Early auditory processing dysfunction in schizophrenia: Mechanisms and implications

Dondé, Clément; Kantrowitz, Joshua T.; Medalia, Alice; Saperstein, Alice M.; Balla, Andrea; Sehatpour, Pejman; Martı́nez, Antı́gona; O’Connell, Monica N.; Javitt, Daniel C.

doi:10.1016/j.neubiorev.2023.105098

Cited by 13 publications

(7 citation statements)

References 291 publications

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“…Alongside the existing evidence suggesting deficits in multisensory speech perception in SZs [ 22 , 24 , 27 , 28 , 34 ], these patients also show deficits in unisensory visual [ 46 , 47 ] and auditory processing [ 48 , 49 , 50 , 51 , 52 , 53 ], which can affect speech comprehension independently. In addition to the reported behavioral data, the electrophysiological results may offer further insights into the observed group difference.…”

Section: Discussionmentioning

confidence: 68%

Deficient Audiovisual Speech Perception in Schizophrenia: An ERP Study

Ghaneirad,

Saenger,

Szycik

et al. 2023

Brain Sciences

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In everyday verbal communication, auditory speech perception is often disturbed by background noise. Especially in disadvantageous hearing conditions, additional visual articulatory information (e.g., lip movement) can positively contribute to speech comprehension. Patients with schizophrenia (SZs) demonstrate an aberrant ability to integrate visual and auditory sensory input during speech perception. Current findings about underlying neural mechanisms of this deficit are inconsistent. Particularly and despite the importance of early sensory processing in speech perception, very few studies have addressed these processes in SZs. Thus, in the present study, we examined 20 adult subjects with SZ and 21 healthy controls (HCs) while presenting audiovisual spoken words (disyllabic nouns) either superimposed by white noise (−12 dB signal-to-noise ratio) or not. In addition to behavioral data, event-related brain potentials (ERPs) were recorded. Our results demonstrate reduced speech comprehension for SZs compared to HCs under noisy conditions. Moreover, we found altered N1 amplitudes in SZ during speech perception, while P2 amplitudes and the N1-P2 complex were similar to HCs, indicating that there may be disturbances in multimodal speech perception at an early stage of processing, which may be due to deficits in auditory speech perception. Moreover, a positive relationship between fronto-central N1 amplitudes and the positive subscale of the Positive and Negative Syndrome Scale (PANSS) has been observed.

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Section: Discussionmentioning

confidence: 68%

Deficient Audiovisual Speech Perception in Schizophrenia: An ERP Study

Ghaneirad,

Saenger,

Szycik

et al. 2023

Brain Sciences

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show abstract

Section: Discussionmentioning

confidence: 99%

“…Among various perceptual and cognitive deficits, early auditory deficits play a crucial role in the pathophysiology of SZ ( Javitt and Sweet, 2015 ; Dondé et al, 2023 ). A recent conceptual review ( Dondé et al, 2023 ) highlights the utility of auditory measures for treatment targets and translational biomarker research. Alternation of gamma-band ASSR is one of the most prominent neurophysiological markers for early auditory deficits in SZ ( Hirano and Uhlhaas, 2021 ; Onitsuka et al, 2022c ).…”

Section: Discussionmentioning

confidence: 99%

“…Notably, our previous MEG study ( Tsuchimoto et al, 2011 ) showed that evoked power and PLF of the 80 Hz ASSR demonstrated greater differential sensitivity to SZ patients compared to those of the 20, 30, and 40 Hz ASSRs. Moreover, early auditory deficits within the auditory cortices are known to play a crucial role in the pathophysiology of SZ ( Javitt and Sweet, 2015 ; Dondé et al, 2023 ). Hence, it would be of great interest to investigate whether SZ patients exhibit reduced evoked power and PLF and a phase delay in the 80 Hz ASSR within the primary and secondary auditory cortex.…”

Section: Introductionmentioning

confidence: 99%

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Abnormal phase entrainment of low- and high-gamma-band auditory steady-state responses in schizophrenia

Nakanishi,

Tamura,

Hirano

et al. 2023

Front. Neurosci.

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IntroductionGamma-band oscillatory deficits have attracted considerable attention as promising biomarkers of schizophrenia (SZ). Notably, a reduced auditory steady-state response (ASSR) in the low gamma band (40 Hz) is widely recognized as a robust finding among SZ patients. However, a comprehensive investigation into the potential utility of the high-gamma-band ASSR in detecting altered neural oscillations in SZ has not yet been conducted.MethodsThe present study aimed to assess the ASSR using magnetoencephalography (MEG) data obtained during steady-state stimuli at frequencies of 20, 30, 40, and 80 Hz from 23 SZ patients and 21 healthy controls (HCs). To evaluate the ASSR, we examined the evoked power and phase-locking factor (PLF) in the time-frequency domain for both the primary and secondary auditory cortices. Furthermore, we calculated the phase-locking angle (PLA) to examine oscillatory phase lead or delay in SZ patients. Taking advantage of the high spatial resolution of MEG, we also focused on the hemispheric laterality of low- and high-gamma-band ASSR deficits in SZ.ResultsWe found abnormal phase delay in the 40 Hz ASSR within the bilateral auditory cortex of SZ patients. Regarding the 80 Hz ASSR, our investigation identified an aberrant phase lead in the left secondary auditory cortex in SZ, accompanied by reduced evoked power in both auditory cortices.DiscussionGiven that abnormal phase lead on 80 Hz ASSR exhibited the highest discriminative power between HC and SZ, we propose that the examination of PLA in the 80 Hz ASSR holds significant promise as a robust candidate for identifying neurophysiological endophenotypes associated with SZ. Furthermore, the left-hemisphere phase lead observed in the deficits of 80 Hz PLA aligns with numerous prior studies, which have consistently proposed that SZ is characterized by left-lateralized brain dysfunctions.

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“…However, the ease of measuring MMN and the replicability of smaller MMN amplitude have contributed to interest in how it might relate to other observed brain changes. While theories put forward to explain the etiology of schizophrenia are many and varied, that most closely tied to the process underlying MMN is the glutamate hypothesis 23 as it pertains to altered synaptic plasticity implicating disruption to n ‐methyl‐ d ‐aspartate (NMDA) glutamate receptors, the excitatory–inhibitory balance in neurotransmission, and potential consequences for brain structure and connectivity 24–31 . Indeed, MMN has also been promoted as an exemplar of the synaptic plasticity involved in the fundamental role of “error‐signaling” in brain function generally 16,32 and altered inferential processing in schizophrenia specifically 33–37 .…”

Section: What Process Does Mismatch Negativity (Mmn) Index?mentioning

confidence: 99%

Why mismatch negativity continues to hold potential in probing altered brain function in schizophrenia

Todd,

Salisbury,

Michie

2023

PCN Reports

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The brain potential known as mismatch negativity (MMN) is one of the most studied indices of altered brain function in schizophrenia. This review looks at what has been learned about MMN in schizophrenia over the last three decades and why the level of interest and activity in this field of research remains strong. A diligent consideration of available evidence suggests that MMN can serve as a biomarker in schizophrenia, but perhaps not the kind of biomarker that early research supposed. This review concludes that MMN measurement is likely to be most useful as a monitoring and response biomarker enabling tracking of an underlying pathology and efficacy of interventions, respectively. The role of, and challenges presented by, pre‐clinical models is discussed as well as the merits of different methodologies that can be brought to bear in pursuing a deeper understanding of pathophysiology that might explain smaller MMN in schizophrenia.

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Early auditory processing dysfunction in schizophrenia: Mechanisms and implications

Cited by 13 publications

References 291 publications

Deficient Audiovisual Speech Perception in Schizophrenia: An ERP Study

Deficient Audiovisual Speech Perception in Schizophrenia: An ERP Study

Abnormal phase entrainment of low- and high-gamma-band auditory steady-state responses in schizophrenia

Why mismatch negativity continues to hold potential in probing altered brain function in schizophrenia

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