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Neural functional correlates of emotional processing in patients with first-episode psychoses: an activation likelihood estimation (ALE) meta-analysis

A. Del Casale, C. Rapinesi, G. D. Kotzalidis, S. Ferracuti, A. Padovano, C. Grassi, G. Sani, P. Girardi, M. Pompili

Abstract


Background. Early emotional recognition impairment characterises rst-episode psychoses (FEP) and remains stable thereafter. Patients with FEP consistently show brain activation changes during emotional processing in functional neuroimaging studies.
Aim and Methods. To identify and compare cerebral activation correlates of FEP patients and healthy controls (HCs) during emotional task performances, we performed an Activation Likelihood Estimation (ALE) meta-analysis of peer-reviewed functional magnetic resonance imaging (fMRI) studies.

Results. Five studies included 71 patients with FEP and 75 HCs. Within-group analyses showed that HCs activated during emotional task performance the bilateral inferior parietal lobule (BAs 39 and 40), left inferior frontal gyrus (BAs 9 and 47), right amygdala, left middle frontal gyrus (BA 9), right cingulate gyrus (BA 32), and right middle temporal gyrus (BA 21). FEP activations correlating with emotional tasks included the right cuneus (BA 17) and right angular gyrus (BA 39).

Conclusions. During emotional task performance, FEP patients fail to activate an extensive brain network comprising emotional processing-related areas, including both cortical and subcortical areas.


Keywords


First episode psychoses; Emotional processing; Right parietal cortex; Left dorsolateral prefrontal cortex; Left cingulate cortex

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References


Anilkumar A.P., Kumari V., Mehrotra R., Aasen I., Mitterschiffthaler M.T., Sharma T. An fMRI study of face encoding and recognition in first-episode schizophrenia. Acta Neuropsychiatr., 20: 129-138, 2008.

Baldwin P., Browne D., Scully P.J., Quinn J.F., Morgan M.G., Kinsella A., Owens J.M., Russell V., O'Callaghan E., Waddington J.L. Epidemiology of first-episode psychosis: illustrating the challenges across diagnostic boundaries through the Cavan-Monaghan study at 8 years. Schizophr. Bull., 31: 624-638, 2005.

Barkl SJ., Lah S., Harris A.W., Williams L.M. Facial emotion identification in early-onset and first-episode psychosis: a systematic review with meta-analysis. Schizophr. Res., 159: 62-69, 2014.

Bastos-Leite A.J., Ridgway G.R., Silveira C., Norton A., Reis S., Friston K.J. Dysconnectivity within the default mode in first-episode schizophrenia: a stochastic dynamic causal modeling study with functional magnetic resonance imaging. Schizophr. Bull., 41: 144-153, 2015.

Bediou B., Asri F., Brunelin J., Krolak-Salmon P., D'Amato T., Saoud M., Tazi I. Emotion recognition and genetic vulnerability to schizophrenia. Br. J. Psychiatry, 191: 126-130, 2007.

Bergé D., Carmona S., Salgado P., Rovira M., Bulbena A., Vilarroya O. Limbic activity in antipsychotic naïve first-episode psychotic subjects during facial emotion discrimination. Eur. Arch. Psychiatry Clin. Neurosci., 264: 271-283, 2014.

Bertrand M.C., Achim A.M., Harvey P.O., Sutton H., Malla A.K., Lepage M. Structural neural correlates of impairments in social cognition in first episode psychosis. Soc. Neurosci., 3: 79-88, 2008.

Bleich-Cohen M., Strous R.D., Even R., Rotshtein P., Yovel G., Iancu I., Olmer A., Hendler T. Diminished neural sensitivity to irregular facial expression in first-episode schizophrenia. Hum. Brain Mapp., 30: 2606-2616, 2009.

Buchy L., Ad-Dab'bagh Y., Malla A., Lepage C., Bodnar M., Joober R., Sergerie K., Evans A., Lepage M. Cortical thickness is associated with poor insight in first-episode psychosis. J. Psychiatr. Res., 45: 781-787, 2001.

Catalan A., Gonzalez de Artaza M., Bustamante S., Orgaz P., Osa L., Angosto V., Valverde C., Bilbao A., Madrazo A., van Os J., Gonzalez-Torres M.A. Differences in Facial Emotion Recognition between First Episode Psychosis., Borderline Personality Disorder and Healthy Controls. PLoS One, 11: e0160056, 2016.

Catalucci A., Mazza M., Ciutti E., Caulo M., Pollice R., Roncone R., Casacchia M., Di Salle F., Gallucci M. Neuronal basis of haedonic appraisal in early onset schizophrenia: FMRI investigation. Neuroradiol. J., 24: 264-270, 2011.

Chou P.H., Koike S., Nishimura Y., Kawasaki S., Satomura Y., Kinoshita A., Takizawa R., Kasai K. Distinct effects of duration of untreated psychosis on brain cortical activities in different treatment phases of schizophrenia: a multi-channel near-infrared spectroscopy study. Prog. Neuropsychopharmacol. Biol. Psychiatry, 49: 63-69, 2014.

Collins D.L., Zijdenbos A.P., Kollokian V., Sled J.G., Kabani N.J., Holmes C.J., Evans A.C. Design and construction of a realistic digital brain phantom. IEEE Trans. Med. Imaging, 17: 463-468, 1998.

Comparelli A., Corigliano V., De Carolis A., Mancinelli I., Trovini G., Ottavi G., Dehning J., Tatarelli R., Brugnoli R., Girardi P. Emotion recognition impairment is present early and is stable throughout the course of schizophrenia. Schizophr. Res., 143: 65-69, 2013.

Das P., Lagopoulos J., Coulston C.M., Henderson A.F., Malhi G.S. Mentalizing impairment in schizophrenia: a functional MRI study. Schizophr. Res., 134: 158-164, 2012.

Dean A.M., Goodby E., Ooi C., Nathan P.J., Lennox B.R., Scoriels L., Shabbir S., Suckling J., Jones P.B., Bullmore E.T., Barnes A. Speed of facial affect intensity recognition as an endophenotype of first-episode psychosis and associated limbic-cortical grey matter systems. Psychol. Med., 43: 591-602, 2013.

Delaveau P., Jabourian M., Lemogne C., Guionnet S., Bergouignan L., Fossati P. Brain effects of antidepressants in major depression: a meta-analysis of emotional processing studies. J. Affect. Disord., 130: 66-74, 2011.

Diener C., Kuehner C., Brusniak W., Ubl B., Wessa M., Flor H. A meta-analysis of neurofunctional imaging studies of emotion and cognition in major depression. Neuroimage, 61: 677-685, 2012.

Edwards J., Pattison P.E., Jackson H.J., Wales R.J. Facial affect and affective prosody recognition in first-episode schizophrenia. Schizophr. Res., 48: 235-253, 2001.

Frith C., Dolan R. The role of the prefrontal cortex in higher cognitive functions. Brain Res. Cogn. Brain Res., 5: 175-181, 1996.

Fusar-Poli P., Smieskova R., Serafini G., Politi P., Borgwardt S. Neuroanatomical markers of genetic liability to psychosis and first episode psychosis: a voxelwise meta-analytical comparison. World J. Biol. Psychiatry, 15: 219-228, 2014.

Goel V., Grafman J., Sadato N., Hallett M. Modeling other minds. Neuroreport, 6: 1741-1746, 1995.

Guo X., Li J., Wang J., Fan X., Hu M., Shen Y., Chen H., Zhao J. Hippocampal and orbital inferior frontal gray matter volume abnormalities and cognitive deficit in treatment-naive., first-episode patients with schizophrenia. Schizophr. Res., 152: 339-343, 2014.

Gutiérrez-Galve L., Wheeler-Kingshott C.A., Altmann D.R., Price G., Chu E.M., Leeson V.C., Lobo A., Barker G.J., Barnes T.R., Joyce E.M., Ron M.A. Changes in the frontotemporal cortex and cognitive correlates in first-episode psychosis. Biol. Psychiatry, 68: 51-60, 2010.

Herniman S.E., Allott K.A., Killackey E., Hester R., Cotton S.M. The effect of comorbid depression on facial and prosody emotion recognition in first-episode schizophrenia spectrum. J. Affect. Disord., 208: 223-229, 2017.

Janssen J., Reig S., Parellada M., Moreno D., Graell M., Fraguas D., Zabala A., Garcia Vazquez V., Desco M., Arango C. Regional gray matter volume deficits in adolescents with first-episode psychosis. J. Am. Acad. Child. Adolesc. Psychiatry, 47: 1311-1320, 2008.

Jardri R. Neuro-imagerie cérébrale des premiers épisodes psychotiques [Brain imaging of first-episode psychosis-Article in French]. Encéphale, 39(Suppl 2): S93-S98, 2013.

Lee C.U., Shenton M.E., Salisbury D.F., Kasai K., Onitsuka T., Dickey C.C., Yurgelun-Todd D., Kikinis R., Jolesz F.A., McCarley R.W. Fusiform gyrus volume reduction in first-episode schizophrenia: a magnetic resonance imaging study. Arch. Gen. Psychiatry, 59: 775-781, 2002.

Lee H., Ku J., Kim J., Jang DP., Yoon KJ., Kim SI., Kim JJ. Aberrant neural responses to social rejection in patients with schizophrenia. Soc. Neurosci., 9: 412-423, 2014.

Lepage M., Sergerie K., Benoit A., Czechowska Y., Dickie E., Armony J.L. Emotional face processing and flat affect in schizophrenia: functional and structural neural correlates. Psychol. Med., 41: 1833-1844, 2011.

Li H., Chan R.C., McAlonan G.M., Gong QY. Facial emotion processing in schizophrenia: a meta-analysis of functional neuroimaging data. Schizophr. Bull., 36: 1029-1039, 2010.

Lui S., Deng W., Huang X., Jiang L., Ma X., Chen H., Zhang T., Li X., Li D., Zou L., Tang H., Zhou X.J., Mechelli A., Collier DA., Sweeney J.A., Li T., Gong Q. Association of cerebral deficits with clinical symptoms in antipsychotic-naive first-episode schizophrenia: an optimized voxel-based morphometry and resting state functional connectivity study. Am. J. Psychiatry, 166: 196-205, 2009.

Lyu H., Hu M., Eyler L.T., Jin H., Wang J., Ou J., Guo X., He Z., Liu F., Zhao J., Guo W. Regional white matter abnormalities in drug-naive., first-episode schizophrenia patients and their healthy unaffected siblings. Aust. N. Z. J. Psychiatry, 49: 246-254, 2015.

Malik F., Khawar R., Chaudhry H.R., Humphreys G.W. Emotion recognition and duration of untreated first-episode psychosis among patients in Pakistan. East Asian Arch. Psychiatry, 20: 31-38, 2010.

Matsumoto H., Simmons A., Williams S., Hadjulis M., Pipe R., Murray R., Frangou S. Superior temporal gyrus abnormalities in early-onset schizophrenia: similarities and differences with adult-onset schizophrenia. Am. J. Psychiatry, 158: 1299-1304, 2001.

Modinos G., Tseng H.H., Falkenberg I., Samson C., McGuire P., Allen P. Neural correlates of aberrant emotional salience predict psychotic symptoms and global functioning in high-risk and first-episode psychosis. Soc. Cogn. Affect. Neurosci., 10: 1429-1436, 2015.

Moher D., Liberati A., Tetzlaff J., Altman D.G.; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int. J. Surg., 8: 336-341, 2010.

Pinkham A., Penn D., Wangelin B., Perkins D., Gerig G., Gu H., Lieberman J. Facial emotion perception and fusiform gyrus volume in first episode schizophrenia. Schizophr. Res., 79: 341-343, 2005.

Radua J., Borgwardt S., Crescini A., Mataix-Cols D., Meyer-Lindenberg A., McGuire P.K., Fusar-Poli P. Multimodal meta-analysis of structural and functional brain changes in first episode psychosis and the effects of antipsychotic medication. Neurosci. Biobehav. Rev., 36: 2325-2333, 2012.

Rasser P.E., Johnston P., Lagopoulos J., Ward P.B., Schall U., Thienel R., Bender S., Toga A.W., Thompson P.M. Functional MRI BOLD response to Tower of London performance of first-episode schizophrenia patients using cortical pattern matching. Neuroimage, 26: 941-951, 2005.

Reske M., Habel U., Kellermann T., Backes V., Jon Shah N., von Wilmsdorff M., Gaebel W., Zilles K., Schneider F. Differential brain activation during facial emotion discrimination in first-episode schizophrenia. J. Psychiatr. Res., 43: 592-599, 2009.

Reske M., Kellermann T., Habel U., Jon Shah N., Backes V., von Wilmsdorff M., Stöcker T., Gaebel W., Schneider F. Stability of emotional dysfunctions? A long-term fMRI study in first-episode schizophrenia. J. Psychiatr. Res., 41: 918-927, 2007a.

Reske M., Kellermann T., Habel U., Jon Shah N., Backes V., von Wilmsdorff M., Stöcker T., Gaebel W., Schneider F. Stability of emotional dysfunctions? A long-term fMRI study in first-episode schizophrenia. J. Psychiatr Res., 41: 918-927, 2007b.

Romero-Ferreiro M.V., Aguado L., Rodriguez-Torresano J., Palomo T., Rodriguez-Jimenez R., Pedreira-Massa JL. Facial affect recognition in early and late-stage schizophrenia patients. Schizophr. Res., 172: 177-183, 2016.

Scanlon C., Anderson-Schmidt H., Kilmartin L., McInerney S., Kenney J., McFarland J., Waldron M., Ambati S., Fullard A., Logan S., Hallahan B., Barker G.J., Elliott M.A., McCarthy P., Cannon D.M., McDonald C. Cortical thinning and caudate abnormalities in first episode psychosis and their association with clinical outcome. Schizophr. Res., 159: 36-42, 2014.

Shelton M.A., Newman J.T., Gu H., Sampson A.R., Fish K.N., MacDonald M.L., Moyer C.E., DiBitetto J.V., Dorph-Petersen K.A., Penzes P., Lewis D.A., Sweet R.A. Loss of Microtubule-Associated Protein 2 Immunoreactivity Linked to Dendritic Spine Loss in Schizophrenia. Biol. Psychiatry, 78: 374-385, 2015.

Talairach J., Tournoux P. Co-Planar Stereotactic Atlas of Human Brain. New York (NY), Thieme Medical Publisher, 1998.

Teixeira S., Machado S., Velasques B., Sanfim A., Minc D., Peressutti C., Bittencourt J., Budde H., Cagy M., Anghinah R., Basile L.F., Piedade R., Ribeiro P., Diniz C., Cartier C., Gongora M., Silva F., Manaia F., Silva J.G. Integrative parietal cortex processes: neurological and psychiatric aspects. J. Neurol. Sci., 338 :12-22, 2014.

Thompson A., Papas A., Bartholomeusz C., Allott K., Amminger G.P., Nelson B., Wood S., Yung A. Social cognition in clinical "at risk" for psychosis and first episode psychosis populations. Schizophr. Res., 141: 204-209, 2012.

Tseng H.H., Roiser J.P., Modinos G., Falkenberg I., Samson C., McGuire P., Allen P. Corticolimbic dysfunction during facial and prosodic emotional recognition in first-episode psychosis patients and individuals at ultra-high risk. Neuroimage Clin., 12: 645-654, 2016.

Turkeltaub P.E., Eickhoff S.B., Laird A.R., Fox M., Wiener M., Fox P. Minimizing within-experiment and within-group effects in Activation Likelihood Estimation meta-analyses. Hum. Brain Mapp., 33: 1-13, 2012.

Whitfield-Gabrieli S., Thermenos H.W., Milanovic S., Tsuang M.T., Faraone S.V., McCarley R., Shenton M.E., Green A.I., Nieto-Castanon A., LaViolette P., Wojcik J., Gabrieli J.D., Seidman L.J. Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proc. Natl. Acad. Sci. U.S.A., 106: 1279-1284, 2009.

Zhang H., Wei X., Tao H., Mwansisya T.E., Pu W., He Z., Hu A., Xu L., Liu Z., Shan B., Xue Z. Opposite effective connectivity in the posterior cingulate and medial prefrontal cortex between first-episode schizophrenic patients with suicide risk and healthy controls. PLoS One, 8: e63477, 2003.

Zhang Y., Zheng J., Fan X., Guo X., Guo W., Yang G., Chen H., Zhao J., Lv L. Dysfunctional resting-state connectivities of brain regions with structural deficits in drug-naive first-episode schizophrenia adolescents. Schizophr. Res., 168: 353-359, 2015.

Zheng L.R., Wang Y.X., Li M., Li LJ., Kang Z., Guo X.F., Zhang J.B., Zhao J.P., Wei Q.L. (郑俩荣 王雁新 李盟 李雷俊 康庄 国效峰 张晋碚 赵靖平 魏钦令). 首发未治疗的精神分裂症患者的大脑皮质的变化 [A study of cerebral cortex in untreated first-episode schizophrenics-Article in Chinese]. Zhonghua Yi Xue Za Zhi (中华医学杂志., Natl. Med. J. China), 93: 3252–3255, 2013.




DOI: https://doi.org/10.12871/aib.v156i1-2.4625

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