Deficient Audiovisual Speech Perception in Schizophrenia: An ERP Study

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.

[1]  Rajan Iyyalol,et al.  Dexamphetamine widens temporal and spatial binding windows in healthy participants , 2023, Journal of psychiatry & neuroscience : JPN.

[2]  D. Javitt,et al.  Early auditory processing dysfunction in schizophrenia: Mechanisms and implications , 2023, Neuroscience & Biobehavioral Reviews.

[3]  D. Senkowski,et al.  Early evoked brain activity underlies auditory and audiovisual speech recognition deficits in schizophrenia , 2021, NeuroImage: Clinical.

[4]  L. Eriksson,et al.  A systematic review of the neural correlates of multisensory integration in schizophrenia , 2021, Schizophrenia Research: Cognition.

[5]  G. Szycik,et al.  Enhanced attentional processing during speech perception in adult high-functioning autism spectrum disorder: An ERP-study , 2021, Neuropsychologia.

[6]  R. McCarley,et al.  Deficit Effect Sizes and Correlations of Auditory Event-Related Potentials at First Hospitalization in the Schizophrenia Spectrum , 2020, Clinical EEG and neuroscience.

[7]  I. Sommer,et al.  Anomalies in language as a biomarker for schizophrenia. , 2020, Current opinion in psychiatry.

[8]  B. Straube,et al.  Dynamic Causal Modelling suggests impaired effective connectivity in patients with schizophrenia spectrum disorders during gesture-speech integration , 2019, Schizophrenia Research.

[9]  T. Iidaka,et al.  A review of impaired visual processing and the daily visual world in patients with schizophrenia , 2018, Nagoya journal of medical science.

[10]  R. Chan,et al.  Multisensory temporal binding window in autism spectrum disorders and schizophrenia spectrum disorders: A systematic review and meta-analysis , 2018, Neuroscience & Biobehavioral Reviews.

[11]  D. Senkowski,et al.  Beta/Gamma Oscillations and Event-Related Potentials Indicate Aberrant Multisensory Processing in Schizophrenia , 2016, Front. Psychol..

[12]  D. Senkowski,et al.  Alpha-Band Oscillations Reflect Altered Multisensory Processing of the McGurk Illusion in Schizophrenia , 2016, Front. Hum. Neurosci..

[13]  Martijn Baart,et al.  Early processing of auditory lexical predictions revealed by ERPs , 2015, Neuroscience Letters.

[14]  S. Shergill,et al.  Eluding the illusion? Schizophrenia, dopamine and the McGurk effect , 2014, Front. Hum. Neurosci..

[15]  J. Vroomen,et al.  Electrophysiological evidence for speech-specific audiovisual integration , 2014, Neuropsychologia.

[16]  Hinderk M. Emrich,et al.  N1 enhancement in synesthesia during visual and audio–visual perception in semantic cross-modal conflict situations: an ERP study , 2014, Front. Hum. Neurosci..

[17]  A. Karmiloff-Smith,et al.  Audio-visual speech perception: a developmental ERP investigation , 2013, Developmental science.

[18]  B. Liu,et al.  Correlation between audio–visual enhancement of speech in different noise environments and SNR: A combined behavioral and electrophysiological study , 2013, Neuroscience.

[19]  S. Soto-Faraco,et al.  Visual information constrains early and late stages of spoken-word recognition in sentence context. , 2013, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[20]  Tilo Kircher,et al.  Neural integration of speech and gesture in schizophrenia: Evidence for differential processing of metaphoric gestures , 2013, Human brain mapping.

[21]  J. Vroomen,et al.  Deficient multisensory integration in schizophrenia: An event-related potential study , 2013, Schizophrenia Research.

[22]  V. V. Wassenhove,et al.  Temporal event structure and timing in schizophrenia: Preserved binding in a longer “now” , 2013, Neuropsychologia.

[23]  Liang Li,et al.  Masking of speech in people with first-episode schizophrenia and people with chronic schizophrenia , 2012, Schizophrenia Research.

[24]  David M. Groppe,et al.  Mass univariate analysis of event-related brain potentials/fields I: a critical tutorial review. , 2011, Psychophysiology.

[25]  R. Kakigi,et al.  Auditory N1 as a change-related automatic response , 2011, Neuroscience Research.

[26]  J. Stephen,et al.  Unisensory processing and multisensory integration in schizophrenia: A high-density electrical mapping study , 2011, Neuropsychologia.

[27]  John J. Foxe,et al.  The N1 auditory evoked potential component as an endophenotype for schizophrenia: high-density electrical mapping in clinically unaffected first-degree relatives, first-episode, and chronic schizophrenia patients , 2011, European Archives of Psychiatry and Clinical Neuroscience.

[28]  W. Dillo,et al.  Maladaptive connectivity of Broca’s area in schizophrenia during audiovisual speech perception: An fMRI study , 2011, Neuroscience.

[29]  D. Senkowski,et al.  The multifaceted interplay between attention and multisensory integration , 2010, Trends in Cognitive Sciences.

[30]  R. McCarley,et al.  Reductions in the N1 and P2 auditory event-related potentials in first-hospitalized and chronic schizophrenia. , 2010, Schizophrenia bulletin.

[31]  V. Ramachandran,et al.  Reduced multisensory integration in patients with schizophrenia on a target detection task , 2010, Neuropsychologia.

[32]  Valerie Kirsch,et al.  Reduced Early Auditory Evoked Gamma-Band Response in Patients with Schizophrenia , 2010, Biological Psychiatry.

[33]  D. Dietrich,et al.  Audiovisual integration of speech is disturbed in schizophrenia: An fMRI study , 2009, Schizophrenia Research.

[34]  Abraham Weizman,et al.  Differences in audiovisual integration, as measured by McGurk phenomenon, among adult and adolescent patients with schizophrenia and age-matched healthy control groups. , 2009, Comprehensive psychiatry.

[35]  O. Bertrand,et al.  Visual Activation and Audiovisual Interactions in the Auditory Cortex during Speech Perception: Intracranial Recordings in Humans , 2008, The Journal of Neuroscience.

[36]  S. Sponheim,et al.  An auditory processing abnormality specific to liability for schizophrenia , 2008, Schizophrenia Research.

[37]  John J. Foxe,et al.  Impaired multisensory processing in schizophrenia: Deficits in the visual enhancement of speech comprehension under noisy environmental conditions , 2007, Schizophrenia Research.

[38]  J. Foucher,et al.  Low time resolution in schizophrenia Lengthened windows of simultaneity for visual, auditory and bimodal stimuli , 2007, Schizophrenia Research.

[39]  B. Mazoyer,et al.  Stability of functional language lateralization over time in schizophrenia patients , 2007, Schizophrenia Research.

[40]  John J. Foxe,et al.  Seeing voices: High-density electrical mapping and source-analysis of the multisensory mismatch negativity evoked during the McGurk illusion , 2007, Neuropsychologia.

[41]  W. Singer,et al.  Neural Synchrony in Brain Disorders: Relevance for Cognitive Dysfunctions and Pathophysiology , 2006, Neuron.

[42]  Iiro P. Jääskeläinen,et al.  Inherited Auditory-Cortical Dysfunction in Twin Pairs Discordant for Schizophrenia , 2006, Biological Psychiatry.

[43]  John J. Foxe,et al.  Do you see what I am saying? Exploring visual enhancement of speech comprehension in noisy environments. , 2006, Cerebral cortex.

[44]  Karl J. Friston,et al.  Synaptic Plasticity and Dysconnection in Schizophrenia , 2006, Biological Psychiatry.

[45]  Marty G. Woldorff,et al.  Selective Attention and Multisensory Integration: Multiple Phases of Effects on the Evoked Brain Activity , 2005, Journal of Cognitive Neuroscience.

[46]  David Poeppel,et al.  Visual speech speeds up the neural processing of auditory speech. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[47]  S. Golaszewski,et al.  Brain activation patterns during a verbal fluency test—a functional MRI study in healthy volunteers and patients with schizophrenia , 2004, Schizophrenia Research.

[48]  A. Fort,et al.  Bimodal speech: early suppressive visual effects in human auditory cortex , 2004, The European journal of neuroscience.

[49]  Seung-Hwan Lee,et al.  Abnormal speech perception in schizophrenia with auditory hallucinations , 2004, Acta Neuropsychiatrica.

[50]  J. Vroomen,et al.  Audio-visual integration in schizophrenia , 2003, Schizophrenia Research.

[51]  C. Schroeder,et al.  Dysfunction of early-stage visual processing in schizophrenia. , 2001, The American journal of psychiatry.

[52]  P F Seitz,et al.  The use of visible speech cues for improving auditory detection of spoken sentences. , 2000, The Journal of the Acoustical Society of America.

[53]  R. Hoffman,et al.  Selective speech perception alterations in schizophrenic patients reporting hallucinated "voices". , 1999, The American journal of psychiatry.

[54]  L. DeLisi,et al.  Language processing and memory in ill and well siblings from multiplex families affected with schizophrenia , 1997, Schizophrenia Research.

[55]  R. Gur,et al.  Neuropsychological deficits in neuroleptic naive patients with first-episode schizophrenia. , 1994, Archives of general psychiatry.

[56]  J. Rabe-Jabłońska,et al.  [Affective disorders in the fourth edition of the classification of mental disorders prepared by the American Psychiatric Association -- diagnostic and statistical manual of mental disorders]. , 1993, Psychiatria polska.

[57]  P. McKenna,et al.  Memory, Knowledge and Delusions , 1991, British Journal of Psychiatry.

[58]  T. McGlashan,et al.  Natural history of schizophrenia subtypes. II. Positive and negative symptoms and long-term course. , 1991, Archives of general psychiatry.

[59]  W. Roth,et al.  Auditory event-related potentials and electrodermal activity in medicated and unmedicated schizophrenics , 1991, Biological Psychiatry.

[60]  C. Ogura,et al.  Abnormalities in Event‐Related Potentials, N100, P200, P300 and Slow Wave in Schizophrenia , 1991, The Japanese journal of psychiatry and neurology.

[61]  D. Pickar,et al.  National Institute of Mental Health longitudinal study of chronic schizophrenia. Prognosis and predictors of outcome. , 1991, Archives of general psychiatry.

[62]  G. Adler,et al.  Influence of stimulation parameters on auditory stimulus processing in schizophrenia and major depression: an auditory evoked potential study , 1990, Acta psychiatrica Scandinavica.

[63]  J. Ford,et al.  P3 in schizophrenia is affected by stimulus modality, response requirements, medication status, and negative symptoms. , 1989, Archives of general psychiatry.

[64]  D. Weinberger,et al.  Physiological dysfunction of dorsolateral prefrontal cortex in schizophrenia. III. A new cohort and evidence for a monoaminergic mechanism. , 1988, Archives of general psychiatry.

[65]  T. Picton,et al.  The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. , 1987, Psychophysiology.

[66]  S. Hillyard,et al.  Event-related brain potentials and selective attention to acoustic and phonetic cues , 1978, Biological Psychology.

[67]  H. McGurk,et al.  Hearing lips and seeing voices , 1976, Nature.

[68]  W. H. Sumby,et al.  Visual contribution to speech intelligibility in noise , 1954 .

[69]  Jean Vroomen,et al.  Neural Correlates of Multisensory Integration of Ecologically Valid Audiovisual Events , 2007, Journal of Cognitive Neuroscience.

[70]  B Mazoyer,et al.  Altered hemispheric functional dominance during word generation in negative schizophrenia. , 2000, Schizophrenia bulletin.

[71]  T. Crow,et al.  Anomalous cerebral asymmetry and language processing in schizophrenia. , 1997, Schizophrenia bulletin.

[72]  R. H. Baayen,et al.  The CELEX Lexical Database (CD-ROM) , 1996 .

[73]  M. Buchsbaum Frontal lobes, basal ganglia, temporal lobes--three sites for schizophrenia? , 1990, Schizophrenia bulletin.

[74]  S. Kay,et al.  The positive and negative syndrome scale (PANSS) for schizophrenia. , 1987, Schizophrenia bulletin.

[75]  M. Buchsbaum The middle evoked response components and schizophrenia. , 1977, Schizophrenia bulletin.