Hostname: page-component-77f85d65b8-pztms Total loading time: 0 Render date: 2026-03-28T01:20:30.710Z Has data issue: false hasContentIssue false
  • English
  • Français

The interaction between early life complications and a polygenic risk score for schizophrenia is associated with brain activity during emotion processing in healthy participants

Published online by Cambridge University Press:  02 February 2024

Veronica Debora Toro ,
Linda A. Antonucci ,
Tiziana Quarto ,
Roberta Passiatore ,
Leonardo Fazio ,
Gianluca Ursini ,
Qiang Chen ,
Rita Masellis ,
Silvia Torretta  and
Leonardo Sportelli
...Show all authors
Veronica Debora Toro
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy Department of Humanities, University of Foggia, Foggia, Italy
Linda A. Antonucci
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy
Tiziana Quarto
Affiliation:
Department of Humanities, University of Foggia, Foggia, Italy
Roberta Passiatore
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy
Leonardo Fazio
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy Department of Medicine and Surgery, Libera Università Mediterranea “Giuseppe Degennaro”, Bari, Italy
Gianluca Ursini
Affiliation:
Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, USA Department of Psychiatry and Behavioral Sciences, Johns Hopkins University, Baltimore, MD, USA
Qiang Chen
Affiliation:
Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, USA
Rita Masellis
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy U.O.C. Psichiatria Universitaria, Azìenda Ospedaliero-Universitaria Consorziale Policlinico, Bari, Italy
Silvia Torretta
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy
Leonardo Sportelli
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy
Gianluca Christos Kikidis
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy
Francesco Massari
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy
Enrico D'Ambrosio
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, SE5 8AF, UK
Antonio Rampino
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy U.O.C. Psichiatria Universitaria, Azìenda Ospedaliero-Universitaria Consorziale Policlinico, Bari, Italy
Giulio Pergola
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, USA
Daniel R. Weinberger
Affiliation:
Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, USA
Alessandro Bertolino
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy U.O.C. Psichiatria Universitaria, Azìenda Ospedaliero-Universitaria Consorziale Policlinico, Bari, Italy
Giuseppe Blasi*
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy U.O.C. Psichiatria Universitaria, Azìenda Ospedaliero-Universitaria Consorziale Policlinico, Bari, Italy
*
Corresponding author: Giuseppe Blasi; Email: giuseppe.blasi@uniba.it
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Previous evidence suggests that early life complications (ELCs) interact with polygenic risk for schizophrenia (SCZ) in increasing risk for the disease. However, no studies have investigated this interaction on neurobiological phenotypes. Among those, anomalous emotion-related brain activity has been reported in SCZ, even if evidence of its link with SCZ-related genetic risk is not solid. Indeed, it is possible this relationship is influenced by non-genetic risk factors. Thus, this study investigated the interaction between SCZ-related polygenic risk and ELCs on emotion-related brain activity.

Methods

169 healthy participants (HP) in a discovery and 113 HP in a replication sample underwent functional magnetic resonance imaging (fMRI) during emotion processing, were categorized for history of ELCs and genome-wide genotyped. Polygenic risk scores (PRSs) were computed using SCZ-associated variants considering the most recent genome-wide association study. Furthermore, 75 patients with SCZ also underwent fMRI during emotion processing to verify consistency of their brain activity patterns with those associated with risk factors for SCZ in HP.

Results

Results in the discovery and replication samples indicated no effect of PRSs, but an interaction between PRS and ELCs in left ventrolateral prefrontal cortex (VLPFC), where the greater the activity, the greater PRS only in presence of ELCs. Moreover, SCZ had greater VLPFC response than HP.

Conclusions

These results suggest that emotion-related VLPFC response lies in the path from genetic and non-genetic risk factors to the clinical presentation of SCZ, and may implicate an updated concept of intermediate phenotype considering early non-genetic factors of risk for SCZ.

Keywords

early life complicationsemotion processingfacesfMRIpolygenic risk scoreschizophrenia

Information

Type
Original Article
Information
Psychological Medicine , Volume 54 , Issue 8 , June 2024 , pp. 1876 - 1885
Check for updates
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Anticevic, A., Van Snellenberg, J. X., Cohen, R. E., Repovs, G., Dowd, E. C., & Barch, D. M. (2012). Amygdala recruitment in schizophrenia in response to aversive emotional material: A meta-analysis of neuroimaging studies. Schizophrenia Bulletin, 38(3), 608–621. doi:10.1093/schbul/sbq131.CrossRefGoogle ScholarPubMed
Belsky, J. (2007). For better and for worse: Differential susceptibility to environmental influences. Current Directions in Psychological Science, 16(6), 300–304.CrossRefGoogle Scholar
Belsky, J., & Pluess, M. (2009). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135(6), 885–908. doi:10.1037/a0017376.CrossRefGoogle ScholarPubMed
Bertolino, A., & Blasi, G. (2009). The genetics of schizophrenia. Neuroscience, 164(1), 288–299. doi:10.1016/j.neuroscience.2009.04.038.CrossRefGoogle ScholarPubMed
Blasi, G., Hariri, A. R., Alce, G., Taurisano, P., Sambataro, F., Das, S., … Mattay, V. S. (2009a). Preferential amygdala reactivity to the negative assessment of neutral faces. Biological Psychiatry, 66(9), 847–853. doi:10.1016/j.biopsych.2009.06.017.CrossRefGoogle Scholar
Blasi, G., Lo Bianco, L., Taurisano, P., Gelao, B., Romano, R., Fazio, L., … Bertolino, A. (2009b). Functional variation of the dopamine D2 receptor gene is associated with emotional control as well as brain activity and connectivity during emotion processing in humans. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience, 29(47), 14812–14819. doi:10.1523/jneurosci.3609-09.2009.CrossRefGoogle ScholarPubMed
Cannon, M., Jones, P. B., & Murray, R. M. (2002). Obstetric complications and schizophrenia: Historical and meta-analytic review. The American Journal of Psychiatry, 159(7), 1080–1092. doi:10.1176/appi.ajp.159.7.1080.CrossRefGoogle ScholarPubMed
Chen, Q., Ursini, G., Romer, A. L., Knodt, A. R., Mezeivtch, K., Xiao, E., … Weinberger, D. R. (2018). Schizophrenia polygenic risk score predicts mnemonic hippocampal activity. Brain, 141(4), 1218–1228. doi:10.1093/brain/awy004.CrossRefGoogle ScholarPubMed
Consortium, S. W. G. o. t. P. G. (2014). Biological insights from 108 schizophrenia-associated genetic loci. Nature, 511(7510), 421–427. doi:10.1038/nature13595.Google Scholar
Cosgrove, D., Harold, D., Mothersill, O., Anney, R., Hill, M. J., Bray, N. J., … Donohoe, G. (2017). MiR-137-derived polygenic risk: Effects on cognitive performance in patients with schizophrenia and controls. Translational Psychiatry, 7(1), e1012. doi:10.1038/tp.2016.286.CrossRefGoogle ScholarPubMed
Davies, E. L., Bell, J. S., & Bhattacharya, S. (2016). Preeclampsia and preterm delivery: A population-based case-control study. Hypertension in Pregnancy, 35(4), 510–519. doi:10.1080/10641955.2016.1190846.CrossRefGoogle ScholarPubMed
Dimitriadis, S. I., Lancaster, T. M., Perry, G., Tansey, K. E., Jones, D. K., Singh, K. D., … Linden, D. E. (2021). Global brain flexibility during working memory is reduced in a high-genetic-risk group for schizophrenia. Biological psychiatry. Cognitive Neuroscience and Neuroimaging, 6(12), 1176–1184. doi:10.1016/j.bpsc.2021.01.007.CrossRefGoogle Scholar
Drabant, E. M., Hariri, A. R., Meyer-Lindenberg, A., Munoz, K. E., Mattay, V. S., Kolachana, B. S., … Weinberger, D. R. (2006). Catechol O-methyltransferase val158met genotype and neural mechanisms related to affective arousal and regulation. Archives of General Psychiatry, 63(12), 1396–1406. doi:10.1001/archpsyc.63.12.1396.CrossRefGoogle ScholarPubMed
Dyck, M., Loughead, J., Gur, R. C., Schneider, F., & Mathiak, K. (2014). Hyperactivation balances sensory processing deficits during mood induction in schizophrenia. Social Cognitive and Affective Neuroscience, 9(2), 167–175. doi:10.1093/scan/nss120.CrossRefGoogle ScholarPubMed
Dzafic, I., Burianová, H., Periyasamy, S., & Mowry, B. (2018). Association between schizophrenia polygenic risk and neural correlates of emotion perception. Psychiatry Research. Neuroimaging, 276, 33–40. doi:10.1016/j.pscychresns.2018.04.005.CrossRefGoogle ScholarPubMed
Ellis, B. J., Essex, M. J., & Boyce, W. T. (2005). Biological sensitivity to context: II. Empirical explorations of an evolutionary-developmental theory. Development and Psychopathology, 17(2), 303–328. doi:10.1017/s0954579405050157.CrossRefGoogle ScholarPubMed
Erk, S., Mohnke, S., Ripke, S., Lett, T. A., Veer, I. M., Wackerhagen, C., … Walter, H. (2017). Functional neuroimaging effects of recently discovered genetic risk loci for schizophrenia and polygenic risk profile in five RDoC subdomains. Translational Psychiatry, 7(1), e997. doi:10.1038/tp.2016.272.CrossRefGoogle ScholarPubMed
Etkin, A., Büchel, C., & Gross, J. J. (2015). The neural bases of emotion regulation. Nature Reviews. Neuroscience, 16(11), 693–700. doi:10.1038/nrn4044.CrossRefGoogle ScholarPubMed
Feghali, M. N., Caritis, S. N., Catov, J. M., & Scifres, C. M. (2016). Timing of delivery and pregnancy outcomes in women with gestational diabetes. American Journal of Obstetrics and Gynecology, 215(2), 243.e241–247. doi:10.1016/j.ajog.2016.03.006.CrossRefGoogle ScholarPubMed
Fiorito, A. M., Aleman, A., Blasi, G., Bourque, J., Cao, H., Chan, R. C. K., … Sescousse, G. (2022). Are brain responses to emotion a reliable endophenotype of schizophrenia? An image-based fMRI meta-analysis. Biological Psychiatry, 93(2), 167–177. doi:10.1016/j.biopsych.2022.06.013.CrossRefGoogle Scholar
Frank, D. W., Dewitt, M., Hudgens-Haney, M., Schaeffer, D. J., Ball, B. H., Schwarz, N. F., … Sabatinelli, D. (2014). Emotion regulation: Quantitative meta-analysis of functional activation and deactivation. Neuroscience and Biobehavioral Reviews, 45, 202–211. doi:10.1016/j.neubiorev.2014.06.010.CrossRefGoogle ScholarPubMed
Fusar-Poli, L., Pries, L. K., van Os, J., Erzin, G., Delespaul, P., Kenis, G., … Guloksuz, S. (2022). Examining facial emotion recognition as an intermediate phenotype for psychosis: Findings from the EUGEI study. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 113, 110440. doi:10.1016/j.pnpbp.2021.110440.CrossRefGoogle ScholarPubMed
Gottesman, I. I., & Shields, J. (1967). A polygenic theory of schizophrenia. Proceedings of the National Academy of Sciences of the United States of America, 58(1), 199–205. doi:10.1073/pnas.58.1.199.CrossRefGoogle ScholarPubMed
Green, M. F., Penn, D. L., Bentall, R., Carpenter, W. T., Gaebel, W., Gur, R. C., … Heinssen, R. (2008). Social cognition in schizophrenia: An NIMH workshop on definitions, assessment, and research opportunities. Schizophrenia Bulletin, 34(6), 1211–1220. doi:10.1093/schbul/sbm145.CrossRefGoogle ScholarPubMed
Hariri, A. R., Bookheimer, S. Y., & Mazziotta, J. C. (2000). Modulating emotional responses: Effects of a neocortical network on the limbic system. Neuroreport, 11(1), 43–48. doi:10.1097/00001756-200001170-00009.CrossRefGoogle ScholarPubMed
Hariri, A. R., Drabant, E. M., Munoz, K. E., Kolachana, B. S., Mattay, V. S., Egan, M. F., & Weinberger, D. R. (2005). A susceptibility gene for affective disorders and the response of the human amygdala. Archives of General Psychiatry, 62(2), 146–152. doi:10.1001/archpsyc.62.2.146.CrossRefGoogle ScholarPubMed
Hariri, A. R., Mattay, V. S., Tessitore, A., Kolachana, B., Fera, F., Goldman, D., … Weinberger, D. R. (2002). Serotonin transporter genetic variation and the response of the human amygdala. Science (New York, N.Y.), 297(5580), 400–403. doi:10.1126/science.1071829.CrossRefGoogle ScholarPubMed
Jaffe, A. E., Gao, Y., Deep-Soboslay, A., Tao, R., Hyde, T. M., Weinberger, D. R., & Kleinman, J. E. (2016). Mapping DNA methylation across development, genotype and schizophrenia in the human frontal cortex. Nature Neuroscience, 19(1), 40–47. doi:10.1038/nn.4181.CrossRefGoogle ScholarPubMed
Koch, E., Nyberg, L., Lundquist, A., & Kauppi, K. (2022). Polygenic risk for schizophrenia has sex-specific effects on brain activity during memory processing in healthy individuals. Genes, 13(3), 412. doi:10.3390/genes13030412.CrossRefGoogle ScholarPubMed
Kohler, C. G., & Martin, E. A. (2006). Emotional processing in schizophrenia. Cognitive Neuropsychiatry, 11(3), 250–271. doi:10.1080/13546800500188575.CrossRefGoogle ScholarPubMed
Lancaster, T. M., Ihssen, N., Brindley, L. M., Tansey, K. E., Mantripragada, K., O'Donovan, M. C., … Linden, D. E. (2016). Associations between polygenic risk for schizophrenia and brain function during probabilistic learning in healthy individuals. Human Brain Mapping, 37(2), 491–500. doi:10.1002/hbm.23044.CrossRefGoogle ScholarPubMed
Lo Bianco, L., Blasi, G., Taurisano, P., Di Giorgio, A., Ferrante, F., Ursini, G., … Bertolino, A. (2013). Interaction between catechol-O-methyltransferase (COMT) Val158Met genotype and genetic vulnerability to schizophrenia during explicit processing of aversive facial stimuli. Psychological Medicine, 43(2), 279–292. doi:10.1017/s0033291712001134.CrossRefGoogle ScholarPubMed
Martin, D., Croft, J., Pitt, A., Strelchuk, D., Sullivan, S., & Zammit, S. (2020). Systematic review and meta-analysis of the relationship between genetic risk for schizophrenia and facial emotion recognition. Schizophrenia Research, 218, 7–13. doi:10.1016/j.schres.2019.12.031.CrossRefGoogle ScholarPubMed
McNeil, T. F., Cantor-Graae, E., & Sjöström, K. (1994). Obstetric complications as antecedents of schizophrenia: Empirical effects of using different obstetric complication scales. Journal of Psychiatric Research, 28(6), 519–530. doi:10.1016/0022-3956(94)90042-6.CrossRefGoogle ScholarPubMed
Mier, D., Lis, S., Zygrodnik, K., Sauer, C., Ulferts, J., Gallhofer, B., & Kirsch, P. (2014). Evidence for altered amygdala activation in schizophrenia in an adaptive emotion recognition task. Psychiatry Research, 221(3), 195–203. doi:10.1016/j.pscychresns.2013.12.001.CrossRefGoogle Scholar
Miller, J. A., Scult, M. A., Conley, E. D., Chen, Q., Weinberger, D. R., & Hariri, A. R. (2018). Effects of schizophrenia polygenic risk scores on brain activity and performance during working memory subprocesses in healthy young adults. Schizophrenia Bulletin, 44(4), 844–853. doi:10.1093/schbul/sbx140.CrossRefGoogle ScholarPubMed
Murata, T., Yasuda, S., Imaizumi, K., Isogami, H., Fukuda, T., Kyozuka, H., … Fujimori, K. (2022). Association of labour duration in spontaneous deliveries with low neonatal apgar scores and foetal acidosis: The Japan Environment and Children's Study. Scientific Reports, 12(1), 21519. doi:10.1038/s41598-022-24359-3.CrossRefGoogle ScholarPubMed
Nicodemus, K. K., Marenco, S., Batten, A. J., Vakkalanka, R., Egan, M. F., Straub, R. E., & Weinberger, D. R. (2008). Serious obstetric complications interact with hypoxia-regulated/vascular-expression genes to influence schizophrenia risk. Molecular Psychiatry, 13(9), 873–877. doi:10.1038/sj.mp.4002153.CrossRefGoogle ScholarPubMed
Owen, M. J., Sawa, A., & Mortensen, P. B. (2016). Schizophrenia. Lancet (London, England), 388(10039), 86–97. doi:10.1016/s0140-6736(15)01121-6.CrossRefGoogle ScholarPubMed
Paradiso, S., Andreasen, N. C., Crespo-Facorro, B., O'Leary, D. S., Watkins, G. L., Boles Ponto, L. L., & Hichwa, R. D. (2003). Emotions in unmedicated patients with schizophrenia during evaluation with positron emission tomography. The American Journal of Psychiatry, 160(10), 1775–1783. doi:10.1176/appi.ajp.160.10.1775.CrossRefGoogle ScholarPubMed
Park, H. Y., Yun, J. Y., Shin, N. Y., Kim, S. Y., Jung, W. H., Shin, Y. S., … Kwon, J. S. (2016). Decreased neural response for facial emotion processing in subjects with high genetic load for schizophrenia. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 71, 90–96. doi:10.1016/j.pnpbp.2016.06.014.CrossRefGoogle ScholarPubMed
Pergola, G., Papalino, M., Gelao, B., Sportelli, L., Vollerbergh, W., Grattagliano, I., & Bertolino, A. (2019). Evocative gene-environment correlation between genetic risk for schizophrenia and bullying victimization. World psychiatry: Official Journal of the World Psychiatric Association (WPA), 18(3), 366–367. doi:10.1002/wps.20685.CrossRefGoogle ScholarPubMed
Phillips, M. L., Drevets, W. C., Rauch, S. L., & Lane, R. (2003). Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biological Psychiatry, 54(5), 504–514. doi:10.1016/s0006-3223(03)00168-9.CrossRefGoogle ScholarPubMed
Purcell, S. M., Wray, N. R., Stone, J. L., Visscher, P. M., O'Donovan, M. C., Sullivan, P. F., & Sklar, P. (2009). Common polygenic variation contributes to risk of schizophrenia and bipolar disorder. Nature, 460(7256), 748–752. doi:10.1038/nature08185.Google ScholarPubMed
Quarto, T., Blasi, G., Maddalena, C., Viscanti, G., Lanciano, T., Soleti, E., … Curci, A. (2016). Association between ability emotional intelligence and left insula during social judgment of facial emotions. PLoS One, 11(2), e0148621. doi:10.1371/journal.pone.0148621.CrossRefGoogle ScholarPubMed
Quarto, T., Paparella, I., De Tullio, D., Viscanti, G., Fazio, L., Taurisano, P., … Blasi, G. (2018). Familial risk and a genome-wide supported DRD2 variant for schizophrenia predict lateral prefrontal-amygdala effective connectivity during emotion processing. Schizophrenia Bulletin, 44(4), 834–843. doi:10.1093/schbul/sbx128.CrossRefGoogle Scholar
Rasetti, R., Mattay, V. S., Wiedholz, L. M., Kolachana, B. S., Hariri, A. R., Callicott, J. H., … Weinberger, D. R. (2009). Evidence that altered amygdala activity in schizophrenia is related to clinical state and not genetic risk. The American Journal of Psychiatry, 166(2), 216–225. doi:10.1176/appi.ajp.2008.08020261.CrossRefGoogle Scholar
Rasmussen, S., Ebbing, C., & Irgens, L. M. (2017). Predicting preeclampsia from a history of preterm birth. PLoS One, 12(7), e0181016. doi:10.1371/journal.pone.0181016.CrossRefGoogle ScholarPubMed
Shifman, S., Bronstein, M., Sternfeld, M., Pisanté, A., Weizman, A., Reznik, I., … Darvasi, A. (2004). COMT: A common susceptibility gene in bipolar disorder and schizophrenia. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics: the Official Publication of the International Society of Psychiatric Genetics, 128b(1), 61–64. doi:10.1002/ajmg.b.30032.CrossRefGoogle Scholar
Smith, S. M., & Nichols, T. E. (2009). Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage, 44(1), 83–98. doi:10.1016/j.neuroimage.2008.03.061.CrossRefGoogle ScholarPubMed
Smolka, M. N., Schumann, G., Wrase, J., Grüsser, S. M., Flor, H., Mann, K., … Heinz, A. (2005). Catechol-O-methyltransferase val158met genotype affects processing of emotional stimuli in the amygdala and prefrontal cortex. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience, 25(4), 836–842. doi:10.1523/jneurosci.1792-04.2005.CrossRefGoogle ScholarPubMed
Spilka, M. J., & Goghari, V. M. (2017). Similar patterns of brain activation abnormalities during emotional and non-emotional judgments of faces in a schizophrenia family study. Neuropsychologia, 96, 164–174. doi:10.1016/j.neuropsychologia.2017.01.014.CrossRefGoogle Scholar
Sullivan, P. F. (2005). The genetics of schizophrenia. PLoS Medicine, 2(7), e212. doi:10.1371/journal.pmed.0020212.CrossRefGoogle ScholarPubMed
Taurisano, P., Blasi, G., Romano, R., Sambataro, F., Fazio, L., Gelao, B., … Bertolino, A. (2013). DAT by perceived MC interaction on human prefrontal activity and connectivity during emotion processing. Social Cognitive and Affective Neuroscience, 8(8), 855–862. doi:10.1093/scan/nss084.CrossRefGoogle ScholarPubMed
Taylor, S. F., Kang, J., Brege, I. S., Tso, I. F., Hosanagar, A., & Johnson, T. D. (2012). Meta-analysis of functional neuroimaging studies of emotion perception and experience in schizophrenia. Biological Psychiatry, 71(2), 136–145. doi:10.1016/j.biopsych.2011.09.007.CrossRefGoogle ScholarPubMed
Taylor, S. F., Liberzon, I., Decker, L. R., & Koeppe, R. A. (2002). A functional anatomic study of emotion in schizophrenia. Schizophrenia Research, 58(2–3), 159–172. doi:10.1016/s0920-9964(01)00403-0.CrossRefGoogle ScholarPubMed
Tottenham, N., Tanaka, J. W., Leon, A. C., McCarry, T., Nurse, M., Hare, T. A., … Nelson, C. (2009). The NimStim set of facial expressions: Judgments from untrained research participants. Psychiatry Research, 168(3), 242–249. doi:10.1016/j.psychres.2008.05.006.CrossRefGoogle ScholarPubMed
Trubetskoy, V., Pardiñas, A. F., Qi, T., Panagiotaropoulou, G., Awasthi, S., Bigdeli, T. B., … O'Donovan, M. C. (2022). Mapping genomic loci implicates genes and synaptic biology in schizophrenia. Nature, 604(7906), 502–508. doi:10.1038/s41586-022-04434-5.CrossRefGoogle ScholarPubMed
Ursini, G., Di Carlo, P., Mukherjee, S., Chen, Q., Han, S., Kim, J., … Weinberger, D. R. (2023). Prioritization of potential causative genes for schizophrenia in placenta. Nature Communication, 14(1), 2613. doi:10.1038/s41467-023-38140-1.CrossRefGoogle ScholarPubMed
Ursini, G., Punzi, G., Chen, Q., Marenco, S., Robinson, J. F., Porcelli, A., … Weinberger, D. R. (2018). Convergence of placenta biology and genetic risk for schizophrenia. Nature Medicine, 24(6), 792–801. doi:10.1038/s41591-018-0021-y.CrossRefGoogle ScholarPubMed
Ursini, G., Punzi, G., Langworthy, B. W., Chen, Q., Xia, K., Cornea, E. A., … Weinberger, D. R. (2021). Placental genomic risk scores and early neurodevelopmental outcomes. Proceedings of the National Academy of Sciences of the United States of America, 118(7), 792–801. doi:10.1073/pnas.2019789118.Google ScholarPubMed
van Buuren, M., Vink, M., Rapcencu, A. E., & Kahn, R. S. (2011). Exaggerated brain activation during emotion processing in unaffected siblings of patients with schizophrenia. Biological Psychiatry, 70(1), 81–87. doi:10.1016/j.biopsych.2011.03.011.CrossRefGoogle ScholarPubMed
van der Meer, L., Swart, M., van der Velde, J., Pijnenborg, G., Wiersma, D., Bruggeman, R., & Aleman, A. (2014). Neural correlates of emotion regulation in patients with schizophrenia and non-affected siblings. PLoS One, 9(6), e99667. doi:10.1371/journal.pone.0099667.CrossRefGoogle ScholarPubMed
van Donkersgoed, R. J., Wunderink, L., Nieboer, R., Aleman, A., & Pijnenborg, G. H. (2015). Social cognition in individuals at ultra-high risk for psychosis: A meta-analysis. PLoS One, 10(10), e0141075. doi:10.1371/journal.pone.0141075.CrossRefGoogle ScholarPubMed
Vassos, E., Kou, J., Tosato, S., Maxwell, J., Dennison, C. A., Legge, S. E., … Murray, R. M. (2022). Lack of support for the genes by early environment interaction hypothesis in the pathogenesis of schizophrenia. Schizophrenia Bulletin, 48(1), 20–26. doi:10.1093/schbul/sbab052.CrossRefGoogle ScholarPubMed
Walton, E., Geisler, D., Lee, P. H., Hass, J., Turner, J. A., Liu, J., … Ehrlich, S. (2014). Prefrontal inefficiency is associated with polygenic risk for schizophrenia. Schizophrenia Bulletin, 40(6), 1263–1271. doi:10.1093/schbul/sbt174.CrossRefGoogle ScholarPubMed
Wang, Y., Li, Z., Liu, W. H., Wei, X. H., Jiang, X. Q., Lui, S. S. Y., … Chan, R. C. K. (2018). Negative schizotypy and altered functional connectivity during facial emotion processing. Schizophrenia Bulletin, 44(suppl_2), S491–s500. doi:10.1093/schbul/sby036.CrossRefGoogle ScholarPubMed
Weinberger, D. R. (1987). Implications of normal brain development for the pathogenesis of schizophrenia. Archives of General Psychiatry, 44(7), 660–669. doi:10.1001/archpsyc.1987.01800190080012.CrossRefGoogle ScholarPubMed
Williams, H. J., Owen, M. J., & O'Donovan, M. C. (2007). Is COMT a susceptibility gene for schizophrenia? Schizophrenia Bulletin, 33(3), 635–641. doi:10.1093/schbul/sbm019.CrossRefGoogle ScholarPubMed
Wolf, D. H., Satterthwaite, T. D., Calkins, M. E., Ruparel, K., Elliott, M. A., Hopson, R. D., … Gur, R. E. (2015). Functional neuroimaging abnormalities in youth with psychosis spectrum symptoms. JAMA Psychiatry, 72(5), 456–465. doi:10.1001/jamapsychiatry.2014.3169.CrossRefGoogle ScholarPubMed
Wortinger, L. A., Engen, K., Barth, C., Andreassen, O. A., Nordbø Jørgensen, K., & Agartz, I. (2022). Asphyxia at birth affects brain structure in patients on the schizophrenia-bipolar disorder spectrum and healthy participants. Psychological Medicine, 52(6), 1050–1059. doi:10.1017/s0033291720002779.CrossRefGoogle ScholarPubMed
Wray, N. R., Goddard, M. E., & Visscher, P. M. (2007). Prediction of individual genetic risk to disease from genome-wide association studies. Genome Research, 17(10), 1520–1528. doi:10.1101/gr.6665407.CrossRefGoogle ScholarPubMed
Yang, Y., & Wu, N. (2022). Gestational diabetes mellitus and preeclampsia: Correlation and influencing factors. Frontiers in Cardiovascular Medicine, 9, 831297. doi:10.3389/fcvm.2022.831297.CrossRefGoogle ScholarPubMed
Supplementary material: File

Toro et al. supplementary material

Toro et al. supplementary material
Download Toro et al. supplementary material(File)
File 373.8 KB