Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-24T15:12:16.029Z Has data issue: false hasContentIssue false
  • English
  • Français

Improvement in prefrontal thalamic connectivity during the early course of the illness in recent-onset psychosis: a 12-month longitudinal follow-up resting-state fMRI study

Published online by Cambridge University Press:  16 December 2020

Daniel Bergé Open the ORCID record for Daniel Bergé [Opens in a new window] ,
Tyler A. Lesh ,
Jason Smucny  and
Cameron S. Carter
Daniel Bergé*
Affiliation:
Neuroimaging Group, Neuroscience Department, IMIM (Hospital del Mar Research Institute), Barcelona, Spain Autonomous University of Barcelona, Barcelona, Spain CIBERSAM, Madrid, Spain
Tyler A. Lesh
Affiliation:
Department of Psychiatry and Behavioral Sciences, University of California (UCDAVIS), Davis, CA, USA
Jason Smucny
Affiliation:
Department of Psychiatry and Behavioral Sciences, University of California (UCDAVIS), Davis, CA, USA
Cameron S. Carter
Affiliation:
Department of Psychiatry and Behavioral Sciences, University of California (UCDAVIS), Davis, CA, USA
*
Author for correspondence: Daniel Bergé, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Previous research in resting-state functional magnetic resonance imaging (rs-fMRI) has shown a mixed pattern of disrupted thalamocortical connectivity in psychosis. The clinical meaning of these findings and their stability over time remains unclear. We aimed to study thalamocortical connectivity longitudinally over a 1-year period in participants with recent-onset psychosis.

Methods

To this purpose, 129 individuals with recent-onset psychosis and 87 controls were clinically evaluated and scanned using rs-fMRI. Among them, 43 patients and 40 controls were re-scanned and re-evaluated 12 months later. Functional connectivity between the thalamus and the rest of the brain was calculated using a seed to voxel approach, and then compared between groups and correlated with clinical features cross-sectionally and longitudinally.

Results

At baseline, participants with recent-onset psychosis showed increased connectivity (compared to controls) between the thalamus and somatosensory and temporal regions (k = 653, T = 5.712), as well as decreased connectivity between the thalamus and left cerebellum and right prefrontal cortex (PFC; k = 201, T = −4.700). Longitudinal analyses revealed increased connectivity over time in recent-onset psychosis (relative to controls) in the right middle frontal gyrus.

Conclusions

Our results support the concept of abnormal thalamic connectivity as a core feature in psychosis. In agreement with a non-degenerative model of illness in which functional changes occur early in development and do not deteriorate over time, no evidence of progressive deterioration of connectivity during early psychosis was observed. Indeed, regionally increased connectivity between thalamus and PFC was observed.

Keywords

schizophreniafirst-episode psychosisfMRIresting state
Type
Original Article
Information
Psychological Medicine , Volume 52 , Issue 13 , October 2022 , pp. 2713 - 2721
Check for updates
Copyright
Copyright © The Author(s), 2020. 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.)

References

Aas, I. M. (2010). Global Assessment of Functioning (GAF): Properties and frontier of current knowledge. Annals of General Psychiatry, 9, 20. doi: 10.1186/1744-859X-9-20CrossRefGoogle ScholarPubMed
Andreasen, N. C. (1984). Scale for the assessment of positive symptoms (SAPS). Iowa City: University of Iowa Iowa City.Google Scholar
Andreasen, N. C. (1989). The Scale for the Assessment of Negative Symptoms (SANS): Conceptual and theoretical foundations. The British Journal of Psychiatry, 155(S7), 49–52. doi: 10.1192/S0007125000291496CrossRefGoogle Scholar
Andreasen, N. C., Paradiso, S., & O'Leary, D. S. (1998). ‘Cognitive dysmetria’ as an integrative theory of schizophrenia: A dysfunction in cortical-subcortical-cerebellar circuitry? Schizophrenia Bulletin, 24(2), 203–218.CrossRefGoogle Scholar
Anticevic, A., Cole, M. W., Repovs, G., Murray, J. D., Brumbaugh, M. S., Winkler, A. M., … Glahn, D. C. (2014a). Characterizing thalamo-cortical disturbances in schizophrenia and bipolar illness. Cerebral Cortex (New York, NY: 1991), 24(12), 3116–3130. doi: 10.1093/cercor/bht165Google Scholar
Anticevic, A., Haut, K., Murray, J. D., Repovs, G., Yang, G. J., Diehl, C., … Cannon, T. D. (2015). Association of thalamic dysconnectivity and conversion to psychosis in youth and young adults at elevated clinical risk. JAMA Psychiatry, 72(9), 882–891. doi: 10.1001/jamapsychiatry.2015.0566CrossRefGoogle Scholar
Anticevic, A., Yang, G., Savic, A., Murray, J. D., Cole, M. W., Repovs, G., … Glahn, D. C. (2014b). Mediodorsal and visual thalamic connectivity differ in schizophrenia and bipolar disorder with and without psychosis history. Schizophrenia Bulletin, 40(6), 1227–1243. doi: 10.1093/schbul/sbu100CrossRefGoogle Scholar
Avram, M., Brandl, F., Bäuml, J., & Sorg, C. (2018). Cortico-thalamic hypo- and hyperconnectivity extend consistently to basal ganglia in schizophrenia. Neuropsychopharmacology, 43(11), 2239–2248. doi: 10.1038/s41386-018-0059-zCrossRefGoogle Scholar
Birchwood, M., Todd, P., & Jackson, C. (1998). Early intervention in psychosis. The critical period hypothesis. The British Journal of Psychiatry. Supplement, 172(33), 53–59.CrossRefGoogle ScholarPubMed
Chai, X. J., Castañón, A. N., Ongür, D., & Whitfield-Gabrieli, S. (2012). Anticorrelations in resting state networks without global signal regression. NeuroImage, 59(2), 1420–1428. doi: 10.1016/j.neuroimage.2011.08.048CrossRefGoogle ScholarPubMed
Cheng, W., Palaniyappan, L., Li, M., Kendrick, K. M., Zhang, J., Luo, Q., … Feng, J. (2015). Voxel-based, brain-wide association study of aberrant functional connectivity in schizophrenia implicates thalamocortical circuitry. NPJ Schizophrenia, 1, 15016. doi: 10.1038/npjschz.2015.16CrossRefGoogle ScholarPubMed
Cheng, H., Skosnik, P., Pruce, B., Brumbaugh, M., Vollmer, J., Fridberg, D., … Newman, S. (2014). Resting state functional magnetic resonance imaging reveals distinct brain activity in heavy cannabis users – a multi-voxel pattern analysis. Journal of Psychopharmacology (Oxford, England), 28(11), 1030–1040. doi: 10.1177/0269881114550354CrossRefGoogle ScholarPubMed
Cho, K. I. K., Kim, M., Yoon, Y. B., Lee, J., Lee, T. Y., & Kwon, J. S. (2019). Disturbed thalamocortical connectivity in unaffected relatives of schizophrenia patients with a high genetic loading. The Australian and New Zealand Journal of Psychiatry, 53(9), 889–895. doi: 10.1177/0004867418824020CrossRefGoogle ScholarPubMed
Desikan, R. S., Ségonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., … Killiany, R. J. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage, 31(3), 968–980. doi: 10.1016/j.neuroimage.2006.01.021CrossRefGoogle ScholarPubMed
Dumontheil, I., Burgess, P. W., & Blakemore, S.-J. (2008). Development of rostral prefrontal cortex and cognitive and behavioural disorders. Developmental Medicine and Child Neurology, 50(3), 168–181. doi: 10.1111/j.1469-8749.2008.02026.xCrossRefGoogle ScholarPubMed
Fair, D., Bathula, D., Mills, K. L., Costa Dias, T. G., Blythe, M. S., Zhang, D., … Nagel, B. J. (2010). Maturing thalamocortical functional connectivity across development. Frontiers in Systems Neuroscience, 4(10), 1–10. doi: 10.3389/fnsys.2010.00010.Google ScholarPubMed
Ferri, J., Ford, J. M., Roach, B. J., Turner, J. A., van Erp, T. G., Voyvodic, J., … Mathalon, D. H. (2018). Resting-state thalamic dysconnectivity in schizophrenia and relationships with symptoms. Psychological Medicine, 48(15), 1–8. doi: 10.1017/S003329171800003X.CrossRefGoogle ScholarPubMed
Fornito, A., Zalesky, A., Pantelis, C., & Bullmore, E. T. (2012). Schizophrenia, neuroimaging and connectomics. NeuroImage, 62(4), 2296–2314. doi: 10.1016/j.neuroimage.2011.12.090CrossRefGoogle ScholarPubMed
Friston, K. J., Worsley, K. J., Frackowiak, R. S., Mazziotta, J. C., & Evans, A. C. (1994). Assessing the significance of focal activations using their spatial extent. Human Brain Mapping, 1(3), 210–220. doi: 10.1002/hbm.460010306CrossRefGoogle ScholarPubMed
Giraldo-Chica, M., & Woodward, N. D. (2017). Review of thalamocortical resting-state fMRI studies in schizophrenia. Schizophrenia Research, 180, 58–63. doi: 10.1016/j.schres.2016.08.005CrossRefGoogle Scholar
Gold, S., Arndt, S., Nopoulos, P., O'Leary, D. S., & Andreasen, N. C. (1999). Longitudinal study of cognitive function in first-episode and recent-onset schizophrenia. The American Journal of Psychiatry, 156(9), 1342–1348. doi: 10.1176/ajp.156.9.1342CrossRefGoogle ScholarPubMed
Halassa, M. M., & Kastner, S. (2017). Thalamic functions in distributed cognitive control. Nature Neuroscience, 20(12), 1669–1679. doi: 10.1038/s41593-017-0020-1CrossRefGoogle ScholarPubMed
Hwang, K., Bertolero, M. A., Liu, W. B., & D'Esposito, M. (2017). The human thalamus is an integrative hub for functional brain networks. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 37(23), 5594–5607. doi: 10.1523/JNEUROSCI.0067-17.2017CrossRefGoogle ScholarPubMed
Karcher, N. R., Rogers, B. P., & Woodward, N. D. (2019). Functional connectivity of the striatum in schizophrenia and psychotic bipolar disorder. Biological Psychiatry. Cognitive Neuroscience and Neuroimaging, 4(11), 956–965. doi: 10.1016/j.bpsc.2019.05.017CrossRefGoogle ScholarPubMed
Kaufmann, T., Alnæs, D., Doan, N. T., Brandt, C. L., Andreassen, O. A., & Westlye, L. T. (2017). Delayed stabilization and individualization in connectome development are related to psychiatric disorders. Nature Neuroscience, 20(4), 513–515. doi: 10.1038/nn.4511CrossRefGoogle ScholarPubMed
Levitt, J. J., Nestor, P. G., Levin, L., Pelavin, P., Lin, P., Kubicki, M., … Rathi, Y. (2017). Reduced structural connectivity in frontostriatal white matter tracts in the associative loop in schizophrenia. The American Journal of Psychiatry, 174(11), 1102–1111. doi: 10.1176/appi.ajp.2017.16091046CrossRefGoogle Scholar
Liu, H., Fan, G., Xu, K., & Wang, F. (2011). Changes in cerebellar functional connectivity and anatomical connectivity in schizophrenia: A combined resting-state fMRI and DTI study. Journal of Magnetic Resonance Imaging: JMRI, 34(6), 1430–1438. doi: 10.1002/jmri.22784CrossRefGoogle Scholar
Lukoff, D., Nuechterlein, K. H., & Ventura, J. (1986). Manual for the expanded brief psychiatric rating scale. Schizophrenia Bulletin, 12, 594–602.Google Scholar
Magnotta, V. A., Adix, M. L., Caprahan, A., Lim, K., Gollub, R., & Andreasen, N. C. (2008). Investigating connectivity between the cerebellum and thalamus in schizophrenia using diffusion tensor tractography: A pilot study. Psychiatry Research, 163(3), 193–200. doi: 10.1016/j.pscychresns.2007.10.005.CrossRefGoogle ScholarPubMed
Miller, D. J., Duka, T., Stimpson, C. D., Schapiro, S. J., Baze, W. B., McArthur, M. J., … Sherwood, C. C. (2012). Prolonged myelination in human neocortical evolution. Proceedings of the National Academy of Sciences of the USA, 109(41), 16480–16485. doi: 10.1073/pnas.1117943109CrossRefGoogle ScholarPubMed
Murphy, K., Birn, R. M., Handwerker, D. A., Jones, T. B., & Bandettini, P. A. (2009). The impact of global signal regression on resting state correlations: Are anti-correlated networks introduced? NeuroImage, 44(3), 893–905. doi: 10.1016/j.neuroimage.2008.09.036CrossRefGoogle ScholarPubMed
Niendam, T. A., Laird, A. R., Ray, K. L., Dean, Y. M., Glahn, D. C., & Carter, C. S. (2012). Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions. Cognitive, Affective & Behavioral Neuroscience, 12(2), 241–268. doi: 10.3758/s13415-011-0083-5CrossRefGoogle ScholarPubMed
Niendam, T. A., Ray, K. L., Iosif, A.-M., Lesh, T. A., Ashby, S. R., Patel, P. K., … Carter, C. S. (2018). Association of age at onset and longitudinal course of prefrontal function in youth with schizophrenia. JAMA Psychiatry, 75(12), 1252–1260. doi: 10.1001/jamapsychiatry.2018.2538CrossRefGoogle ScholarPubMed
Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage, 59(3), 2142–2154. doi: 10.1016/j.neuroimage.2011.10.018CrossRefGoogle ScholarPubMed
Sarpal, D. K., Robinson, D. G., Lencz, T., Argyelan, M., Ikuta, T., Karlsgodt, K., … Malhotra, A. K. (2015). Antipsychotic treatment and functional connectivity of the striatum in first-episode schizophrenia. JAMA Psychiatry, 72(1), 5–13. doi: 10.1001/jamapsychiatry.2014.1734CrossRefGoogle ScholarPubMed
Sheffield, J. M., & Barch, D. M. (2016). Cognition and resting-state functional connectivity in schizophrenia. Neuroscience and Biobehavioral Reviews, 61, 108–120. doi: 10.1016/j.neubiorev.2015.12.007CrossRefGoogle Scholar
Skåtun, K. C., Kaufmann, T., Brandt, C. L., Doan, N. T., Alnæs, D., Tønnesen, S., … Westlye, L. T. (2018). Thalamo-cortical functional connectivity in schizophrenia and bipolar disorder. Brain Imaging and Behavior, 12(3), 640–652. doi: 10.1007/s11682-017-9714-yGoogle ScholarPubMed
Smucny, J., Lesh, T. A., & Carter, C. S. (2019). Baseline frontoparietal task-related BOLD activity as a predictor of improvement in clinical symptoms at 1-year follow-up in recent-onset psychosis. The American Journal of Psychiatry, 176(10), 839–845. doi: 10.1176/appi.ajp.2019.18101126CrossRefGoogle ScholarPubMed
Smucny, J., Lesh, T. A., Zarubin, V. C., Niendam, T. A., Ragland, J. D., Tully, L. M., … Carter, C. S. (2020). One-year stability of frontoparietal cognitive control network connectivity in recent onset schizophrenia: A task-related 3T fMRI study. Schizophrenia Bulletin, 46(5), 1249–1258. doi: 10.1093/schbul/sbz122.CrossRefGoogle Scholar
Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., … Joliot, M. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage, 15(1), 273–289. doi: 10.1006/nimg.2001.0978CrossRefGoogle ScholarPubMed
Viher, P. V., Docx, L., Van Hecke, W., Parizel, P. M., Sabbe, B., Federspiel, A., … Morrens, M. (2019). Aberrant fronto-striatal connectivity and fine motor function in schizophrenia. Psychiatry Research. Neuroimaging, 288, 44–50. doi: 10.1016/j.pscychresns.2019.04.010Google Scholar
Whitfield-Gabrieli, S., & Nieto-Castanon, A. (2012). Conn: A functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connectivity, 2(3), 125–141. doi: 10.1089/brain.2012.0073CrossRefGoogle ScholarPubMed
Woodward, N. D., & Heckers, S. (2016). Mapping thalamocortical functional connectivity in chronic and early stages of psychotic disorders. Biological Psychiatry, 79(12), 1016–1025. doi: 10.1016/j.biopsych.2015.06.026CrossRefGoogle ScholarPubMed
Woodward, N. D., Karbasforoushan, H., & Heckers, S. (2012). Thalamocortical dysconnectivity in schizophrenia. The American Journal of Psychiatry, 169(10), 1092–1099. doi: 10.1176/appi.ajp.2012.12010056.CrossRefGoogle Scholar
Supplementary material: PDF

Bergé et al. supplementary material

Bergé et al. supplementary material

Download Bergé et al. supplementary material(PDF)
PDF 650.4 KB