Left-dominant temporal-frontal hypercoupling in schizophrenia patients with hallucinations during speech perception

Abstract

Background: Task-based functional neuroimaging studies of schizophrenia have not yet replicated the increased coordinated hyperactivity in speech-related brain regions that is reported with symptom-capture and resting-state studies of hallucinations. This may be due to suboptimal selection of cognitive tasks.

Methods: In the current study, we used a task that allowed experimental manipulation of control over verbal material and compared brain activity between 23 schizophrenia patients (10 hallucinators, 13 nonhallucinators), 22 psychiatric (bipolar), and 27 healthy controls. Two conditions were presented, one involving inner verbal thought (in which control over verbal material was required) and another involving speech perception (SP; in which control verbal material was not required).

Results: A functional connectivity analysis resulted in a left-dominant temporal-frontal network that included speech-related auditory and motor regions and showed hypercoupling in past-week hallucinating schizophrenia patients (relative to nonhallucinating patients) during SP only.

Conclusions: These findings replicate our previous work showing generalized speech-related functional network hypercoupling in schizophrenia during inner verbal thought and SP, but extend them by suggesting that hypercoupling is related to past-week hallucination severity scores during SP only, when control over verbal material is not required. This result opens the possibility that practicing control over inner verbal thought processes may decrease the likelihood or severity of hallucinations.

Keywords: functional connectivity; functional magnetic resonance imaging; inner speech; schizophrenia; speech perception.

© The Author 2014. Published by Oxford University Press on behalf of the Maryland Psychiatric Research Center. All rights reserved. For permissions, please email: journals.permissions@oup.com.

Figures

Fig. 1.

Timeline of the experimental procedure. Participants were instructed to either mentally generate (voluntary verbal thought generation; VTG) or to listen to (speech perception; SP) a simple definition of a word (eg, “Something you rest your head on when sleeping” for the word “pillow”). The conditions were cued with the words “something you…” or “listen…” presented under the images for the VTG and SP conditions, respectively. The VTG condition is depicted here. For a color version, see this figure online.

Fig. 2.

(A) Dominant 10% of component loadings for component 1 (red/yellow = positive loadings, threshold = 0.20, max = 0.37, no negative loadings passed threshold) and component 2 (blue/green = negative loadings, negative threshold = −0.14, min = −0.25). Component 2 positive loadings in the occipital regions overlapped with those from component 1 (see supplementary tables 2 and 3). Axial slices are located at Montreal Neurological Institute Z-axis coordinates −32, −12, −1, 24, 48. (B) Mean finite impulse response (FIR)-based predictor weights for speech perception, averaged over components and plotted as a function of peristimulus time. (C) Mean FIR-based predictor weights for voluntary verbal thought generation, averaged over components and plotted as a function of peristimulus time. Error bars are SEs. HDR, estimated hemodynamic response; L, left; R, right; SZ, schizophrenia. For a color version, see this figure online.