S, Klosterkötter J, Hellmich M, Leweke FM (2009) Binocular depth inversion as a paradigm of reduced visual information processing in prodromal state, antipsychotic-naïve and treated schizophrenia. Eur Arch Psychiatry Clin Neurosci 259:195PubMedCrossRefGoogle Scholar
  53. 53.
    Lee JS, Park G, Song MJ, Choi KH, Lee SH (2016) Early visual processing for low spatial frequency fearful face is correlated with cortical volume in patients with schizophrenia. Neuropsychiatr Dis Treatm 12:1–14Google Scholar
  54. 54.
    Leweke FM, Giuffrida A, Wurster U, Emrich HM, Piomelli D (1999) Elevated endogenous cannabinoids in schizophrenia. Neuroreport 10:1665–1669PubMedCrossRefGoogle Scholar
  55. 55.
    Leweke FM, Schneider U, Radwan M, Schmidt E, Emrich HM (2000) Different effects of nabilone and cannabidiol on binocular depth inversion in man. Pharmacol Biochem Behav 66:175–181PubMedCrossRefGoogle Scholar
  56. 56.
    Leweke FM, Schneider U, Thies M, Münte TF, Emrich HM (1999) Effects of synthetic δ9-tetrahydrocannabinol on binocular depth inversion of natural and artificial objects in man. Psychopharmacology 142:230–235PubMedCrossRefGoogle Scholar
  57. 57.
    Liu Y, Zhang Y, Lv L, Wu R, Zhao J, Guo W (2017) Abnormal neural activity as a potential biomarker for drug-naive first-episode adolescent-onset schizophrenia with coherence regional homogeneity and support vector machine analyses. Schizophr ResGoogle Scholar
  58. 58.
    Martinez A, Hillyard SA, Bickel S, Dias EC, Butler PD, Javitt DC (2012) Consequences of magnocellular dysfunction on processing attended information in schizophrenia. Cereb Cortex 22:1282–1293PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Martinez A, Hillyard SA, Dias EC, Hagler DJ Jr, Butler PD, Guilfoyle DN, Jalbrzikowski M, Silipo G, Javitt DC (2008) Magnocellular pathway impairment in schizophrenia: evidence from functional magnetic resonance imaging. J Neurosci 28:7492–7500PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    McDonald JH (2015) Handbook of biological statistics. Sparky House Publishing, BaltimoreGoogle Scholar
  61. 61.
    Nachev P, Husain M (2006) Disorders of visual attention and the posterior parietal cortex. Cortex 42:766–773PubMedCrossRefGoogle Scholar
  62. 62.
    Nenadic I, Maitra R, Langbein K, Dietzek M, Lorenz C, Smesny S, Reichenbach JR, Sauer H, Gaser C (2015) Brain structure in schizophrenia vs. psychotic bipolar I disorder: a VBM study. Schizophr Res 165:212–219PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Oostermeijer S, Whittle S, Suo C, Allen NB, Simmons JG, Vijayakumar N, van de Ven PM, Jansen LM, Yucel M, Popma A (2016) Trajectories of adolescent conduct problems in relation to cortical thickness development: a longitudinal MRI study. Transl Psychiatry 6:e841PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Palaniyappan L, Liddle PF (2012) Differential effects of surface area, gyrification and cortical thickness on voxel based morphometric deficits in schizophrenia. NeuroImage 60:693–699PubMedCrossRefGoogle Scholar
  65. 65.
    Phal PM, Usmanov A, Nesbit GM, Anderson JC, Spencer D, Wang P, Helwig JA, Roberts C, Hamilton BE (2008) Qualitative comparison of 3-t and 1.5-t mri in the evaluation of epilepsy. Am J Roentgenol 191:890–895CrossRefGoogle Scholar
  66. 66.
    Pina-Camacho L, Garcia-Prieto J, Parellada M, Castro-Fornieles J, Gonzalez-Pinto AM, Bombin I, Graell M, Paya B, Rapado-Castro M, Janssen J, Baeza I, Del Pozo F, Desco M, Arango C (2015) Predictors of schizophrenia spectrum disorders in early-onset first episodes of psychosis: a support vector machine model. Eur Child Adolesc Psychiatry 24:427–440PubMedCrossRefGoogle Scholar
  67. 67.
    Rakic P (1995) The development of the frontal lobe. A view from the rear of the brain. Adv Neurol 66:1–6 (discussion 6–8) PubMedGoogle Scholar
  68. 68.
    Rakic P (1995) Radial versus tangential migration of neuronal clones in the developing cerebral cortex. Proc Natl Acad Sci USA 92:11323–11327PubMedCrossRefGoogle Scholar
  69. 69.
    Reuter AR, Bumb JM, Mueller JK, Rohleder C, Pahlisch F, Hanke F, Arens E, Leweke FM, Koethe D, Schwarz E (2017) Association of anandamide with altered binocular depth inversion illusion in schizophrenia. World J Biol Psychiatry 18:483–488PubMedCrossRefGoogle Scholar
  70. 70.
    Schaer M, Ottet MC, Scariati E, Dukes D, Franchini M, Eliez S, Glaser B (2013) Decreased frontal gyrification correlates with altered connectivity in children with autism. Front Hum Neurosci 7:750PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Scheperjans F, Grefkes C, Palomero-Gallagher N, Schleicher A, Zilles K (2005) Subdivisions of human parietal area 5 revealed by quantitative receptor autoradiography: a parietal region between motor, somatosensory, and cingulate cortical areas. NeuroImage 25:975–992PubMedCrossRefGoogle Scholar
  72. 72.
    Scheperjans F, Palomero-Gallagher N, Grefkes C, Schleicher A, Zilles K (2005) Transmitter receptors reveal segregation of cortical areas in the human superior parietal cortex: relations to visual and somatosensory regions. NeuroImage 28:362–379PubMedCrossRefGoogle Scholar
  73. 73.
    Schneider U, Borsutzky M, Seifert J, Leweke FM, Huber TJ, Rollnik JD, Emrich HM (2002) Reduced binocular depth inversion in schizophrenic patients. Schizophr Res 53:101–108PubMedCrossRefGoogle Scholar
  74. 74.
    Schultz CC, Koch K, Wagner G, Roebel M, Schachtzabel C, Gaser C, Nenadic I, Reichenbach JR, Sauer H, Schlosser RG (2010) Reduced cortical thickness in first episode schizophrenia. Schizophr Res 116:204–209PubMedCrossRefGoogle Scholar
  75. 75.
    Schultz CC, Nenadic I, Koch K, Wagner G, Roebel M, Schachtzabel C, Muhleisen TW, Nothen MM, Cichon S, Deufel T, Kiehntopf M, Rietschel M, Reichenbach JR, Sauer H, Schlosser RG (2011) Reduced cortical thickness is associated with the glutamatergic regulatory gene risk variant daoa arg30lys in schizophrenia. Neuropsychopharmacology 36:1747–1753PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Schultze-Lutter F, Ruhrmann S, Hoyer C, Klosterkotter J, Leweke FM (2007) The initial prodrome of schizophrenia: different duration, different underlying deficits? Compr Psychiatry 48:479–488PubMedCrossRefGoogle Scholar
  77. 77.
    Segonne F, Dale AM, Busa E, Glessner M, Salat D, Hahn HK, Fischl B (2004) A hybrid approach to the skull stripping problem in mri. NeuroImage 22:1060–1075PubMedCrossRefGoogle Scholar
  78. 78.
    Semple DM, Ramsden F, McIntosh AM (2003) Reduced binocular depth inversion in regular cannabis users. Pharmacol Biochem Behav 75:789–793PubMedCrossRefGoogle Scholar
  79. 79.
    Sheffield JM, Barch DM (2016) Cognition and resting-state functional connectivity in schizophrenia. Neurosci Biobehav Rev 61:108–120PubMedCrossRefGoogle Scholar
  80. 80.
    Sled JG, Zijdenbos AP, Evans AC (1998) A nonparametric method for automatic correction of intensity nonuniformity in mri data. IEEE Trans Med Imaging 17:87–97PubMedCrossRefGoogle Scholar
  81. 81.
    Smith GN, Thornton AE, Lang DJ, MacEwan GW, Kopala LC, Su W, Honer WG (2014) Cortical morphology and early adverse birth events in men with first-episode psychosis. Psychol Med 45(9):1825–1837.  https://doi.org/10.1017/S003329171400292X CrossRefPubMedGoogle Scholar
  82. 82.
    Storsve AB, Fjell AM, Tamnes CK, Westlye LT, Overbye K, Aasland HW, Walhovd KB (2014) Differential longitudinal changes in cortical thickness, surface area and volume across the adult life span: regions of accelerating and decelerating change. J Neurosci 34:8488–8498PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Taylor SF, Kang J, Brege IS, Tso IF, Hosanagar A, Johnson TD (2012) Meta-analysis of functional neuroimaging studies of emotion perception and experience in schizophrenia. Biol Psychiatry 71:136–145PubMedCrossRefGoogle Scholar
  84. 84.
    Thayer RE, Hagerty SL, Sabbineni A, Claus ED, Hutchison KE, Weiland BJ (2016) Negative and interactive effects of sex, aging, and alcohol abuse on gray matter morphometry. Hum Brain Mapp 37:2276–2292PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Uddin LQ, Kaplan JT, Molnar-Szakacs I, Zaidel E, Iacoboni M (2005) Self-face recognition activates a frontoparietal “mirror” network in the right hemisphere: an event-related FMRI study. NeuroImage 25:926–935PubMedCrossRefGoogle Scholar
  86. 86.
    Vijayakumar N, Allen NB, Youssef G, Dennison M, Yucel M, Simmons JG, Whittle S (2016) Brain development during adolescence: a mixed-longitudinal investigation of cortical thickness, surface area, and volume. Hum Brain Mapp 37:2027–2038PubMedCrossRefGoogle Scholar
  87. 87.
    Wang J, Yang Y, Fan L, Xu J, Li C, Liu Y, Fox PT, Eickhoff SB, Yu C, Jiang T (2015) Convergent functional architecture of the superior parietal lobule unraveled with multimodal neuroimaging approaches. Hum Brain Mapp 36:238–257PubMedCrossRefGoogle Scholar
  88. 88.
    Watanuki T, Matsuo K, Egashira K, Nakashima M, Harada K, Nakano M, Matsubara T, Takahashi K, Watanabe Y (2016) Precentral and inferior prefrontal hypoactivation during facial emotion recognition in patients with schizophrenia: a functional near-infrared spectroscopy study. Schizophr Res 170:109–114PubMedCrossRefGoogle Scholar
  89. 89.
    Woo CW, Krishnan A, Wager TD (2014) Cluster-extent based thresholding in FMRI analyses: pitfalls and recommendations. NeuroImage 91:412–419PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Yuan X, Han Y, Wei Y, Xia M, Sheng C, Jia J, He Y (2016) Regional homogeneity changes in amnestic mild cognitive impairment patients. Neurosci Lett 629:1–8PubMedCrossRefGoogle Scholar
  91. 91.
    Zilles K, Palomero-Gallagher N, Amunts K (2013) Development of cortical folding during evolution and ontogeny. Trends Neurosci 36:275–284PubMedCrossRefGoogle Scholar
  92. 92.
    Zipursky RB, Lim KO, Sullivan EV, Brown BW, Pfefferbaum A (1992) Widespread cerebral gray matter volume deficits in schizophrenia. Arch Gen Psychiatry 49:195–205PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Cathrin Rohleder
    • 1
    • 2
  • Dagmar Koethe
    • 3
    • 4
  • Stefan Fritze
    • 1
  • Cristina E. Topor
    • 1
  • F. Markus Leweke
    • 1
    • 4
  • Dusan Hirjak
    • 1
    Email author
  1. 1.Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty MannheimHeidelberg UniversityMannheimGermany
  2. 2.Institute of Radiochemistry and Experimental Molecular ImagingUniversity Hospital of CologneCologneGermany
  3. 3.Department of Psychosomatic Medicine and Psychotherapy, Central Institute of Mental Health, Medical Faculty MannheimHeidelberg UniversityMannheimGermany
  4. 4.Brain and Mind CentreUniversity of SydneySydneyAustralia

Personalised recommendations