Hostname: page-component-848d4c4894-x5gtn Total loading time: 0 Render date: 2024-06-03T00:00:28.911Z Has data issue: false hasContentIssue false

Brain functional correlates of formal thought disorder in schizophrenia: examining the frontal/dysexecutive hypothesis

Published online by Cambridge University Press:  27 April 2020

P. Fuentes-Claramonte
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM, Spain
L. López-Araquistain
Affiliation:
Benito Menni CASM, Sant Boi, and University of Barcelona, Spain
S. Sarró
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM, Spain
B. Sans-Sansa
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain
J. Ortiz-Gil
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM, Spain Hospital de Granollers, Spain
T. Maristany
Affiliation:
Fundació Sant Joan de Déu, Barcelona, Spain
R. Salvador
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM, Spain
P.J. McKenna*
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM, Spain
E. Pomarol-Clotet
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM, Spain
*
Author for correspondence: P.J. McKenna, E-mail: mckennapeter1@gmail.com

Abstract

Background

One hypothesis proposed to underlie formal thought disorder (FTD), the incoherent speech is seen in some patients with schizophrenia, is that it reflects impairment in frontal/executive function. While this proposal has received support in neuropsychological studies, it has been relatively little tested using functional imaging. This study aimed to examine brain activations associated with FTD, and its two main factor-analytically derived subsyndromes, during the performance of a working memory task.

Methods

Seventy patients with schizophrenia showing a full range of FTD scores and 70 matched healthy controls underwent fMRI during the performance of the 2-back version of the n-back task. Whole-brain corrected, voxel-based correlations with FTD scores were examined in the patient group.

Results

During 2-back performance the patients showed clusters of significant inverse correlation with FTD scores in the inferior frontal cortex and dorsolateral prefrontal cortex bilaterally, the left temporal cortex and subcortically in the basal ganglia and thalamus. Further analysis revealed that these correlations reflected an association only with ‘alogia’ (poverty of speech, poverty of content of speech and perseveration) and not with the ‘fluent disorganization’ component of FTD.

Conclusions

This study provides functional imaging support for the view that FTD in schizophrenia may involve impaired executive/frontal function. However, the relationship appears to be exclusively with alogia and not with the variables contributing to fluent disorganization.

Type
Original Article
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

Alexander, M. P., Benson, D. F., & Stuss, D. T. (1989). Frontal lobes and language. Brain and Language, 37, 656691.CrossRefGoogle Scholar
Andreasen, N. C. (1979). Thought, language, and communication disorders. I. Clinical assessment, definition of terms, and evaluation of their reliability. Archives of General Psychiatry, 36, 13151321.CrossRefGoogle ScholarPubMed
Andreasen, N. C. (1982). Negative symptoms in schizophrenia. Definition and reliability. Archives of General Psychiatry, 39, 784788.CrossRefGoogle ScholarPubMed
Andreasen, N. C. (1986). Scale for the assessment of thought, language, and communication (tlc). Schizophrenia Bulletin, 12, 473482.CrossRefGoogle Scholar
Andreasen, N. C., & Grove, W. M. (1986). Thought, language, and communication in schizophrenia: Diagnosis and prognosis. Schizophrenia Bulletin, 12, 348359.CrossRefGoogle ScholarPubMed
Baddeley, A., & Wilson, B. (1988). Frontal amnesia and the dysexecutive syndrome. Brain and Cognition, 7, 212230.CrossRefGoogle ScholarPubMed
Beckmann, C. F., Jenkinson, M., & Smith, S. M. (2003). General multilevel linear modeling for group analysis in fMRI. Neuroimage, 20, 10521063.CrossRefGoogle Scholar
Blumer, D., & Benson, D. F. (1975). Personality changes with frontal and temporal lobe lesions. In Benson, D. F. and Blumer, D. (Eds.), Psychiatric aspects of neurologic disease (pp. 151170). New York: Grune & Stratton.Google Scholar
Bora, E., Yalincetin, B., Akdede, B. B., & Alptekin, K. (2019). Neurocognitive and linguistic correlates of positive and negative formal thought disorder: A meta-analysis. Schizophrenia Research, 209, 211.CrossRefGoogle ScholarPubMed
Chaika, E. (1990). Understanding psychotic speech: Beyond Freud and Chomsky. Springfield: Charles C. Thomas.Google Scholar
Del Ser, T., Gonzalez-Montalvo, J. I., Martinez-Espinosa, S., Delgado-Villapalos, C., & Bermejo, F. (1997). Estimation of premorbid intelligence in Spanish people with the word accentuation test and its application to the diagnosis of dementia. Brain and Cognition, 33, 343356.CrossRefGoogle ScholarPubMed
Dibben, C. R., Rice, C., Laws, K., & McKenna, P. J. (2009). Is executive impairment associated with schizophrenic syndromes? A meta-analysis. Psychological Medicine, 39, 381392.CrossRefGoogle ScholarPubMed
Erkwoh, R., Sabri, O., Schreckenberger, M., Setani, K., Assfalg, S., Sturz, L., … Plessmann, S. (2002). Cerebral correlates of selective attention in schizophrenic patients with formal thought disorder: A controlled H2 15O-PET study. Psychiatry Research, 115, 137153.CrossRefGoogle ScholarPubMed
Gevins, A., & Cutillo, B. (1993). Spatiotemporal dynamics of component processes in human working memory. Electroencephalography and Clinical Neurophysiology, 87, 128143.CrossRefGoogle ScholarPubMed
Gomar, J. J., Ortiz-Gil, J., McKenna, P. J., Salvador, R., Sans-Sansa, B., Sarro, S., … Pomarol-Clotet, E. (2011). Validation of the word accentuation test (tap) as a means of estimating premorbid iq in Spanish speakers. Schizophrenia Research, 128, 175176.CrossRefGoogle ScholarPubMed
Green, D. M., & Swets, J. A. (1966). Signal detection theory and psychophysics. New York: Krieger.Google Scholar
Kay, S. R., Fiszbein, A., & Opler, L. A. (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin, 13, 261276.CrossRefGoogle Scholar
Kircher, T., Brohl, H., Meier, F., & Engelen, J. (2018). Formal thought disorders: From phenomenology to neurobiology. The Lancet. Psychiatry, 5, 515526.CrossRefGoogle ScholarPubMed
Kircher, T., Liddle, P., Brammer, M., Murray, R., & McGuire, P. (2003). [Neural correlates of “negative” formal thought disorder]. Nervenarzt, 74, 748754.CrossRefGoogle Scholar
Kircher, T. T., Liddle, P. F., Brammer, M. J., Williams, S. C., Murray, R. M., & McGuire, P. K. (2001). Neural correlates of formal thought disorder in schizophrenia: Preliminary findings from a functional magnetic resonance imaging study. Archives of General Psychiatry, 58, 769774.CrossRefGoogle ScholarPubMed
Liddle, P. F. (1987). Schizophrenic syndromes, cognitive performance and neurological dysfunction. Psychological Medicine, 17, 4957.CrossRefGoogle ScholarPubMed
McGrath, J. (1991). Ordering thoughts on thought disorder. British Journal of Psychiatry, 158, 307316.CrossRefGoogle ScholarPubMed
McKenna, P. J., & Oh, T. (2005). Schizophrenic speech: Making sense of bathroots and ponds that fall in doorways. Cambridge: Cambridge University Press.Google Scholar
Neary, D., Snowden, J. S., Northen, B., & Goulding, P. (1988). Dementia of frontal lobe type. Journal of Neurology Neurosurgery and Psychiatry, 51, 353361.CrossRefGoogle ScholarPubMed
Novoa, O. P., & Ardila, A. (1987). Linguistic abilities in patients with prefrontal damage. Brain and Language, 30, 206225.CrossRefGoogle ScholarPubMed
Oh, T. M., McCarthy, R. A., & McKenna, P. J. (2002). Is there a schizophasia? A study applying the single case approach to formal thought disorder in schizophrenia. Neurocase, 8, 233244.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, 4659.CrossRefGoogle ScholarPubMed
Peralta, V., Cuesta, M. J., & de Leon, J. (1992). Formal thought disorder in schizophrenia: A factor analytic study. Comprehensive Psychiatry, 33, 105110.CrossRefGoogle ScholarPubMed
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, 312323.CrossRefGoogle Scholar
Roche, E., Creed, L., MacMahon, D., Brennan, D., & Clarke, M. (2015). The epidemiology and associated phenomenology of formal thought disorder: A systematic review. Schizophrenia Bulletin, 41, 951962.CrossRefGoogle ScholarPubMed
Rochester, S. R., & Martin, J. R. (1979). Crazy talk: A study of the discourse of schizophrenic speakers. New York: Plenum.CrossRefGoogle Scholar
Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E., Johansen-Berg, H., … Matthews, P. M. (2004). Advances in functional and structural mr image analysis and implementation as fsl. Neuroimage, 23(Suppl 1), S208S219.CrossRefGoogle ScholarPubMed
Tagamets, M. A., Cortes, C. R., Griego, J. A., & Elvevag, B. (2014). Neural correlates of the relationship between discourse coherence and sensory monitoring in schizophrenia. Cortex, 55, 7787.CrossRefGoogle Scholar
Wensing, T., Cieslik, E. C., Muller, V. I., Hoffstaedter, F., Eickhoff, S. B., & Nickl-Jockschat, T. (2017). Neural correlates of formal thought disorder: An activation likelihood estimation meta-analysis. Human Brain Mapping, 38, 49464965.CrossRefGoogle ScholarPubMed
Ziauddeen, H., Dibben, C., Kipps, C., Hodges, J. R., & McKenna, P. J. (2011). Negative schizophrenic symptoms and the frontal lobe syndrome: One and the same? European Archives of Psychiatry and Clinical Neuroscience, 261, 5967.CrossRefGoogle ScholarPubMed
Supplementary material: File

Fuentes-Claramonte et al. supplementary material

Table S1

Download Fuentes-Claramonte et al. supplementary material(File)
File 16.5 KB