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Neurocognitive correlates of working memory and emotional processing in postpartum psychosis: an fMRI study

Published online by Cambridge University Press:  16 March 2020

Olivia S. Kowalczyk Open the ORCID record for Olivia S. Kowalczyk [Opens in a new window] ,
Astrid M. Pauls ,
Montserrat Fusté ,
Steven C.R. Williams ,
Katie Hazelgrove ,
Costanza Vecchio ,
Gertrude Seneviratne ,
Carmine M. Pariante ,
Paola Dazzan  and
Mitul A. Mehta
Olivia S. Kowalczyk
Affiliation:
Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
Astrid M. Pauls
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
Montserrat Fusté
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK CIBERSAM, Centro de Investigación Biomédica en Red de Salud Mental, Madrid, Spain
Steven C.R. Williams
Affiliation:
Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK National Institute for Health Research (NIHR) Mental Health Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King's College London, London, UK
Katie Hazelgrove
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK Section of Stress, Psychiatry and Immunology and Perinatal Psychiatry, Department of Psychological Medicine, Institute of Psychiatry, Psychology & Neurosciences, King's College London, London, UK
Costanza Vecchio
Affiliation:
Section of Stress, Psychiatry and Immunology and Perinatal Psychiatry, Department of Psychological Medicine, Institute of Psychiatry, Psychology & Neurosciences, King's College London, London, UK
Gertrude Seneviratne
Affiliation:
Section of Stress, Psychiatry and Immunology and Perinatal Psychiatry, Department of Psychological Medicine, Institute of Psychiatry, Psychology & Neurosciences, King's College London, London, UK
Carmine M. Pariante
Affiliation:
National Institute for Health Research (NIHR) Mental Health Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King's College London, London, UK Section of Stress, Psychiatry and Immunology and Perinatal Psychiatry, Department of Psychological Medicine, Institute of Psychiatry, Psychology & Neurosciences, King's College London, London, UK
Paola Dazzan
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
Mitul A. Mehta*
Affiliation:
Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
*
Author for correspondence: Mitul A. Mehta, E-mail: [email protected]
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Abstract

Background

Postpartum psychosis (PP) is a severe postpartum disorder. While working memory and emotional processing-related brain function are consistently impaired in psychoses unrelated to the puerperium, no studies have investigated them in PP.

Methods

Twenty-four women at risk of developing PP (11 developed an episode – PE; 13 remained well – NPE) and 20 healthy postpartum women completed two functional magnetic resonance imaging tasks within a year of delivery: working memory (n-back) and emotional face recognition (fearful faces). We compared women at-risk of PP to controls, as well as NPE, PE, and controls to test for potential effects of a PP episode occurrence.

Results

Women at-risk of PP and PE showed hyperactivation of lateral visual areas, precuneus, and posterior cingulate during the n-back task. The at-risk group as a whole, as well as the PE and NPE groups, showed hyperconnectivity of the right dorsolateral prefrontal cortex (DLPFC) with various parieto-occipito-temporo-cerebellar regions compared to controls during several n-back conditions. Increases in connectivity between the right DLPFC and ipsilateral middle temporal gyrus were observed in the PE group compared to NPE during 2-back. During the fearful faces task, at-risk women as a group showed hyperactivation of fronto-cingulo-subcortical regions, and hypoconnectivity between the left amygdala and ipsilateral occipito-parietal regions compared to controls. No significant performance differences were observed.

Conclusions

These results present preliminary evidence of a differential nature of functional brain abnormalities in PP compared to the typically observed reduced connectivity with the DLPFC in psychoses unrelated to puerperium, such as bipolar disorder.

Keywords

Emotional processingfMRIfunctional connectivitypostpartum psychosisworking memory
Type
Original Article
Information
Psychological Medicine , Volume 51 , Issue 10 , July 2021 , pp. 1724 - 1732
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Adler, C. M., Holland, S. K., Schmithorst, V., Tuchfarber, M. J., & Strakowski, S. M. (2004). Changes in neuronal activation in patients with bipolar disorder during performance of a working memory task. Bipolar Disorders, 6, 540–549.CrossRefGoogle ScholarPubMed
Bähner, F., & Meyer-Lindenberg, A. (2017). Hippocampal–prefrontal connectivity as a translational phenotype for schizophrenia. European Neuropsychopharmacology, 27, 93–106.CrossRefGoogle Scholar
Bora, E., Yücel, M., & Pantelis, C. (2010). Cognitive impairment in schizophrenia and affective psychoses: Implications for DSM-V criteria and beyond. Schizophrenia Bulletin, 36, 36–42.CrossRefGoogle ScholarPubMed
Cabeza, R., & Nyberg, L. (2000). Imaging cognition II: An empirical review of 275 PET and fMRI studies. Journal of Cognitive Neuroscience, 12, 1–47.CrossRefGoogle ScholarPubMed
Chen, C.-H., Suckling, J., Lennox, B. R., Ooi, C., & Bullmore, E. T. (2011). A quantitative meta-analysis of fMRI studies in bipolar disorder. Bipolar Disorders, 13, 1–15.CrossRefGoogle ScholarPubMed
Cremaschi, L., Penzo, B., Palazzo, M., Dobrea, C., Cristoffanini, M., Dell'Osso, B., & Altamura, A. C. (2013). Assessing working memory via n-back task in euthymic bipolar I disorder patients: A review of functional magnetic resonance imaging studies. Neuropsychobiology, 68, 63–70.CrossRefGoogle ScholarPubMed
Das, P., Kemp, A., Flynn, G., Harris, A., Liddell, B., Whitford, T., … Williams, L. (2007). Functional disconnections in the direct and indirect amygdala pathways for fear processing in schizophrenia. Schizophrenia Research, 90, 284–294.CrossRefGoogle Scholar
Dell'Osso, B., Cinnante, C., Di Giorgio, A., Cremaschi, L., Palazzo, M. C., Cristoffanini, M., … Altamura, A. C. (2015). Altered prefrontal cortex activity during working memory task in bipolar disorder: A functional magnetic resonance imaging study in euthymic bipolar I and II patients. Journal of Affective Disorders, 184, 116–122.CrossRefGoogle ScholarPubMed
Deserno, L., Sterzer, P., Wüstenberg, T., Heinz, A., & Schlagenhauf, F. (2012). Reduced prefrontal-parietal effective connectivity and working memory deficits in schizophrenia. The Journal of Neuroscience, 32, 12–20.CrossRefGoogle Scholar
Dickinson, T., Becerra, R., & Coombes, J. (2017). Executive functioning deficits among adults with bipolar disorder (types I and II): A systematic review and meta-analysis. Journal of Affective Disorders, 218, 407–427.CrossRefGoogle ScholarPubMed
Ekman, P, & Friesen, WV. (1976). Measuring facial movement. J Nonverbal Behav, 1, 56–75.CrossRefGoogle Scholar
Fahim, C., Stip, E., Mancini-Marie, A., Potvin, S., & Malaspina, D. (2007). Orbitofrontal dysfunction in a monozygotic twin discordant for postpartum affective psychosis: A functional magnetic resonance imaging study. Bipolar Disorders, 9, 541–545.CrossRefGoogle Scholar
Fernández-Corcuera, P., Salvador, R., Monté, G. C., Salvador Sarró, S., Goikolea, J. M., Amann, B., … Pomarol-Clotet, E. (2013). Bipolar depressed patients show both failure to activate and failure to de-activate during performance of a working memory task. Journal of Affective Disorders, 148, 170–178.CrossRefGoogle ScholarPubMed
Fusar-Poli, P., Borgwardt, S., Crescini, A., Deste, G., Kempton, M. J., Lawrie, S., … Sacchetti, E. (2011). Neuroanatomy of vulnerability to psychosis: A voxel-based meta-analysis. Neuroscience & Biobehavioral Reviews, 35, 1175–1185.CrossRefGoogle ScholarPubMed
Fusar-Poli, P., Placentino, A., Carletti, F., Landi, P., Allen, P., Surguladze, S., … Politi, P. (2009). Functional atlas of emotional faces processing: A voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry & Neuroscience: JPN, 34, 418–432.Google ScholarPubMed
Fusté, M., Pauls, A., Worker, A., Reinders, A. A. T. S., Simmons, A., Williams, S. C. R., … Dazzan, P. (2017). Brain structure in women at risk of postpartum psychosis: An MRI study. Translational Psychiatry, 7, 1286.CrossRefGoogle Scholar
Gingnell, M., Bannbers, E., Moes, H., Engman, J., Sylvén, S., Skalkidou, A., … Sundström-Poromaa, I. (2015). Emotion reactivity is increased 4–6 weeks postpartum in healthy women: A longitudinal fMRI study. PLoS One, 10, e0128964.CrossRefGoogle ScholarPubMed
Glahn, D. C., Ragland, J. D., Abramoff, A., Barrett, J., Laird, A. R., Bearden, C. E., & Velligan, D. I. (2005). Beyond hypofrontality: A quantitative meta-analysis of functional neuroimaging studies of working memory in schizophrenia. Human Brain Mapping, 25, 60–69.CrossRefGoogle Scholar
Grave, J., Soares, S. C., Martins, M. J., & Madeira, N. (2017). Facial emotion processing in schizophrenia: A review of behavioural and neural correlates. International Journal of Clinical Neurosciences and Mental Health, 4(Suppl. 3), S06.Google Scholar
Hanford, L. C., Nazarov, A., Hall, G. B., & Sassi, R. B. (2016). Cortical thickness in bipolar disorder: A systematic review. Bipolar Disorders, 18, 4–18.CrossRefGoogle ScholarPubMed
Henseler, I., Falkai, P., & Gruber, O. (2009). A systematic fMRI investigation of the brain systems subserving different working memory components in schizophrenia. European Journal of Neuroscience, 30, 693–702.CrossRefGoogle Scholar
Houenou, J., Frommberger, J., Carde, S., Glasbrenner, M., Diener, C., Leboyer, M., & Wessa, M. (2011). Neuroimaging-based markers of bipolar disorder: Evidence from two meta-analyses. Journal of Affective Disorders, 132, 344–355.CrossRefGoogle ScholarPubMed
IBM Corp. (2016). IBM SPSS Statistics for Macintosh. Armonk, NY: IBM Corp. 24.0.Google Scholar
Jogia, J., Dima, D., Kumari, V., & Frangou, S. (2012). Frontopolar cortical inefficiency may underpin reward and working memory dysfunction in bipolar disorder. The World Journal of Biological Psychiatry, 13, 605–615.CrossRefGoogle ScholarPubMed
Jones, I., Chandra, P. S., Dazzan, P., & Howard, L. M. (2014). Bipolar disorder, affective psychosis, and schizophrenia in pregnancy and the post-partum period. Lancet (London, England), 384, 1789–1799.CrossRefGoogle ScholarPubMed
Jones, I., & Craddock, N. (2001). Familiality of the puerperal trigger in bipolar disorder: Results of a family study. American Journal of Psychiatry, 158, 913–917.CrossRefGoogle ScholarPubMed
Kim, M. A., Tura, E., Potkin, S. G., Fallon, J. H., Manoach, D. S., Calhoun VD, F. B. I. R. N., & Turner, J. A. (2010). Working memory circuitry in schizophrenia shows widespread cortical inefficiency and compensation. Schizophrenia Research, 117, 42–51.CrossRefGoogle ScholarPubMed
Kohler, C. G., Walker, J. B., Martin, E. A., Healey, K. M., & Moberg, P. J. (2010). Facial emotion perception in schizophrenia: A meta-analytic review. Schizophrenia Bulletin, 36, 1009–1019.CrossRefGoogle ScholarPubMed
Kupferschmidt, D. A., & Zakzanis, K. K. (2011). Toward a functional neuroanatomical signature of bipolar disorder: Quantitative evidence from the neuroimaging literature. Psychiatry Research, 193, 71–79.CrossRefGoogle Scholar
Kuroki, N., Shenton, M. E., Salisbury, D. F., Hirayasu, Y., Onitsuka, T., Ersner-Hershfield, H., … McCarley, R. W. (2006). Middle and inferior temporal gyrus gray matter volume abnormalities in first-episode schizophrenia: An MRI study. The American Journal of Psychiatry, 163, 2103–2110.CrossRefGoogle Scholar
Kyriakopoulos, M., Dima, D., Roiser, J. P., Corrigall, R., Barker, G. J., & Frangou, S. (2012). Abnormal functional activation and connectivity in the working memory network in early-onset schizophrenia. Journal of the American Academy of Child & Adolescent Psychiatry, 51, 911–920. e2.CrossRefGoogle ScholarPubMed
Lagopoulos, J., Ivanovski, B., & Malhi, G. S. (2007). An event-related functional MRI study of working memory in euthymic bipolar disorder. Journal of Psychiatry & Neuroscience: JPN, 32, 174–184.Google ScholarPubMed
Lanczik, M., Fritze, J., Hofmann, E., Schulz, C., Knoche, M., & Becker, T. (1998). Ventricular abnormality in patients with postpartum psychoses. Archives of Women's Mental Health, 1, 45–47.CrossRefGoogle Scholar
Li, H., Chan, R. C. K., Gong, Q., Liu, Y., Liu, S., Shum, D., & Ma, Z. (2012). Facial emotion processing in patients with schizophrenia and their non-psychotic siblings: A functional magnetic resonance imaging study. Schizophrenia Research, 134, 143–150.CrossRefGoogle ScholarPubMed
Loeb, F. F., Zhou, X., Craddock, K. E. S., Shora, L., Broadnax, D. D., Gochman, P., … Liu, S. (2018). Reduced functional brain activation and connectivity during a working memory task in childhood-onset schizophrenia. Journal of the American Academy of Child & Adolescent Psychiatry, 57, 166–174.CrossRefGoogle ScholarPubMed
Malhi, G. S., Ivanovski, B., Hadzi-Pavlovic, D., Mitchell, P. B., Vieta, E., & Sachdev, P. (2007a). Neuropsychological deficits and functional impairment in bipolar depression, hypomania and euthymia. Bipolar Disorders, 9, 114–125.CrossRefGoogle Scholar
Malhi, G. S., Lagopoulos, J., Owen, A. M., Ivanovski, B., Shnier, R., & Sachdev, P. (2007b). Reduced activation to implicit affect induction in euthymic bipolar patients: An fMRI study. Journal of Affective Disorders, 97, 109–122.CrossRefGoogle Scholar
Minzenberg, M. J., Laird, A. R., Thelen, S., Carter, C. S., & Glahn, D. C. (2009). Meta-analysis of 41 functional neuroimaging studies of executive function in schizophrenia. Archives of General Psychiatry, 66, 811.CrossRefGoogle Scholar
Modinos, G., Tseng, H.-H., Falkenberg, I., Samson, C., McGuire, P., & Allen, P. (2015). Neural correlates of aberrant emotional salience predict psychotic symptoms and global functioning in high-risk and first-episode psychosis. Social Cognitive and Affective Neuroscience, 10, 1429–1436.CrossRefGoogle ScholarPubMed
Monks, P. J., Thompson, J. M., Bullmore, E. T., Suckling, J., Brammer, M. J., Williams, S. C., … Curtis, V. A. (2004). A functional MRI study of working memory task in euthymic bipolar disorder: Evidence for task-specific dysfunction. Bipolar Disorders, 6, 550–564.CrossRefGoogle ScholarPubMed
Mukherjee, P., Whalley, H. C., McKirdy, J. W., McIntosh, A. M., Johnstone, E. C., Lawrie, S. M., & Hall, J. (2012). Lower effective connectivity between amygdala and parietal regions in response to fearful faces in schizophrenia. Schizophrenia Research, 134, 118–124.CrossRefGoogle Scholar
Munk-Olsen, T., Laursen, T. M., Pedersen, C. B., Mors, O., & Mortensen, P. B. (2006). New parents and mental disorders. JAMA, 296, 2582.CrossRefGoogle ScholarPubMed
Nielsen, J. D., Madsen, K. H., Wang, Z., Liu, Z., Friston, K. J., & Zhou, Y. (2017). Working memory modulation of frontoparietal network connectivity in first-episode schizophrenia. Cerebral Cortex, 27, 3832–3841.CrossRefGoogle ScholarPubMed
Onitsuka, T., Shenton, M. E., Salisbury, D. F., Dickey, C. C., Kasai, K., Toner, S. K., … McCarley, R. W. (2004). Middle and inferior temporal gyrus gray matter volume abnormalities in chronic schizophrenia: An MRI study. The American Journal of Psychiatry, 161, 1603–1611.CrossRefGoogle Scholar
Owen, A. M., McMillan, K. M., Laird, A. R., & Bullmore, E. (2005). N-back working memory paradigm: A meta-analysis of normative functional neuroimaging studies. Human Brain Mapping, 25, 46–59.CrossRefGoogle ScholarPubMed
Phillips, M. L., & Swartz, H. A. (2014). A critical appraisal of neuroimaging studies of bipolar disorder: Toward a new conceptualization of underlying neural circuitry and a road map for future research. The American Journal of Psychiatry, 171, 829–843.CrossRefGoogle Scholar
Quidé, Y., Morris, R. W., Shepherd, A. M., Rowland, J. E., & Green, M. J. (2013). Task-related fronto-striatal functional connectivity during working memory performance in schizophrenia. Schizophrenia Research, 150, 468–475.CrossRefGoogle Scholar
Ragland, J. D., Moelter, S. T., Bhati, M. T., Valdez, J. N., Kohler, C. G., Siegel, S. J., … Gur, R. E. (2008). Effect of retrieval effort and switching demand on fMRI activation during semantic word generation in schizophrenia. Schizophrenia Research, 99, 312–323.CrossRefGoogle Scholar
Röder, C. H., Dieleman, S., van der Veen, F. M., & Linden, D. (2013). Systematic review of the influence of antipsychotics on the blood oxygenation level-dependent signal of functional magnetic resonance imaging. Current Medicinal Chemistry, 20, 448–461.Google Scholar
Schneider, F., Habel, U., Reske, M., Kellermann, T., Stöcker, T., Shah, N. J., … Gaebel, W. (2007). Neural correlates of working memory dysfunction in first-episode schizophrenia patients: An fMRI multi-center study. Schizophrenia Research, 89, 198–210.CrossRefGoogle ScholarPubMed
Sit, D., Rothschild, A. J., & Wisner, K. L. (2006). A review of postpartum psychosis. Journal of Women's Health, 15, 352–368.CrossRefGoogle ScholarPubMed
Stegmayer, K., Usher, J., Trost, S., Henseler, I., Tost, H., Rietschel, M., … Gruber, O. (2015). Disturbed cortico–amygdalar functional connectivity as pathophysiological correlate of working memory deficits in bipolar affective disorder. European Archives of Psychiatry and Clinical Neuroscience, 265, 303–311.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, 136–145.CrossRefGoogle Scholar
Thermenos, H. W., Goldstein, J. M., Milanovic, S. M., Whitfield-Gabrieli, S., Makris, N., Laviolette, P., … Seidman, L. J. (2010). An fMRI study of working memory in persons with bipolar disorder or at genetic risk for bipolar disorder. American Journal of Medical Genetics. Part B. Neuropsychiatric Genetics, 153, 120–131.Google Scholar
Townsend, J. D., Torrisi, S. J., Lieberman, M. D., Sugar, C. A., Bookheimer, S. Y., & Altshuler, L. L. (2013). Frontal-amygdala connectivity alterations during emotion downregulation in bipolar I disorder. Biological Psychiatry, 73, 127–135.CrossRefGoogle ScholarPubMed
Vita, A., De Peri, L., Deste, G., Barlati, S., & Sacchetti, E. (2015). The effect of antipsychotic treatment on cortical gray matter changes in schizophrenia: Does the class matter? A meta-analysis and meta-regression of longitudinal magnetic resonance imaging studies. Biological Psychiatry, 78, 403–412.CrossRefGoogle Scholar
Winkler, AM, Ridgway, GR, Webster, MA, Smith, SM, & Nichols, TE. (2014). Permutation inference for the general linear model. Neuroimage, 92, 381–97.CrossRefGoogle ScholarPubMed
Wu, S., Wang, H., Chen, C., Zou, J., Huang, H., Li, P., … Wang, G. (2017). Task performance modulates functional connectivity involving the dorsolateral prefrontal cortex in patients with schizophrenia. Frontiers in Psychology, 8, 56.CrossRefGoogle ScholarPubMed
Wu, G., Wang, Y., Mwansisya, T. E., Pu, W., Zhang, H., Liu, C., … Shan, B. (2014). Effective connectivity of the posterior cingulate and medial prefrontal cortices relates to working memory impairment in schizophrenic and bipolar patients. Schizophrenia Research, 158, 85–90.CrossRefGoogle ScholarPubMed
Zhang, L., Opmeer, E. M., van der Meer, L., Aleman, A., Ćurčić-Blake, B., & Ruhé, H. G. (2018). Altered frontal-amygdala effective connectivity during effortful emotion regulation in bipolar disorder. Bipolar Disorders, 20, 349-358.CrossRefGoogle ScholarPubMed
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