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Context-specific abnormalities of the central executive network in first-episode psychosis: relationship with cognition

Published online by Cambridge University Press:  23 November 2020

Deepak K. Sarpal*
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
Goda Tarcijonas
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
Finnegan J. Calabro
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA, USA
William Foran
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA
Gretchen L. Haas
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA Department of Psychology, University of Pittsburgh, Pittsburgh, PA, USA
Beatriz Luna
Affiliation:
Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA Department of Psychology, University of Pittsburgh, Pittsburgh, PA, USA Department of Pediatrics, University of Pittsburgh, Pittsburgh, PA, USA
Vishnu P. Murty
Affiliation:
Department of Psychology, Temple University, Philadelphia, PA, USA
*
Author for correspondence: Deepak K. Sarpal, E-mail: [email protected]

Abstract

Background

Cognitive impairments, which contribute to the profound functional deficits observed in psychotic disorders, have found to be associated with abnormalities in trial-level cognitive control. However, neural tasks operate within the context of sustained cognitive states, which can be assessed with ‘background connectivity’ following the removal of task effects. To date, little is known about the integrity of brain processes supporting the maintenance of a cognitive state in individuals with psychotic disorders. Thus, here we examine background connectivity during executive processing in a cohort of participants with first-episode psychosis (FEP).

Methods

The following fMRI study examined background connectivity of the dorsolateral prefrontal cortex (DLPFC), during working memory engagement in a group of 43 patients with FEP, relative to 35 healthy controls (HC). Findings were also examined in relation to measures of executive function.

Results

The FEP group relative to HC showed significantly lower background DLPFC connectivity with bilateral superior parietal lobule (SPL) and left inferior parietal lobule. Background connectivity between DLPFC and SPL was also positively associated with overall cognition across all subjects and in our FEP group. In comparison, resting-state frontoparietal connectivity did not differ between groups and was not significantly associated with overall cognition, suggesting that psychosis-related alterations in executive networks only emerged during states of goal-oriented behavior.

Conclusions

These results provide novel evidence indicating while frontoparietal connectivity at rest appears intact in psychosis, when engaged during a cognitive state, it is impaired possibly undermining cognitive control capacities in FEP.

Type
Original Article
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

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References

Al-Aidroos, N., Said, C. P., & Turk-Browne, N. B. (2012). Top-down attention switches coupling between low-level and high-level areas of human visual cortex. Proceedings of the National Academy of Sciences of the USA, 109(36), 1467514680. doi: 10.1073/pnas.1202095109.CrossRefGoogle ScholarPubMed
Andreasen, N. C., Pressler, M., Nopoulos, P., Miller, D., & Ho, B. C. (2010). Antipsychotic dose equivalents and dose-years: A standardized method for comparing exposure to different drugs. Biological Psychiatry, 67(3), 255262. doi: 10.1016/j.biopsych.2009.08.040.CrossRefGoogle ScholarPubMed
Arfanakis, K., Cordes, D., Haughton, V. M., Moritz, C. H., Quigley, M. A., & Meyerand, M. E. (2000). Combining independent component analysis and correlation analysis to probe interregional connectivity in fMRI task activation datasets. Magnetic Resonance Imaging, 18(8), 921930. doi: 10.1016/s0730-725x(00)00190-9.CrossRefGoogle ScholarPubMed
August, S. M., Kiwanuka, J. N., McMahon, R. P., & Gold, J. M. (2012). The MATRICS consensus cognitive battery (MCCB): Clinical and cognitive correlates. Schizophrenia Research, 134(1), 7682. doi: 10.1016/j.schres.2011.10.015.CrossRefGoogle ScholarPubMed
Barch, D. M., Carter, C. S., Braver, T. S., Sabb, F. W., MacDonald, A., 3rd, Noll, D. C., & Cohen, J. D. (2001). Selective deficits in prefrontal cortex function in medication-naive patients with schizophrenia. Archives of General Psychiatry, 58(3), 280288. doi: 10.1001/archpsyc.58.3.280.CrossRefGoogle ScholarPubMed
Barch, D. M., & Ceaser, A. (2012). Cognition in schizophrenia: Core psychological and neural mechanisms. Trends in Cognitive Sciences, 16(1), 2734. doi: 10.1016/j.tics.2011.11.015.CrossRefGoogle ScholarPubMed
Bowie, C. R., & Harvey, P. D. (2006). Cognitive deficits and functional outcome in schizophrenia. Neuropsychiatric Disease and Treatment, 2(4), 531536. doi: 10.2147/nedt.2006.2.4.531.CrossRefGoogle Scholar
Braver, T. S. (2012). The variable nature of cognitive control: A dual mechanisms framework. Trends in Cognitive Sciences, 16(2), 106113. doi: 10.1016/j.tics.2011.12.010.CrossRefGoogle ScholarPubMed
Braver, T. S., Reynolds, J. R., & Donaldson, D. I. (2003). Neural mechanisms of transient and sustained cognitive control during task switching. Neuron, 39(4), 713726. doi: 10.1016/s0896-6273(03)00466-5.CrossRefGoogle ScholarPubMed
Chadick, J. Z., & Gazzaley, A. (2011). Differential coupling of visual cortex with default or frontal-parietal network based on goals. Nature Neuroscience, 14(7), 830832. doi: 10.1038/nn.2823.CrossRefGoogle ScholarPubMed
Cohen, J. D., Braver, T. S., & Brown, J. W. (2002). Computational perspectives on dopamine function in prefrontal cortex. Current Opinions in Neurobiology, 12(2), 223229. doi: 10.1016/s0959-4388(02)00314-8.CrossRefGoogle ScholarPubMed
Cole, M. W., Bassett, D. S., Power, J. D., Braver, T. S., & Petersen, S. E. (2014). Intrinsic and task-evoked network architectures of the human brain. Neuron, 83(1), 238251. doi: 10.1016/j.neuron.2014.05.014.CrossRefGoogle ScholarPubMed
Cowan, N. (2017). The many faces of working memory and short-term storage. Psychonomic Bulletin & Review, 24(4), 11581170. doi: 10.3758/s13423-016-1191-6.CrossRefGoogle ScholarPubMed
D'Esposito, M., & Postle, B. R. (2015). The cognitive neuroscience of working memory. Annual Review of Psychology, 66, 115142. doi: 10.1146/annurev-psych-010814-015031.CrossRefGoogle ScholarPubMed
Dickinson, D., Ramsey, M. E., & Gold, J. M. (2007). Overlooking the obvious: A meta-analytic comparison of digit symbol coding tasks and other cognitive measures in schizophrenia. Archives of General Psychiatry, 64(5), 532542. doi: 10.1001/archpsyc.64.5.532.CrossRefGoogle Scholar
Dokucu, M. E. (2015). Neuromodulation treatments for schizophrenia. Current Treatment Options in Psychiatry, 2(3), 339348. doi: 10.1007/s40501-015-0055-4.CrossRefGoogle Scholar
Dong, D., Wang, Y., Chang, X., Luo, C., & Yao, D. (2018). Dysfunction of large-scale brain networks in schizophrenia: A meta-analysis of resting-state functional connectivity. Schizophrenia Bulletin, 44(1), 168181. doi: 10.1093/schbul/sbx034.CrossRefGoogle ScholarPubMed
Elkhetali, A. S., Fleming, L. L., Vaden, R. J., Nenert, R., Mendle, J. E., & Visscher, K. M. (2019). Background connectivity between frontal and sensory cortex depends on task state, independent of stimulus modality. NeuroImage, 184, 790800. doi: 10.1016/j.neuroimage.2018.09.040.CrossRefGoogle ScholarPubMed
Engle, R. W., Tuholski, S. W., Laughlin, J. E., & Conway, A. R. A. (1999). Working memory, short-term memory, and general fluid intelligence: A latent-variable approach. Journal of Experimental Psychology: General, 128(3), 309331. doi: 10.1037/0096-3445.128.3.309.CrossRefGoogle ScholarPubMed
Fox, M. D., & Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Reviews Neuroscience, 8(9), 700711. doi: 10.1038/nrn2201.CrossRefGoogle ScholarPubMed
Gong, J., Wang, J., Luo, X., Chen, G., Huang, H., Huang, R., … Wang, Y. (2020). Abnormalities of intrinsic regional brain activity in first-episode and chronic schizophrenia: A meta-analysis of resting-state functional MRI. Journal of Psychiatry & Neuroscience, 45(1), 5568. doi: 10.1503/jpn.180245.CrossRefGoogle ScholarPubMed
Green, M. F., Harris, J. G., & Nuechterlein, K. H. (2014). The MATRICS consensus cognitive battery: What we know 6 years later. The American Journal of Psychiatry, 171(11), 11511154. doi: 10.1176/appi.ajp.2014.14070936.CrossRefGoogle ScholarPubMed
Green, M. F., Kern, R. S., Braff, D. L., & Mintz, J. (2000). Neurocognitive deficits and functional outcome in schizophrenia: Are we measuring the ‘right stuff’? Schizophrenia Bulletin, 26(1), 119136. doi: 10.1093/oxfordjournals.schbul.a033430.CrossRefGoogle Scholar
Griffis, J. C., Elkhetali, A. S., Burge, W. K., Chen, R. H., & Visscher, K. M. (2015). Retinotopic patterns of background connectivity between V1 and fronto-parietal cortex are modulated by task demands. Frontiers in Human Neuroscience, 9, 338. doi: 10.3389/fnhum.2015.00338.CrossRefGoogle ScholarPubMed
Hahn, B., Robinson, B. M., Leonard, C. J., Luck, S. J., & Gold, J. M. (2018). Posterior parietal cortex dysfunction is central to working memory storage and broad cognitive deficits in schizophrenia. The Journal of Neuroscience, 38(39), 83788387. doi: 10.1523/JNEUROSCI.0913-18.2018.CrossRefGoogle Scholar
Haynes, J. D., Tregellas, J., & Rees, G. (2005). Attentional integration between anatomically distinct stimulus representations in early visual cortex. Proceedings of the National Academy of Sciences of the USA, 102(41), 1492514930. doi: 10.1073/pnas.0501684102.CrossRefGoogle ScholarPubMed
Jalbrzikowski, M., Murty, V. P., Stan, P. L., Saifullan, J., Simmonds, D., Foran, W., … Luna, B. (2017). Differentiating between clinical and behavioral phenotypes in first-episode psychosis during maintenance of visuospatial working memory. Schizophrenia Research, 197, 357364. doi:10.1016/j.schres.2017.11.012.CrossRefGoogle ScholarPubMed
Jarskog, L. F., Dong, Z., Kangarlu, A., Colibazzi, T., Girgis, R. R., Kegeles, L. S., … Lieberman, J. A. (2013). Effects of davunetide on N-acetylaspartate and choline in dorsolateral prefrontal cortex in patients with schizophrenia. Neuropsychopharmacology, 38(7), 12451252. doi: 10.1038/npp.2013.23.CrossRefGoogle ScholarPubMed
Karlsgodt, K. H., Sanz, J., van Erp, T. G., Bearden, C. E., Nuechterlein, K. H., & Cannon, T. D. (2009). Re-evaluating dorsolateral prefrontal cortex activation during working memory in schizophrenia. Schizophrenia Research, 108(1–3), 143150. doi: 10.1016/j.schres.2008.12.025.CrossRefGoogle Scholar
Lewis, D. A., & Gonzalez-Burgos, G. (2008). Neuroplasticity of neocortical circuits in schizophrenia. Neuropsychopharmacology, 33(1), 141165. doi: 10.1038/sj.npp.1301563.CrossRefGoogle Scholar
Li, S., Hu, N., Zhang, W., Tao, B., Dai, J., Gong, Y., … Lui, S. (2019). Dysconnectivity of multiple brain networks in schizophrenia: A meta-analysis of resting-state functional connectivity. Frontiers in Psychiatry, 10, 482. doi: 10.3389/fpsyt.2019.00482.CrossRefGoogle ScholarPubMed
Littow, H., Huossa, V., Karjalainen, S., Jaaskelainen, E., Haapea, M., Miettunen, J., … Kiviniemi, V. J. (2015). Aberrant functional connectivity in the default mode and central executive networks in subjects with schizophrenia – a whole-brain resting-state ICA study. Frontiers in Psychiatry, 6, 26. doi: 10.3389/fpsyt.2015.00026.CrossRefGoogle ScholarPubMed
Manivannan, A., Foran, W., Jalbrzikowski, M., Murty, V. P., Haas, G. L., Tarcijonas, G., … Sarpal, D. K. (2019). Association between duration of untreated psychosis and frontostriatal connectivity during maintenance of visuospatial working memory. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 4(5), 454461. doi:10.1016/j.bpsc.2019.01.007.Google ScholarPubMed
Manoliu, A., Riedl, V., Zherdin, A., Muhlau, M., Schwerthoffer, D., Scherr, M., … Sorg, C. (2014). Aberrant dependence of default mode/central executive network interactions on anterior insular salience network activity in schizophrenia. Schizophrenia Bulletin, 40(2), 428437. doi: 10.1093/schbul/sbt037.CrossRefGoogle Scholar
Marek, S., & Dosenbach, N. U. F. (2018). The frontoparietal network: Function, electrophysiology, and importance of individual precision mapping. Dialogues in Clinical Neuroscience, 20(2), 133140. doi: 10.31887/DCNS.2018.20.2/smarek.CrossRefGoogle ScholarPubMed
Mesholam-Gately, R. I., Giuliano, A. J., Goff, K. P., Faraone, S. V., & Seidman, L. J. (2009). Neurocognition in first-episode schizophrenia: A meta-analytic review. Neuropsychology, 23(3), 315336. doi: 10.1037/a0014708.CrossRefGoogle ScholarPubMed
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(8), 811822. doi: 10.1001/archgenpsychiatry.2009.91.CrossRefGoogle Scholar
Mitchell, D. J., & Cusack, R. (2008). Flexible, capacity-limited activity of posterior parietal cortex in perceptual as well as visual short-term memory tasks. Cerebral Cortex, 18(8), 17881798. doi: 10.1093/cercor/bhm205.CrossRefGoogle ScholarPubMed
Murty, V. P., Shah, H., Montez, D., Foran, W., Calabro, F., & Luna, B. (2018). Age-related trajectories of functional coupling between the VTA and nucleus accumbens depend on motivational state. The Journal of Neuroscience, 38(34), 74207427. doi: 10.1523/JNEUROSCI.3508-17.2018.CrossRefGoogle ScholarPubMed
Nagel, B. J., Herting, M. M., Maxwell, E. C., Bruno, R., & Fair, D. (2013). Hemispheric lateralization of verbal and spatial working memory during adolescence. Brain and Cognition, 82(1), 5868. doi: 10.1016/j.bandc.2013.02.007.CrossRefGoogle ScholarPubMed
Norman-Haignere, S. V., McCarthy, G., Chun, M. M., & Turk-Browne, N. B. (2012). Category-selective background connectivity in ventral visual cortex. Cerebral Cortex, 22(2), 391402. doi: 10.1093/cercor/bhr118.CrossRefGoogle ScholarPubMed
Nuechterlein, K. H., Green, M. F., Kern, R. S., Baade, L. E., Barch, D. M., Cohen, J. D., … Marder, S. R. (2008). The MATRICS consensus cognitive battery, part 1: Test selection, reliability, and validity. The American Journal of Psychiatry, 165(2), 203213. doi: 10.1176/appi.ajp.2007.07010042.CrossRefGoogle ScholarPubMed
O'Neill, A., Mechelli, A., & Bhattacharyya, S. (2019). Dysconnectivity of large-scale functional networks in early psychosis: A meta-analysis. Schizophrenia Bulletin, 45(3), 579590. doi: 10.1093/schbul/sby094.CrossRefGoogle ScholarPubMed
Perlstein, W. M., Carter, C. S., Noll, D. C., & Cohen, J. D. (2001). Relation of prefrontal cortex dysfunction to working memory and symptoms in schizophrenia. The American Journal of Psychiatry, 158(7), 11051113. doi: 10.1176/appi.ajp.158.7.1105.CrossRefGoogle Scholar
Potkin, S. G., Turner, J. A., Brown, G. G., McCarthy, G., Greve, D. N., & Glover, G. H., … Fbirn. (2009). Working memory and DLPFC inefficiency in schizophrenia: The FBIRN study. Schizophrenia Bulletin, 35(1), 1931. doi: 10.1093/schbul/sbn162.CrossRefGoogle ScholarPubMed
Ray, K. L., Lesh, T. A., Howell, A. M., Salo, T. P., Ragland, J. D., MacDonald, A. W., … Carter, C. S. (2017). Functional network changes and cognitive control in schizophrenia. NeuroImage: Clinical, 15, 161170. doi: 10.1016/j.nicl.2017.05.001.CrossRefGoogle Scholar
Reynolds, J. R., O'Reilly, R. C., Cohen, J. D., & Braver, T. S. (2012). The function and organization of lateral prefrontal cortex: A test of competing hypotheses. PLoS ONE, 7(2), e30284. doi: 10.1371/journal.pone.0030284.CrossRefGoogle ScholarPubMed
Reynolds, J. R., West, R., & Braver, T. (2009). Distinct neural circuits support transient and sustained processes in prospective memory and working memory. Cerebral Cortex, 19(5), 12081221. doi: 10.1093/cercor/bhn164.CrossRefGoogle ScholarPubMed
Rund, B. R., Melle, I., Friis, S., Johannessen, J. O., Larsen, T. K., Midboe, L. J., … McGlashan, T. (2007). The course of neurocognitive functioning in first-episode psychosis and its relation to premorbid adjustment, duration of untreated psychosis, and relapse. Schizophrenia Research, 91(1–3), 132140. doi: 10.1016/j.schres.2006.11.030.CrossRefGoogle ScholarPubMed
Seidman, L. J., Shapiro, D. I., Stone, W. S., Woodberry, K. A., Ronzio, A., Cornblatt, B. A., … Woods, S. W. (2016). Association of neurocognition with transition to psychosis: Baseline functioning in the second phase of the North American prodrome longitudinal study. JAMA Psychiatry, 73(12), 12391248. doi: 10.1001/jamapsychiatry.2016.2479.CrossRefGoogle ScholarPubMed
Shamsi, S., Lau, A., Lencz, T., Burdick, K. E., DeRosse, P., Brenner, R., … Malhotra, A. K. (2011). Cognitive and symptomatic predictors of functional disability in schizophrenia. Schizophrenia Research, 126(1–3), 257264. doi: 10.1016/j.schres.2010.08.007.CrossRefGoogle Scholar
Sui, J., Pearlson, G. D., Du, Y., Yu, Q., Jones, T. R., Chen, J., … Calhoun, V. D. (2015). In search of multimodal neuroimaging biomarkers of cognitive deficits in schizophrenia. Biological Psychiatry, 78(11), 794804. doi: 10.1016/j.biopsych.2015.02.017.CrossRefGoogle Scholar
Szoke, A., Trandafir, A., Dupont, M. E., Meary, A., Schurhoff, F., & Leboyer, M. (2008). Longitudinal studies of cognition in schizophrenia: Meta-analysis. The British Journal of Psychiatry, 192(4), 248257. doi: 10.1192/bjp.bp.106.029009.CrossRefGoogle ScholarPubMed
Tompary, A., Al-Aidroos, N., & Turk-Browne, N. B. (2018). Attending to what and where: Background connectivity integrates categorical and spatial attention. Journal of Cognitive Neuroscience, 30(9), 12811297. doi: 10.1162/jocn_a_01284.CrossRefGoogle Scholar
Tregellas, J. R., Smucny, J., Harris, J. G., Olincy, A., Maharajh, K., Kronberg, E., … Freedman, R. (2014). Intrinsic hippocampal activity as a biomarker for cognition and symptoms in schizophrenia. The American Journal of Psychiatry, 171(5), 549556. doi: 10.1176/appi.ajp.2013.13070981.CrossRefGoogle Scholar
Van Snellenberg, J. X., Girgis, R. R., Horga, G., van de Giessen, E., Slifstein, M., Ojeil, N., … Abi-Dargham, A. (2016). Mechanisms of working memory impairment in schizophrenia. Biological Psychiatry, 80(8), 617626. doi: 10.1016/j.biopsych.2016.02.017.CrossRefGoogle Scholar
Woerner, M. G., Mannuzza, S., & Kane, J. M. (1988). Anchoring the BPRS: An aid to improved reliability. Psychopharmacology Bulletin, 24(1), 112117. Retrieved from https://pubmed.ncbi.nlm.nih.gov/3387514/.Google ScholarPubMed
Woodward, N. D., Rogers, B., & Heckers, S. (2011). Functional resting-state networks are differentially affected in schizophrenia. Schizophrenia Research, 130(1–3), 8693. doi: 10.1016/j.schres.2011.03.010.CrossRefGoogle Scholar
Xu, Y. (2017). Reevaluating the sensory account of visual working memory storage. Trends in Cognitive Sciences, 21(10), 794815. doi: 10.1016/j.tics.2017.06.013.CrossRefGoogle ScholarPubMed
Xu, Y., & Chun, M. M. (2006). Dissociable neural mechanisms supporting visual short-term memory for objects. Nature, 440(7080), 9195. doi: 10.1038/nature04262.CrossRefGoogle ScholarPubMed
Yarkoni, T., Poldrack, R. A., Nichols, T. E., Van Essen, D. C., & Wager, T. D. (2011). Large-scale automated synthesis of human functional neuroimaging data. Nature Methods, 8(8), 665670. doi: 10.1038/nmeth.1635.CrossRefGoogle ScholarPubMed
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