Reduced frontal theta oscillations indicate altered crossmodal prediction error processing in schizophrenia

Abstract

Our brain generates predictions about forthcoming stimuli and compares predicted with incoming input. Failures in predicting events might contribute to hallucinations and delusions in schizophrenia (SZ). When a stimulus violates prediction, neural activity that reflects prediction error (PE) processing is found. While PE processing deficits have been reported in unisensory paradigms, it is unknown whether SZ patients (SZP) show altered crossmodal PE processing. We measured high-density electroencephalography and applied source estimation approaches to investigate crossmodal PE processing generated by audiovisual speech. In SZP and healthy control participants (HC), we used an established paradigm in which high- and low-predictive visual syllables were paired with congruent or incongruent auditory syllables. We examined crossmodal PE processing in SZP and HC by comparing differences in event-related potentials and neural oscillations between incongruent and congruent high- and low-predictive audiovisual syllables. In both groups event-related potentials between 206 and 250 ms were larger in high- compared with low-predictive syllables, suggesting intact audiovisual incongruence detection in the auditory cortex of SZP. The analysis of oscillatory responses revealed theta-band (4-7 Hz) power enhancement in high- compared with low-predictive syllables between 230 and 370 ms in the frontal cortex of HC but not SZP. Thus aberrant frontal theta-band oscillations reflect crossmodal PE processing deficits in SZ. The present study suggests a top-down multisensory processing deficit and highlights the role of dysfunctional frontal oscillations for the SZ psychopathology.

Keywords: audiovisual speech; multisensory processing; neural synchrony; oscillatory activity; predictive coding.

Fig. 1.

Trial sequence of high- and low-predictive incongruent audiovisual syllables. Each trial started with the presentation of the first static frame of a video clip that was presented for a random interval ranging from 500 to 800 ms. After this frame the video clip, in which a female speaker uttered a syllable, was presented for 2,000 ms. ISI, interstimulus interval. The participants' tasks were to respond to the occasional auditory syllable /fa/ and to an occasional change of the fixation cross, which turned into a white circle. The tasks ensured that participants were attending to the sensory inputs.

Fig. 2.

Global field power (GFP) and event-related potentials (ERPs) at fronto-central scalp electrodes. A: traces of GFP in HC (left) and SZP (right) for congruent (red lines) and incongruent (blue lines) trials. Dashed lines represent low- and solid lines represent high-predictive trials. Time 0 denotes the onset of the auditory syllable. The analysis of GFP revealed a significant condition effect in the 206–250 ms interval (highlighted in gray). B: traces of ERPs in HC (left) and SZP (right) for congruent (red lines) and incongruent (blue lines) trials. Dashed lines represent low- and solid lines high-predictive trials. ERPs revealed a typical N1-P2 amplitude pattern to the auditory syllable onset, with smaller amplitudes in SZP compared with HC.

Fig. 3.

Topographies of event-related potentials to the 4 experimental stimulus types, as well as for the difference between incongruent and congruent trials during the 206–250 ms interval.

Fig. 4.

Local autoregressive average source estimation of ERPs for the 4 experimental stimulus types and the difference between incongruent and congruent trials during the 206–250 ms interval. Figure shows similar incongruence detection in SZP and HC that was localized in the auditory cortex.

Fig. 5.

Time-frequency responses and topographies of oscillatory power. A: time-frequency responses of 4- to 30-Hz power to the 4 experimental stimulus types and the difference between incongruent and congruent trials at fronto-central scalp electrodes. Time 0 denotes the onset of the auditory syllable. The differences between incongruent and congruent trials (bottom) revealed enhanced theta-band power (i.e., 7 Hz) around 300 ms, particularly in the control group. B: topographies of fronto-central theta-band power. Bold dots at bottom (differences) denote the electrode group in which a significant Group × Condition interaction was found in the 230–370 ms interval. Theta-band power was enhanced in the control group, especially in the incongruent high condition.

Fig. 6.

Traces of fronto-central theta-band power: traces of theta-band power in HC (left) and SZP (right) for congruent (red lines) and incongruent (blue lines) trials at fronto-central electrodes. Dashed lines represent low- and solid lines high-predictive trials. The time course of theta-band power was similar in HC and SZP, while the amplitude was substantially reduced in SZP, most strongly in the incongruent high condition.

Fig. 7.

DICS source analysis of oscillatory power in the theta band. The source of theta-band power was localized in the medial frontal gyrus and anterior cingulate cortex. In HC crossmodal PE processing was found in frontal areas, particularly in the high-predictive condition. No such effect was observed in SZP.

Fig. 8.

Summary of main results. Amplitudes of GFP (left) and 7.5-Hz power (right) at fronto-central electrodes. Amplitudes of GFP are depicted for the interval of 206–250 ms. GFP differences (incongruent minus congruent trials) were positive in high- and negative in low-predictive trials. The pattern of effects did not differ between groups (bottom left). Amplitudes of 7.5-Hz power are depicted for the 230–370 ms interval. Power differences between incongruent and congruent trials were stronger in high- compared with low-predictive trials, particularly in the HC group (bottom right).