Attenuated Resting-State Functional Anticorrelation between Attention and Executive Control Networks in Schizotypal Personality Disorder
Abstract
1. Introduction
2. Methods and Materials
2.1. Participants
2.2. Measures
2.2.1. Clinical Symptoms
2.2.2. Social Functions
2.3. Image Acquisition and Preprocessing
2.4. Intra- and Inter-Network Functional Connectivity
2.5. Statistical Analyses
3. Results
3.1. Participant Characteristics
3.2. Overall Characteristics of Intra- and Inter-Network Connectivity
3.2.1. Intra-Network Connectivity
3.2.2. Inter-Network Connectivity
3.3. Correlation Analysis
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Li, S.; Hu, N.; Zhang, W.; Tao, B.; Dai, J.; Gong, Y.; Tan, Y.; Cai, D.; Lui, S. Dysconnectivity of multiple brain networks in schizophrenia: A meta-analysis of resting-state functional connectivity. Front. Psychiatry 2019, 10. [Google Scholar] [CrossRef]
- Northoff, G.; Duncan, N.W. How do abnormalities in the brain’s spontaneous activity translate into symptoms in schizophrenia? From an overview of resting state activity findings to a proposed spatiotemporal psychopathology. Prog. Neurobiol. 2016, 145–146, 26–45. [Google Scholar] [CrossRef] [PubMed]
- Ryan, A.; Macdonald, A.; Walker, E. The treatment of adolescents with schizotypal personality disorder and related conditions: A practice-oriented review of the literature. Clin. Psychol. 2013, 20, 408–424. [Google Scholar] [CrossRef]
- Chemerinski, E.; Triebwasser, J.; Roussos, P.; Siever, L.J. Schizotypal personality disorder. J. Personal. Disord. 2013, 27, 652–679. [Google Scholar] [CrossRef] [PubMed]
- APA. Diagnostic and Statistical Manual of Mental Disorders (DSM-5®); American Psychiatric Pub: Arlington, VA, USA, 2013. [Google Scholar]
- Di Carlo, P.; Pergola, G.; Antonucci, L.A.; Bonvino, A.; Mancini, M.; Quarto, T.; Rampino, A.; Popolizio, T.; Bertolino, A.; Blasi, G. Multivariate patterns of gray matter volume in thalamic nuclei are associated with positive schizotypy in healthy individuals. Psychol. Med. 2020, 50, 1501–1509. [Google Scholar] [CrossRef] [PubMed]
- Ettinger, U.; Mohr, C.; Gooding, D.C.; Cohen, A.S.; Rapp, A.; Haenschel, C.; Park, S. Cognition and brain function in schizotypy: A selective review. Schizophr. Bull. 2015, 41, S417–S426. [Google Scholar] [CrossRef] [PubMed]
- Asami, T.; Whitford, T.J.; Bouix, S.; Dickey, C.C.; Niznikiewicz, M.; Shenton, M.E.; Voglmaier, M.M.; McCarley, R.W. Globally and locally reduced MRI gray matter volumes in neuroleptic-naive men with schizotypal personality disorder: Association with negative symptoms. JAMA Psychiatry 2013, 70, 361–372. [Google Scholar] [CrossRef]
- Woodward, N.D.; Cowan, R.L.; Park, S.; Ansari, M.S.; Baldwin, R.M.; Li, R.; Doop, M.; Kessler, R.M.; Zald, D.H. Correlation of individual differences in schizotypal personality traits with amphetamine-induced dopamine release in striatal and extrastriatal brain regions. Am. J. Psychiatry 2011, 168, 418–426. [Google Scholar] [CrossRef]
- Zoghbi, A.W.; Bernanke, J.A.; Gleichman, J.; Masucci, M.D.; Corcoran, C.M.; Califano, A.; Segovia, J.; Colibazzi, T.; First, M.B.; Brucato, G.; et al. Schizotypal personality disorder in individuals with the Attenuated Psychosis Syndrome: Frequent co-occurrence without an increased risk for conversion to threshold psychosis. J. Psychiatr. Res. 2019, 114, 88–92. [Google Scholar] [CrossRef]
- Finn, E.S.; Shen, X.; Scheinost, D.; Rosenberg, M.D.; Huang, J.; Chun, M.M.; Papademetris, X.; Constable, R.T. Functional connectome fingerprinting: Identifying individuals using patterns of brain connectivity. Nat. Neurosci. 2015, 18, 1664–1671. [Google Scholar] [CrossRef]
- Viviano, J.D.; Buchanan, R.W.; Calarco, N.; Gold, J.M.; Foussias, G.; Bhagwat, N.; Stefanik, L.; Hawco, C.; DeRosse, P.; Argyelan, M.; et al. Resting-state connectivity biomarkers of cognitive performance and social function in individuals with schizophrenia spectrum disorder and healthy control subjects. Biol. Psychiatry 2018, 84, 665–674. [Google Scholar] [CrossRef] [PubMed]
- Li, T.; Wang, Q.; Zhang, J.; Rolls, E.T.; Yang, W.; Palaniyappan, L.; Zhang, L.; Cheng, W.; Yao, Y.; Liu, Z.; et al. Brain-wide analysis of functional connectivity in first-episode and chronic stages of schizophrenia. Schizophr. Bull. 2017, 43, 436–448. [Google Scholar] [CrossRef] [PubMed]
- Smallwood, J.; Brown, K.; Baird, B.; Schooler, J.W. Cooperation between the default mode network and the frontal–parietal network in the production of an internal train of thought. Brain Res. 2012, 1428, 60–70. [Google Scholar] [CrossRef] [PubMed]
- Pu, W.; Luo, Q.; Palaniyappan, L.; Xue, Z.; Yao, S.; Feng, J.; Liu, Z. Failed cooperative, but not competitive, interaction between large-scale brain networks impairs working memory in schizophrenia. Psychol. Med. 2016, 46, 1211–1224. [Google Scholar] [CrossRef] [PubMed]
- Menon, V. Large-scale brain networks and psychopathology: A unifying triple network model. Trends Cogn. Sci. 2011, 15, 483–506. [Google Scholar] [CrossRef]
- Mishara, A.; Bonoldi, I.; Allen, P.; Rutigliano, G.; Perez, J.; Fusar-Poli, P.; McGuire, P. Neurobiological models of self-disorders in early schizophrenia. Schizophr. Bull. 2016, 42, 874–880. [Google Scholar] [CrossRef]
- Woodward, N.D.; Rogers, B.; Heckers, S. Functional resting-state networks are differentially affected in schizophrenia. Schizophr. Res. 2011, 130, 86–93. [Google Scholar] [CrossRef]
- Carhart-Harris, R.L.; Friston, K.J. The default-mode, ego-functions and free-energy: A neurobiological account of Freudian ideas. Brain 2010, 133, 1265–1283. [Google Scholar] [CrossRef]
- Spadone, S.; Della Penna, S.; Sestieri, C.; Betti, V.; Tosoni, A.; Perrucci, M.G.; Romani, G.L.; Corbetta, M. Dynamic reorganization of human resting-state networks during visuospatial attention. Proc. Natl. Acad. Sci. USA 2015, 112, 8112–8117. [Google Scholar] [CrossRef]
- Dixon, M.L.; Andrews-Hanna, J.R.; Spreng, R.N.; Irving, Z.C.; Mills, C.; Girn, M.; Christoff, K. Interactions between the default network and dorsal attention network vary across default subsystems, time, and cognitive states. NeuroImage 2017, 147, 632–649. [Google Scholar] [CrossRef]
- Gong, J.; Wang, J.; Luo, X.; Chen, G.; Huang, H.; Huang, R.; Huang, L.; Wang, Y. Abnormalities of intrinsic regional brain activity in first-episode and chronic schizophrenia: A meta-analysis of resting-state functional MRI. J. Psychiatry Neurosci. 2020, 45, 55–68. [Google Scholar] [CrossRef] [PubMed]
- Su, T.-W.; Hsu, T.-W.; Lin, Y.-C.; Lin, C.-P. Schizophrenia symptoms and brain network efficiency: A resting-state fMRI study. Psychiatry Res. Neuroimaging 2015, 234, 208–218. [Google Scholar] [CrossRef]
- Lagioia, A.; van de Ville, D.; Debbane, M.; Lazeyras, F.; Eliez, S. Adolescent resting state networks and their associations with schizotypal trait expression. Front. Syst. Neurosci. 2010, 4. [Google Scholar] [CrossRef]
- Waltmann, M.; O’Daly, O.; Egerton, A.; McMullen, K.; Kumari, V.; Barker, G.J.; Williams, S.C.R.; Modinos, G. Multi-echo fMRI, resting-state connectivity, and high psychometric schizotypy. Neuroimage Clin. 2019, 21, 101603. [Google Scholar] [CrossRef]
- Zhang, Q.; Shen, J.; Wu, J.; Yu, X.; Lou, W.; Fan, H.; Shi, L.; Wang, D. Altered default mode network functional connectivity in schizotypal personality disorder. Schizophr. Res. 2014, 160, 51–56. [Google Scholar] [CrossRef] [PubMed]
- Zhu, Y.; Tang, Y.; Zhang, T.; Li, H.; Tang, Y.; Li, C.; Luo, X.; He, Y.; Lu, Z.; Wang, J. Reduced functional connectivity between bilateral precuneus and contralateral parahippocampus in schizotypal personality disorder. BMC Psychiatry 2017, 17, 48. [Google Scholar] [CrossRef] [PubMed]
- Schultze-Lutter, F.; Nenadic, I.; Grant, P. Psychosis and schizophrenia-spectrum personality disorders require early detection on different symptom dimensions. Front. Psychiatry 2019, 10, 476. [Google Scholar] [CrossRef]
- Hur, J.-W.; Blake, R.; Cho, K.I.K.; Kim, J.; Kim, S.-Y.; Choi, S.-H.; Kang, D.-H.; Kwon, J.S. Biological motion perception, brain responses, and schizotypal personality disorder. JAMA Psychiatry 2016, 73, 260–267. [Google Scholar] [CrossRef]
- Choe, A.; Hwang, S.; Kim, J.; Park, K.; Chey, J.; Hong, S. Validity of the K-WAIS-IV short forms. Korean J. Clin. Psychol. 2014, 33, 413–428. [Google Scholar]
- Raine, A. The SPQ: A scale for the assessment of schizotypal personality based on DSM-III-R criteria. Schizophr. Bull. 1991, 17, 555–564. [Google Scholar] [CrossRef]
- Moon, H.O.; Yang, I.H.; Lee, H.P.; Kim, M.E.; Ham, W. The preliminary study on the validation of schizotypal personality questionnaire-Korean version. J. Korean Neuropsychiatr. Assoc. 1997, 36, 329–343. [Google Scholar]
- Reynolds, C.A.; Raine, A.; Mellingen, K.; Venables, P.H.; Mednick, S.A. Three-factor model of schizotypal personality: Invariance across culture, gender, religious affiliation, family adversity, and psychopathology. Schizophr. Bull. 2000, 26, 603–618. [Google Scholar] [CrossRef] [PubMed]
- Jones, S.H.; Thornicroft, G.; Coffey, M.; Dunn, G. A brief mental health outcome scale: Reliability and validity of the Global Assessment of Functioning (GAF). Br. J. Psychiatry 1995, 166, 654–659. [Google Scholar] [CrossRef] [PubMed]
- Lee, H.-R.; Nam, G.; Hur, J.-W. Development and validation of the Korean version of the reading the mind in the eyes test. PLoS ONE 2020, 15, e0238309. [Google Scholar] [CrossRef]
- Baron-Cohen, S.; Wheelwright, S.; Hill, J.; Raste, Y.; Plumb, I. The “Reading the Mind in the Eyes” Test revised version: A study with normal adults, and adults with Asperger syndrome or high-functioning autism. J. Child Psychol. Psychiatry Allied Discip. 2001, 42, 241–251. [Google Scholar] [CrossRef]
- Birchwood, M.; Smith, J.; Cochrane, R.; Wetton, S.; Copestake, S. The social functioning scale. The development and validation of a new scale of social adjustment for use in family intervention programmes with schizophrenic patients. Br. J. Psychiatry 1990, 157, 853–859. [Google Scholar] [CrossRef]
- Ashburner, J.; Friston, K.J. Nonlinear spatial normalization using basis functions. Hum. Brain Mapp. 1999, 7, 254–266. [Google Scholar] [CrossRef]
- Hallquist, M.N.; Hwang, K.; Luna, B. The nuisance of nuisance regression: Spectral misspecification in a common approach to resting-state fMRI preprocessing reintroduces noise and obscures functional connectivity. NeuroImage 2013, 82, 208–225. [Google Scholar] [CrossRef]
- Whitfield-Gabrieli, S.; Nieto-Castanon, A. Conn: A functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect. 2012, 2, 125–141. [Google Scholar] [CrossRef]
- Shen, W.; Tu, Y.; Gollub, R.L.; Ortiz, A.; Napadow, V.; Yu, S.; Wilson, G.; Park, J.; Lang, C.; Jung, M.; et al. Visual network alterations in brain functional connectivity in chronic low back pain: A resting state functional connectivity and machine learning study. Neuroimage Clin. 2019, 22, 101775. [Google Scholar] [CrossRef]
- Wolak, T.; Cieśla, K.; Pluta, A.; Włodarczyk, E.; Biswal, B.; Skarżyński, H. Altered functional connectivity in patients with sloping sensorineural hearing loss. Front. Hum. Neurosci. 2019, 13. [Google Scholar] [CrossRef] [PubMed]
- Cole, M.W.; Reynolds, J.R.; Power, J.D.; Repovs, G.; Anticevic, A.; Braver, T.S. Multi-task connectivity reveals flexible hubs for adaptive task control. Nat. Neurosci. 2013, 16, 1348–1355. [Google Scholar] [CrossRef] [PubMed]
- Vossel, S.; Geng, J.J.; Fink, G.R. Dorsal and ventral attention systems: Distinct neural circuits but collaborative roles. Neuroscientist 2014, 20, 150–159. [Google Scholar] [CrossRef] [PubMed]
- Posner, M.I.; Fan, J. Attention as an organ system. In Topics in Integrative Neuroscience; Cambridge University Press: Cambridge, UK, 2008; pp. 31–61. [Google Scholar]
- Ozaki, T.J. Frontal-to-parietal top-down causal streams along the dorsal attention network exclusively mediate voluntary orienting of attention. PLoS ONE 2011, 6, e20079. [Google Scholar] [CrossRef] [PubMed]
- Allan, P.G.; Briggs, R.G.; Conner, A.K.; O’Neal, C.M.; Bonney, P.A.; Maxwell, B.D.; Baker, C.M.; Burks, J.D.; Sali, G.; Glenn, C.A.; et al. Parcellation-based tractographic modeling of the dorsal attention network. Brain Behav. 2019, 9, e01365. [Google Scholar] [CrossRef] [PubMed]
- Dosenbach, N.U.F.; Visscher, K.M.; Palmer, E.D.; Miezin, F.M.; Wenger, K.K.; Kang, H.C.; Burgund, E.D.; Grimes, A.L.; Schlaggar, B.L.; Petersen, S.E. A core system for the implementation of task sets. Neuron 2006, 50, 799–812. [Google Scholar] [CrossRef] [PubMed]
- Qureshi, A.; Nielsen, J.; Sepulcre, J. Topographic shifts in functional connectivity and reduced lateralization in 16p11.2 deletion carriers: A genetics-first approach to understanding autism. Res. Sq. 2020. [Google Scholar] [CrossRef]
- Dixon, M.L.; de la Vega, A.; Mills, C.; Andrews-Hanna, J.; Spreng, R.N.; Cole, M.W.; Christoff, K. Heterogeneity within the frontoparietal control network and its relationship to the default and dorsal attention networks. Proc. Natl. Acad. Sci. USA 2018, 115, E1598–E1607. [Google Scholar] [CrossRef]
- Chai, X.J.; Ofen, N.; Gabrieli, J.D.E.; Whitfield-Gabrieli, S. Selective development of anticorrelated networks in the intrinsic functional organization of the human brain. J. Cogn. Neurosci. 2014, 26, 501–513. [Google Scholar] [CrossRef]
- Karcher, N.R.; Michelini, G.; Kotov, R.; Barch, D.M. Associations between resting state functional connectivity and a hierarchical dimensional structure of psychopathology in middle childhood. bioRxiv 2020. [Google Scholar] [CrossRef]
- Manoliu, A.; Riedl, V.; Zherdin, A.; Mühlau, M.; Schwerthöffer, D.; Scherr, M.; Peters, H.; Zimmer, C.; Förstl, H.; Bäuml, J.; et al. Aberrant dependence of default mode/central executive network interactions on anterior insular salience network activity in schizophrenia. Schizophr. Bull. 2013, 40, 428–437. [Google Scholar] [CrossRef] [PubMed]
- Hare, S.M.; Ford, J.M.; Mathalon, D.H.; Damaraju, E.; Bustillo, J.; Belger, A.; Lee, H.J.; Mueller, B.A.; Lim, K.O.; Brown, G.G.; et al. Salience-default mode functional network connectivity linked to positive and negative symptoms of schizophrenia. Schizophr. Bull. 2019, 45, 892–901. [Google Scholar] [CrossRef] [PubMed]
- Mallikarjun, P.K.; Lalousis, P.A.; Dunne, T.F.; Heinze, K.; Reniers, R.L.E.P.; Broome, M.R.; Farmah, B.; Oyebode, F.; Wood, S.J.; Upthegrove, R. Aberrant salience network functional connectivity in auditory verbal hallucinations: A first episode psychosis sample. Transl. Psychiatry 2018, 8, 69. [Google Scholar] [CrossRef] [PubMed]
- Laws, K.R.; Patel, D.D.; Tyson, P.J. Awareness of everyday executive difficulties precede overt executive dysfunction in schizotypal subjects. Psychiatry Res. 2008, 160, 8–14. [Google Scholar] [CrossRef] [PubMed]
- Compton, M.T.; Chien, V.H.; Bollini, A.M. Psychometric properties of the Brief Version of the Schizotypal Personality Questionnaire in relatives of patients with schizophrenia-spectrum disorders and non-psychiatric controls. Schizophr. Res. 2007, 91, 122–131. [Google Scholar] [CrossRef]
- Wilson, S.; Stroud, C.B.; Durbin, C.E. Interpersonal dysfunction in personality disorders: A meta-analytic review. Psychol. Bull. 2017, 143, 677–734. [Google Scholar] [CrossRef]
- Buschman, T.J.; Miller, E.K. Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 2007, 315, 1860–1862. [Google Scholar] [CrossRef]
- Hur, J.-W.; Byun, M.S.; Shin, N.Y.; Shin, Y.S.; Kim, S.N.; Jang, J.H.; Kwon, J.S. General intellectual functioning as a buffer against theory-of-mind deficits in individuals at ultra-high risk for psychosis. Schizophr. Res. 2013, 149, 83–87. [Google Scholar] [CrossRef]
Variables | SPD | Controls | Statistics | |
---|---|---|---|---|
(N = 22) | (N = 30) | t (χ2) | p-Value | |
Age, mean (SD), years | 22.68 (3.71) | 22.53 (2.60) | 0.16 | 0.87 |
Sex, male/female | 15/7 | 23/7 | (0.46) | 0.50 |
Handedness, left/right/ambidextrous | 18/4/0 | 28/1/1 | (3.83) | 0.15 |
Estimated IQ, mean (SD) | 119.32 (7.40) | 120.10 (7.14) | −0.38 | 0.70 |
Education, mean (SD), years | 14.86 (1.55) | 14.90 (1.06) | −0.10 | 0.92 |
SES self, mean (SD) | 3.05 (1.17) | 2.67 (0.80) | (3.61) | 0.46 |
SES parental, mean (SD) | 2.86 (0.99) | 2.77 (0.77) | (3.01) | 0.56 |
SPQ total, mean (SD) | 35.05 (13.61) | 5.37 (5.44) | 9.68 | <0.001 |
Subscale 1: Ideas of reference | 5.24 (2.51) | 1.10 (1.06) | 7.13 | <0.001 |
Subscale 2: Social anxiety | 3.95 (2.29) | 1.50 (1.78) | 4.31 | <0.001 |
Subscale 3: Odd beliefs/magical thinking | 3.86 (1.68) | 0.10 (0.31) | 10.12 | <0.001 |
Subscale 4: Unusual perceptual experiences | 4.00 (2.24) | 0.10 (0.31) | 7.94 | <0.001 |
Subscale 5: Eccentric/odd behavior and appearance | 4.05 (2.06) | 0.20 (0.48) | 8.40 | <0.001 |
Subscale 6: No close friends | 3.48 (2.48) | 0.50 (0.90) | 5.26 | <0.001 |
Subscale 7: Odd speech | 4.86 (2.37) | 0.63 (1.03) | 7.67 | <0.001 |
Subscale 8: Constricted affect | 3.24 (1.48) | 0.77 (1.25) | 6.44 | <0.001 |
Subscale 9: Suspiciousness/paranoid ideation | 3.62 (1.86) | 0.53 (1.07) | 6.86 | <0.001 |
SPQ factor 1: Cognitive–perceptual deficits | 16.71 (6.37) | 1.83 (2.05) | 10.33 | <0.001 |
SPQ factor 2: Interpersonal deficits | 14.29 (6.45) | 3.30 (3.69) | 7.04 | <0.001 |
SPQ factor 3: Disorganization | 8.90 (3.90) | 0.83 (1.34) | 9.12 | <0.001 |
GAF, mean (SD) | 66.00 (13.58) | 90.70 (3.20) | −8.36 | <0.001 |
RMET (correct), mean (SD) | 25.55 (2.81) | 26.50 (2.32) | −1.34 | 0.19 |
SFS total, mean (SD) | 102.67 (10.78) | 116.39 (4.84) | −6.19 | <0.001 |
Withdrawal | 98.98 (11.32) | 112.62 (9.34) | −4.75 | <0.001 |
Interpersonal | 108.14 (16.57) | 120.40 (12.27) | −3.07 | 0.003 |
Prosocial | 103.57 (15.48) | 120.58 (8.82) | −4.64 | <0.001 |
Recreation | 98.55 (12.97) | 110.43 (14.33) | −3.08 | 0.003 |
Independence–competence | 93.66 (24.21) | 113.72 (9.36) | −4.15 | <0.001 |
Independence–performance | 100.30 (12.82) | 115.20 (8.33) | −5.08 | <0.001 |
Employment/occupation | 115.52 (11.92) | 121.78 (2.21) | −2.43 | 0.024 |
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Hur, J.-W.; Kim, T.; Cho, K.I.K.; Kwon, J.S. Attenuated Resting-State Functional Anticorrelation between Attention and Executive Control Networks in Schizotypal Personality Disorder. J. Clin. Med. 2021, 10, 312. https://doi.org/10.3390/jcm10020312
Hur J-W, Kim T, Cho KIK, Kwon JS. Attenuated Resting-State Functional Anticorrelation between Attention and Executive Control Networks in Schizotypal Personality Disorder. Journal of Clinical Medicine. 2021; 10(2):312. https://doi.org/10.3390/jcm10020312
Chicago/Turabian StyleHur, Ji-Won, Taekwan Kim, Kang Ik K. Cho, and Jun Soo Kwon. 2021. "Attenuated Resting-State Functional Anticorrelation between Attention and Executive Control Networks in Schizotypal Personality Disorder" Journal of Clinical Medicine 10, no. 2: 312. https://doi.org/10.3390/jcm10020312
APA StyleHur, J.-W., Kim, T., Cho, K. I. K., & Kwon, J. S. (2021). Attenuated Resting-State Functional Anticorrelation between Attention and Executive Control Networks in Schizotypal Personality Disorder. Journal of Clinical Medicine, 10(2), 312. https://doi.org/10.3390/jcm10020312