Neural basis of speech-gesture mismatch detection in schizophrenia spectrum disorders
Background: Patients suffering from schizophrenia spectrum disorders experience the grave effects of their illness on various facets of their daily lives. Previous investigations have shown that schizophrenia spectrum disorder patients have deficits in the perception and recognition of speech accom...
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Format: | Doctoral Thesis |
Language: | English |
Published: |
Philipps-Universität Marburg
2023
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Online Access: | PDF Full Text |
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Summary: | Background: Patients suffering from schizophrenia spectrum disorders experience the grave effects of their illness on various facets of their daily lives.
Previous investigations have shown that schizophrenia spectrum disorder patients have deficits in the perception and recognition of speech accompanied by gestures. In particular, they struggle to differentiate between related and unrelated speech-gesture combinations. Also, patients have considerable difficulties in understanding and processing abstract semantic information. A key region in the integration of speech and gesture is the inferior frontal gyrus embedded in a frontotemporal network, however, it is unclear which neural mechanisms contribute to defective mismatch and abstractness perception during the mismatch detection task.
Objective: This study aimed to investigate the neural underpinnings of impaired speech-gesture mismatch detection and abstract semantic processing in schizophrenia spectrum disorder patients and to identify relevant dysfunctional brain areas.
Methods: A novel mismatch-detection fMRI paradigm was implemented manipulating speech-gesture abstractness (abstract/concrete) and relatedness (related/unrelated). During fMRI data acquisition, 42 patients (schizophrenia, schizoaffective disorder or other non-organic psychotic disorder [ICD-10: F20, F25, F28; DSM-IV: 295.X]) and 36 healthy controls were presented with short video clips of an actor reciting abstract or concrete sentences accompanied by either a semantically related or unrelated gesture. Participants indicated via button press whether they perceived each gesture as matching the speech content or not.
We compared task performances across groups and semantic context (abstract/concrete) using the detection rate from Signal Detection Theory by repeated-measures ANOVA.
For the functional MRI data, an event-related design was chosen to measure the hemodynamic responses to each presented video. The data were loaded into a flexible-factorial analysis in a 2 x 2 x 2 design (group x abstractness x relatedness). Between-group conjunctions and group differences were respectively calculated for the contrasts unrelated > related and abstract > concrete in whole-brain analyses.
Results: Speech-gesture mismatch detection performance was significantly impaired in patients compared to controls, irrespective of abstractness. fMRI data analysis revealed that patients exhibited reduced engagement of the right supplementary motor area and bilateral anterior cingulate cortices for unrelated > related stimuli. A rostral part of the supplementary motor area was equally activated in both groups. In contrast, we found frontotemporal hyperactivation in patients for the same contrast. Furthermore, patients showed lower activation in bilateral frontal areas including the inferior frontal gyrus for all abstract > concrete speech-gesture pairs. The temporal lobe, however, was engaged in both groups equally for this contrast.
Discussion: In this study, we found evidence for impaired gesture-speech relatedness judgment in schizophrenia spectrum disorders. This was accompanied by dysfunctions of the supplementary motor area and the anterior cingulate cortices, possibly reflecting reduced facilitation of comprehension and defective error processing for unrelated speech-gesture combinations. The frontotemporal hyperactivation may represent an increased processing effort to compensate for the dysfunction. In addition, our data confirmed the conjecture of an inferior frontal gyrus dysfunction contributing to impaired processing of abstract semantic stimuli. Partially intact processing was discovered in a rostral part of the supplementary motor area for mismatches, and in the temporal lobes for abstract stimuli. These findings suggest that semantic processing in schizophrenia spectrum disorders is not completely dysfunctional, but that there is a functioning basis on which therapeutic measures can build on.
Conclusion: We provide first evidence that impaired speech-gesture mismatch detection in schizophrenia spectrum disorders could be the result of dysfunctional activation of the supplementary motor area and anterior cingulate cortex. Failure to activate the left inferior frontal gyrus disrupts the integration of abstract speech-gesture combinations in particular. Future investigations should focus on brain-stimulation of these regions to improve communication and social functioning in schizophrenia spectrum disorders. |
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Physical Description: | 137 Pages |
DOI: | 10.17192/z2023.0412 |