Anterior cingulate cortex-related connectivity in first-episode schizophrenia: A spectral dynamic causal modeling study with functional magnetic resonance imaging

Frontiers in Human Neuroscience

Volumn 9, Issue NOVEMBER, 2015, Pages

  Cui, Long Biao ^a   Liu, Jian ^b   Wang, Liu Xian ^a   Li, Chen ^a   Xi, Yi Bin ^a   Guo, Fan ^a   Wang, Hua Ning ^a   Zhang, Lin Chuan ^b   Liu, Wen Ming ^a   He, Hong ^a   Tian, Ping ^a   Yin, Hong ^a   Lu, Hongbing ^b  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Anterior cingulate cortex; Effective connectivity; Functional magnetic resonance imaging; Schizophrenia; Spectral dynamic causal modeling

Indexed keywords

ADULT; ANTERIOR CINGULATE; ARTICLE; BRAIN DYSFUNCTION; CAUSAL MODELING; CLINICAL ARTICLE; CONTROLLED STUDY; DORSOLATERAL PREFRONTAL CORTEX; FEMALE; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; LEFT HEMISPHERE; MALE; MEDIAL PREFRONTAL CORTEX; NERVOUS SYSTEM PARAMETERS; PATHOPHYSIOLOGY; POSITIVE AND NEGATIVE SYNDROME SCALE; PREDICTIVE VALIDITY; RIGHT HEMISPHERE; SCHIZOPHRENIA;

EID: 84947588521     PISSN: 16625161     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2015.00589     Document Type: Article

References (64)

1. APA (2013). Diagnostic and Statistical Manual of Mental Disorders, 5th Edn. Washington, DC: American Psychiatric Association.
2. Argyelan, M., Ikuta, T., DeRosse, P., Braga, R. J., Burdick, K. E., John, M., et al. (2014). Resting-state fMRI connectivity impairment in schizophrenia and bipolar disorder. Schizophr. Bull. 40, 100-110. doi: 10.1093/schbul/sbt092
3. Bastos-Leite, A. J., Ridgway, G. R., Silveira, C., Norton, A., Reis, S., and Friston, K. J. (2015). Dysconnectivity within the default mode in first- episode schizophrenia: a stochastic dynamic causal modeling study with functional magnetic resonance imaging. Schizophr. Bull. 41, 144-153. doi:10.1093/schbul/sbu080
4. Benedetti, F., Radaelli, D., Poletti, S., Falini, A., Cavallaro, R., Dallaspezia, S., et al. (2011). Emotional reactivity in chronic schizophrenia: structural and functional brain correlates and the influence of adverse childhood experiences. Psychol. Med. 41, 509-519. doi: 10.1017/S0033291710001108
5. Bois, C., Ronan, L., Levita, L., Whalley, H. C., Giles, S., Mcintosh, A. M., et al. (2015). Cortical surface area differentiates familial high risk individuals who go on to develop schizophrenia. Biol. Psychiatry 78, 413-420. doi:10.1016/j.biopsych.2014.12.030
6. Carter, C. S., and van Veen, V. (2007). Anterior cingulate cortex and conflict detection: an update of theory and data. Cogn. Affect. Behav. Neurosci. 7, 367-379. doi: 10.3758/CABN.7.4.367
7. Chang, X., Xi, Y. B., Cui, L. B., Wang, H. N., Sun, J. B., Zhu, Y. Q., et al. (2015). Distinct inter-hemispheric dysconnectivity in schizophrenia patients with and without auditory verbal hallucinations. Sci. Rep. 5:11218. doi:10.1038/srep11218
8. Chun, S., Westmoreland, J. J., Bayazitov, I. T., Eddins, D., Pani, A. K., Smeyne, R. J., et al. (2014). Specific disruption of thalamic inputs to the auditory cortex in schizophrenia models. Science 344, 1178-1182. doi: 10.1126/science.1253895
9. Coughlin, J. M., Tanaka, T., Marsman, A., Wang, H., Bonekamp, S., Kim, P. K., et al. (2015). Decoupling of N-acetyl-aspartate and Glutamate within the Dorsolateral prefrontal cortex in Schizophrenia. Curr. Mol. Med. 15, 176-183. doi: 10.2174/1566524015666150303104811
10. Das, P., Kemp, A. H., Flynn, G., Harris, A. W., Liddell, B. J., Whitford, T. J., et al. (2007). Functional disconnections in the direct and indirect amygdale pathways for fear processing in schizophrenia. Schizophr. Res. 90, 284-294. doi:10.1016/j.schres.2006.11.023
11. Diwadkar, V. A., Wadehra, S., Pruitt, P., Keshavan, M. S., Rajan, U., Zajac- Benitez, C., et al. (2012). Disordered corticolimbic interactions during affective processing in children and adolescents at risk for schizophrenia revealed by functional magnetic resonance imaging and dynamic causal modeling. Arch. Gen. Psychiatry 69, 231-242. doi: 10.1001/archgenpsychiatry.2011.1349
12. Ellison-Wright, I., and Bullmore, E. (2009). Meta-analysis of diffusion tensor imaging studies in schizophrenia. Schizophr. Res. 108, 3-10. doi:10.1016/j.schres.2008.11.021
13. Elvevåg, B., and Goldberg, T. E. (2000). Cognitive impairment in schizophrenia is the core of the disorder. Crit. Rev. Neurobiol. 14, 1-21. doi:10.1615/critrevneurobiol.v14.i1.10
14. Fan, F. M., Tan, S. P., Yang, F. D., Tan, Y. L., Zhao, Y. L., Chen, N., et al. (2013). Ventral medial prefrontal functional connectivity and emotion regulation in chronic schizophrenia: a pilot study. Neurosci. Bull. 29, 59-74. doi:10.1007/s12264-013-1300-8
15. Fornito, A., Zalesky, A., Pantelis, C., and Bullmore, E. T. (2012). Schizophrenia, neuroimaging and connectomics. Neuroimage 62, 2296-2314. doi: 10.1016/j.neuroimage.2011.12.090
16. Friedman, J. I., Tang, C., Carpenter, D., Buchsbaum, M., Schmeidler, J., Flanagan, L., et al. (2008). Diffusion tensor imaging findings in first-episode and chronic schizophrenia patients. Am. J. Psychiatry 165, 1024-1032. doi:10.1176/appi.ajp.2008.07101640
17. Friston, K., and Penny, W. (2011). Post hoc Bayesian model selection. Neuroimage 56, 2089-2099. doi: 10.1016/j.neuroimage.2011.03.062
18. Friston, K. J. (1998). The disconnection hypothesis. Schizophr. Res. 30, 115-125. doi: 10.1016/S0920-9964(97)00140-0
19. Friston, K. J., and Frith, C. D. (1995). Schizophrenia: a disconnection syndrome? Clin. Neurosci. 3, 89-97.
20. Friston, K. J., Kahan, J., Biswal, B., and Razi, A. (2014). A DCM for resting state fMRI. Neuroimage 94, 396-407. doi: 10.1016/j.neuroimage.2013.12.009
21. Friston, K. J., Li, B., Daunizeau, J., and Stephan, K. E. (2011). Network discovery with DCM. Neuroimage 56, 1202-1221. doi: 10.1016/j.neuroimage.2010.12.039
22. Friston, K. J., Stephan, K., Li, B. J., and Daunizeau, J. (2010). Generalised filtering. Math. Probl. Eng. 2010:621670. doi: 10.1155/2010/621670
23. Genzel, L., Dresler, M., Cornu, M., Jäger, E., Konrad, B., Adamczyk, M., et al. (2015). Medial prefrontal-hippocampal connectivity and motor memory consolidation in depression and schizophrenia. Biol. Psychiatry 77, 177-186. doi: 10.1016/j.biopsych.2014.06.004
24. Guo, W., Liu, F., Liu, J., Yu, L., Zhang, J., Zhang, Z., et al. (2015). Abnormal causal connectivity by structural deficits in first-episode, drug-naive schizophrenia at rest. Schizophr. Bull. 41, 57-65. doi: 10.1093/schbul/sbu126
25. Hoptman, M. J., Antonius, D., Mauro, C. J., Parker, E. M., and Javitt, D. C. (2014). Cortical thinning, functional connectivity, and mood-related impulsivity in schizophrenia: relationship to aggressive attitudes and behavior. Am. J. Psychiatry 171, 939-948. doi: 10.1176/appi.ajp.2014.13111553
26. Ivleva, E. I., Bidesi, A. S., Keshavan, M. S., Pearlson, G. D., Meda, S. A., Dodig, D., et al. (2013). Gray matter volume as an intermediate phenotype for psychosis: bipolar-schizophrenia network on intermediate phenotypes (B-SNIP). Am. J. Psychiatry 170, 1285-1296. doi: 10.1176/appi.ajp.2013.13010126
27. Kay, S. R., Fiszbein, A., and Opler, L. A. (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 13, 261-276. doi:10.1093/schbul/13.2.261
28. Khadka, S., Meda, S. A., Stevens, M. C., Glahn, D. C., Calhoun, V. D., Sweeney, J. A., et al. (2013). Is aberrant functional connectivity a psychosis endophenotype? A resting state functional magnetic resonance imaging study. Biol. Psychiatry 74, 458-466. doi: 10.1016/j.biopsych.2013.04.024
29. Kubota, M., Miyata, J., Sasamoto, A., Sugihara, G., Yoshida, H., Kawada, R., et al. (2013). Thalamocortical disconnection in the orbitofrontal region associated with cortical thinning in schizophrenia. JAMA Psychiatry 70, 12-21. doi:10.1001/archgenpsychiatry.2012.1023
30. Leitman, D. I., Loughead, J., Wolf, D. H., Ruparel, K., Kohler, C. G., Elliott, M. A., et al. (2008). Abnormal superior temporal connectivity during fear perception in schizophrenia. Schizophr. Bull. 34, 673-678. doi: 10.1093/schbul/sbn052
31. Li, B., Wang, X., Yao, S., Hu, D., and Friston, K. (2012). Task-dependent modulation of effective connectivity within the default mode network. Front. Psychol. 3:206. doi: 10.3389/fpsyg.2012.00206
32. Liu, B., Zhang, X., Hou, B., Li, J., Qiu, C., Qin, W., et al. (2014a). The impact of MIR137 on dorsolateral prefrontal-hippocampal functional connectivity in healthy subjects. Neuropsychopharmacology 39, 2153-2160. doi:10.1038/npp.2014.63
33. Liu, H., Tang, Y., Womer, F., Fan, G., Lu, T., Driesen, N., et al. (2014b). Differentiating patterns of amygdala-frontal functional connectivity in schizophrenia and bipolar disorder. Schizophr. Bull. 40, 469-477. doi:10.1093/schbul/sbt044
34. Loewy, R. L., Bearden, C. E., Johnson, J. K., Raine, A., and Cannon, T. D. (2005). The prodromal questionnaire (PQ): preliminary validation of a self-report screening measure for prodromal and psychotic syndromes. Schizophr. Res. 79, 117-125. doi: 10.1016/j.schres.2005.03.007
35. Lui, S., Yao, L., Xiao, Y., Keedy, S. K., Reilly, J. L., Keefe, R. S., et al. (2015). Resting-state brain function in schizophrenia and psychotic bipolar probands and their first-degree relatives. Psychol. Med. 45, 97-108. doi:10.1017/S003329171400110X
36. Maldjian, J. A., Laurienti, P. J., and Burdette, J. H. (2004). Precentral gyrus discrepancy in electronic versions of the Talairach atlas. Neuroimage 21, 450-455. doi: 10.1016/j.neuroimage.2003.09.032
37. Maldjian, J. A., Laurienti, P. J., Kraft, R. A., and Burdette, J. H. (2003). An automated method for neuroanatomic and cytoarchitectonic atlasbased interrogation of fMRI data sets. Neuroimage 19, 1233-1239. doi:10.1016/S1053-8119(03)00169-1
38. Mamah, D., Barch, D. M., and Repovš, G. (2013). Resting state functional connectivity of five neural networks in bipolar disorder and schizophrenia. J. Affect. Disord. 150, 601-609. doi: 10.1016/j.jad.2013.01.051
39. Meda, S. A., Ruaño, G., Windemuth, A., O’Neil, K., Berwise, C., Dunn, S. M., et al. (2014). Multivariate analysis reveals genetic associations of the resting default mode network in psychotic bipolar disorder and schizophrenia. Proc. Natl. Acad. Sci. U.S.A 111, E2066-E2075. doi: 10.1073/pnas.1313093111
40. Minzenberg, M. J., Laird, A. R., Thelen, S., Carter, C. S., and Glahn, D. C. (2009). Meta-analysis of 41 functional neuroimaging studies of executive function in schizophrenia. Arch. Gen. Psychiatry 66, 811-822. doi:10.1001/archgenpsychiatry.2009.91
41. Modinos, G., Ormel, J., and Aleman, A. (2010). Altered activation and functional connectivity of neural systems supporting cognitive controlof emotion in psychosis proneness. Schizophr. Res. 118, 88-97. doi:10.1016/j.schres.2010.01.030
42. Moran, R. J., Jones, M. W., Blockeel, A. J., Adams, R. A., Stephan, K. E., and Friston, K. J. (2015). Losing control under ketamine: suppressed cortico-hippocampal drive following acute ketamine in rats. Neuropsychopharmacology 40, 268-277. doi: 10.1038/npp.2014.184
43. Moriya, J., Kakeda, S., Abe, O., Goto, N., Yoshimura, R., Hori, H., et al. (2010). Gray and white matter volumetric and diffusion tensor imaging (DTI) analyses in the early stage of first-episode schizophrenia. Schizophr. Res. 116, 196-203. doi: 10.1016/j.schres.2009.10.002
44. Mothersill, O., Morris, D. W., Kelly, S., Rose, E. J., Bokde, A., Reilly, R., et al. (2014). Altered medial prefrontal activity during dynamic face processing in schizophrenia spectrum patients. Schizophr. Res. 157, 225-230. doi:10.1016/j.schres.2014.05.023
45. Mukherjee, P., Whalley, H. C., McKirdy, J. W., Sprengelmeyer, R., Young, A. W., McIntosh, A. M., et al. (2014). Altered amygdala connectivity within the social brain in schizophrenia. Schizophr. Bull. 40, 152-160. doi: 10.1093/schbul/sbt086
46. Ohtani, T., Bouix, S., Hosokawa, T., Saito, Y., Eckbo, R., Ballinger, T., et al. (2014). Abnormalities in white matter connections between orbitofrontal cortex and anterior cingulate cortex and their associations with negative symptoms in schizophrenia: a DTI study. Schizophr. Res. 157, 190-197. doi:10.1016/j.schres.2014.05.016
47. Pettersson-Yeo, W., Allen, P., Benetti, S., McGuire, P., and Mechelli, A. (2011). Dysconnectivity in schizophrenia: where are we now? Neurosci. Biobehav. Rev. 35, 1110-1124. doi: 10.1016/j.neubiorev.2010.11.004
48. Pomarol-Clotet, E., Canales-Rodríguez, E. J., Salvador, R., Sarró, S., Gomar, J. J., Vila, F., et al. (2010). Medial prefrontal cortex pathology in schizophrenia as revealed by convergent findings from multimodal imaging. Mol. Psychiatry 15, 823-830. doi: 10.1038/mp.2009.146
49. Razi, A., Kahan, J., Rees, G., and Friston, K. J. (2015). Construct validation of a DCM for resting state fMRI. Neuroimage 106, 1-14. doi:10.1016/j.neuroimage.2014.11.027
50. Schlösser, R. G. M., Nenadic, I., Wagner, G., Güllmar, D., von Consbruch, K., Köhler, S., et al. (2007). White matter abnormalities and brain activation inschizophrenia: a combined DTI and fMRI study. Schizophr. Res. 89, 1-11. doi:10.1016/j.schres.2006.09.007
51. Skudlarski, P., Schretlen, D. J., Thaker, G. K., Stevens, M. C., Keshavan, M. S., Sweeney, J. A., et al. (2013). Diffusion tensor imaging white matter endophenotypes in patients with schizophrenia or psychotic bipolar disorder and their relatives. Am. J. Psychiatry 170, 886-898. doi:10.1176/appi.ajp.2013.12111448
52. Stan, A. D., Ghose, S., Zhao, C., Hulsey, K., Mihalakos, P., Yanagi, M., et al. (2015). Magnetic resonance spectroscopy and tissue protein concentrations together suggest lower glutamate signaling in dentate gyrus in schizophrenia. Mol. Psychiatry 20, 433-439. doi: 10.1038/mp.2014.54
53. Stephan, K. E., Friston, K. J., and Frith, C. D. (2009). Dysconnection in schizophrenia: from abnormal synaptic plasticity to failures of self-monitoring. Schizophr. Bull. 35, 509-527. doi: 10.1093/schbul/sbn176
54. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15, 273-289. doi: 10.1006/nimg.2001.0978
55. Vai, B., Sferrazza Papa, G., Poletti, S., Radaelli, D., Donnici, E., Bollettini, I., et al. (2015). Abnormal cortico-limbic connectivity during emotional processing correlates with symptom severity in schizophrenia. Eur. Psychiatry 30, 590-597. doi: 10.1016/j.eurpsy.2015.01.002
56. van den Heuvel, M. P., Sporns, O., Collin, G., Scheewe, T., Mandl, R. C., Cahn, W., et al. (2013). Abnormal rich club organization and functional brain dynamics in schizophrenia. JAMA Psychiatry 70, 783-792. doi:10.1001/jamapsychiatry.2013.1328
57. van Elst, L. T., Valerius, G., Büchert, M., Thiel, T., Rüsch, N., Bubl, E., et al. (2005). Increased prefrontal and hippocampal glutamate concentration in schizophrenia: evidence from a magnetic resonance spectroscopy study. Biol. Psychiatry 58, 724-730. doi: 10.1016/j.biopsych.2005.04.041
58. Voineskos, A. N., Foussias, G., Lerch, J., Felsky, D., Remington, G., Rajji, T. K., et al. (2013). Neuroimaging evidence for the deficit subtype of schizophrenia. JAMA Psychiatry 70, 472-480. doi: 10.1001/jamapsychiatry.2013.786
59. Wagner, G., De la Cruz, F., Schachtzabel, C., Güllmar, D., Schultz, C. C., Schlösser, R. G., et al. (2015). Structural and functional dysconnectivity of the fronto-thalamic system in schizophrenia: a DCM-DTI study. Cortex 66, 35-45. doi:10.1016/j.cortex.2015.02.004
60. White, T., Nelson, M., and Lim, K. O. (2008). Diffusion tensor imaging in psychiatric disorders. Top. Magn. Reson. Imaging 19, 97-109. doi:10.1097/RMR.0b013e3181809f1e
61. Whiteford, H. A., Degenhardt, L., Rehm, J., Baxter, A. J., Ferrari, A. J., Erskine, H. E., et al. (2013). Global burden of disease attributable to mental and substance use disorders: findings from the Global Burden of Disease Study 2010. Lancet 382, 1575-1586. doi: 10.1016/S0140-6736(13)61611-6
62. Whitford, T. J., Kubicki, M., Schneiderman, J. S., O’Donnell, L. J., King, R., Alvarado, J. L., et al. (2010). Corpus callosum abnormalities and their association with psychotic symptoms in patients with schizophrenia. Biol. Psychiatry 68, 70-77. doi: 10.1016/j.biopsych.2010.03.025
63. Yamasue, H., Iwanami, A., Hirayasu, Y., Yamada, H., Abe, O., Kuroki, N., et al. (2004). Localized volume reduction in prefrontal, temporolimbic, and paralimbic regions in schizophrenia: an MRI parcellation study. Psychiatry Res. 131, 195-207. doi: 10.1016/j.pscychresns.2004.05.004
64. Yu, Y., Shen, H., Zeng, L. L., Ma, Q., and Hu, D. (2013). Convergent and divergent functional connectivity patterns in schizophrenia and depression. PLoS ONE 8:e68250. doi: 10.1371/journal.pone.0068250