Yadira Roa Romero

GABA concentration in superior temporal sulcus predicts gamma power and perception in the sound-induced flash illusion

In everyday life we are confronted with inputs of multisensory stimuli that need to be integrated across our senses. Individuals vary considerably in how they integrate multisensory information, yet the neurochemical foundations underlying this variability are not well understood. Neural oscillations, especially in the gamma band (>30Hz) play an important role in multisensory processing. Furthermore, gamma-aminobutyric acid (GABA) neurotransmission contributes to the generation of gamma band oscillations (GBO), which can be sustained by activation of metabotropic glutamate receptors. Hence, differences in the GABA and glutamate systems might contribute to individual differences in multisensory processing. In this combined magnetic resonance spectroscopy and electroencephalography study, we examined the relationships between GABA and glutamate concentrations in the superior temporal sulcus (STS), source localized GBO, and illusion rate in the sound-induced flash illusion (SIFI). In 39 human volunteers we found robust relationships between GABA concentration, GBO power, and the SIFI perception rate (r-values=0.44 to 0.53). The correlation between GBO power and SIFI perception rate was about twofold higher when the modulating influence of the GABA level was included in the analysis as compared to when it was excluded. No significant effects were obtained for glutamate concentration. Our study suggests that the GABA level shapes individual differences in audiovisual perception through its modulating influence on GBO. GABA neurotransmission could be a promising target for treatment interventions of multisensory processing deficits in clinical populations, such as schizophrenia or autism.

Early and late beta-band power reflect audiovisual perception in the McGurk illusion

The McGurk illusion is a prominent example of audiovisual speech perception and the influence that visual stimuli can have on auditory perception. In this illusion, a visual speech stimulus influences the perception of an incongruent auditory stimulus, resulting in a fused novel percept. In this high-density electroencephalography (EEG) study, we were interested in the neural signatures of the subjective percept of the McGurk illusion as a phenomenon of speech-specific multisensory integration. Therefore, we examined the role of cortical oscillations and event-related responses in the perception of congruent and incongruent audiovisual speech. We compared the cortical activity elicited by objectively congruent syllables with incongruent audiovisual stimuli. Importantly, the latter elicited a subjectively congruent percept: the McGurk illusion. We found that early event-related responses (N1) to audiovisual stimuli were reduced during the perception of the McGurk illusion compared with congruent stimuli. Most interestingly, our study showed a stronger poststimulus suppression of beta-band power (13-30 Hz) at short (0-500 ms) and long (500-800 ms) latencies during the perception of the McGurk illusion compared with congruent stimuli. Our study demonstrates that auditory perception is influenced by visual context and that the subsequent formation of a McGurk illusion requires stronger audiovisual integration even at early processing stages. Our results provide evidence that beta-band suppression at early stages reflects stronger stimulus processing in the McGurk illusion. Moreover, stronger late beta-band suppression in McGurk illusion indicates the resolution of incongruent physical audiovisual input and the formation of a coherent, illusory multisensory percept.

Positive and Negative Symptoms in Schizophrenia Relate to Distinct Oscillatory Signatures of Sensory Gating.

Oscillatory activity in neural populations and temporal synchronization within these populations are important mechanisms contributing to perception and cognition. In schizophrenia, perception and cognition are impaired. Aberrant gating of irrelevant sensory information, which has been related to altered oscillatory neural activity, presumably contributes to these impairments. However, the link between schizophrenia symptoms and sensory gating deficits, as reflected in oscillatory activity, is not clear. In this electroencephalography study, we used a paired-stimulus paradigm to investigate frequency-resolved oscillatory activity in 22 schizophrenia patients and 22 healthy controls. We found sensory gating deficits in patients compared to controls, as reflected in reduced gamma-band power and alpha-band phase synchrony difference between the first and the second auditory stimulus. We correlated these markers of neural activity with a five-factor model of the Positive and Negative Syndrome Scale. Gamma-band power sensory gating was positively correlated with positive symptoms. Moreover, alpha-band phase synchrony sensory gating was negatively correlated with negative symptoms. A cluster analysis revealed three schizophrenia phenotypes, characterized by (i) aberrant gamma-band power and high positive symptoms, (ii) aberrant alpha-band phase synchrony, low positive, and low negative symptom scores or (iii) by intact sensory gating and high negative symptoms. Our study demonstrates that aberrant neural synchronization, as reflected in gamma-band power and alpha-band phase synchrony, relates to the schizophrenia psychopathology. Different schizophrenia phenotypes express distinct levels of positive and negative symptoms as well as varying degrees of aberrant oscillatory neural activity. Identifying the individual phenotype might improve therapeutic interventions in schizophrenia.

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

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.

Beta/Gamma Oscillations and Event-Related Potentials Indicate Aberrant Multisensory Processing in Schizophrenia

Recent behavioral and neuroimaging studies have suggested multisensory processing deficits in patients with schizophrenia (SCZ). Thus far, the neural mechanisms underlying these deficits are not well understood. Previous studies with unisensory stimulation have shown altered neural oscillations in SCZ. As such, altered oscillations could contribute to aberrant multisensory processing in this patient group. To test this assumption, we conducted an electroencephalography (EEG) study in 15 SCZ and 15 control participants in whom we examined neural oscillations and event-related potentials (ERPs) in the sound-induced flash illusion (SIFI). In the SIFI multiple auditory stimuli that are presented alongside a single visual stimulus can induce the illusory percept of multiple visual stimuli. In SCZ and control participants we compared ERPs and neural oscillations between trials that induced an illusion and trials that did not induce an illusion. On the behavioral level, SCZ (55.7%) and control participants (55.4%) did not significantly differ in illusion rates. The analysis of ERPs revealed diminished amplitudes and altered multisensory processing in SCZ compared to controls around 135 ms after stimulus onset. Moreover, the analysis of neural oscillations revealed altered 25–35 Hz power after 100 to 150 ms over occipital scalp for SCZ compared to controls. Our findings extend previous observations of aberrant neural oscillations in unisensory perception paradigms. They suggest that altered ERPs and altered occipital beta/gamma band power reflect aberrant multisensory processing in SCZ.

Reduced low-frequency power and phase locking reflect restoration in the auditory continuity illusion

Interruptions in auditory input can be perceptually restored if they coincide with a masking sound, resulting in a continuity illusion. Previous studies have shown that this continuity illusion is associated with reduced low‐frequency neural oscillations in the auditory cortex. However, the precise contribution of oscillatory amplitude changes and phase alignment to auditory restoration remains unclear. Using electroencephalography, we investigated induced power changes and phase locking in response to 3 Hz amplitude‐modulated tones during the interval of an interrupting noise. We experimentally manipulated both the physical continuity of the tone (continuous vs. interrupted) and the masking potential of the noise (notched vs. full). We observed an attenuation of 3 Hz power during continuity illusions in comparison with both continuous tones and veridically perceived interrupted tones. This illusion‐related suppression of low‐frequency oscillations likely reflects a blurring of auditory object boundaries that supports continuity perception. We further observed increased 3 Hz phase locking during fully masked continuous tones compared with the other conditions. This low‐frequency phase alignment may reflect the neural registration of the interrupting noise as a newly appearing object, whereas during continuity illusions, a spectral portion of this noise is delegated to filling the interruption. Taken together, our findings suggest that the suppression of slow cortical oscillations in both the power and phase domains supports perceptual restoration of interruptions in auditory input.

Glutamate Concentration in the Superior Temporal Sulcus Relates to Neuroticism in Schizophrenia

Clinical studies suggest aberrant neurotransmitter concentrations in the brains of patients with schizophrenia (SCZ). Numerous studies have indicated deviant glutamate concentrations in SCZ, although the findings are inconsistent. Moreover, alterations in glutamate concentrations could be linked to personality traits in SCZ. Here, we examined the relationships between personality dimensions and glutamate concentrations in a voxel encompassing the occipital cortex (OCC) and another voxel encompassing the left superior temporal sulcus (STS). We used proton magnetic resonance spectroscopy to examine glutamate concentrations in the OCC and the STS in 19 SCZ and 21 non-psychiatric healthy control (HC) participants. Personality dimensions neuroticism, extraversion, openness, agreeableness and conscientiousness were assessed using the NEO-FFI questionnaire. SCZ compared to HC showed higher glutamate concentrations in the STS, reduced extraversion scores, and enhanced neuroticism scores. No group differences were observed for the other personality traits and for glutamate concentrations in the OCC. For the SCZ group, glutamate concentrations in STS were negatively correlated with the neuroticism scores [r = -0.537, p = 0.018] but this was not found in HC [r(19) = 0.011, p = 0.962]. No other significant correlations were found. Our study showed an inverse relationship between glutamate concentrations in the STS and neuroticism scores in SCZ. Elevated glutamate in the STS might serve as a compensatory mechanism that enables patients with enhanced concentrations to control and prevent the expression of neuroticism.

Corrigendum: Positive and Negative Symptoms in Schizophrenia Relate to Distinct Oscillatory Signatures of Sensory Gating

[This corrects the article on p. 104 in vol. 10, PMID: 27014035.].