Distinct processing of ambiguous speech in people with non‐clinical auditory verbal hallucinations

&NA; Auditory verbal hallucinations (hearing voices) are typically associated with psychosis, but a minority of the general population also experience them frequently and without distress. Such ‘non‐clinical’ experiences offer a rare and unique opportunity to study hallucinations apart from confounding clinical factors, thus allowing for the identification of symptom‐specific mechanisms. Recent theories propose that hallucinations result from an imbalance of prior expectation and sensory information, but whether such an imbalance also influences auditory‐perceptual processes remains unknown. We examine for the first time the cortical processing of ambiguous speech in people without psychosis who regularly hear voices. Twelve non‐clinical voice‐hearers and 17 matched controls completed a functional magnetic resonance imaging scan while passively listening to degraded speech (‘sine‐wave’ speech), that was either potentially intelligible or unintelligible. Voice‐hearers reported recognizing the presence of speech in the stimuli before controls, and before being explicitly informed of its intelligibility. Across both groups, intelligible sine‐wave speech engaged a typical left‐lateralized speech processing network. Notably, however, voice‐hearers showed stronger intelligibility responses than controls in the dorsal anterior cingulate cortex and in the superior frontal gyrus. This suggests an enhanced involvement of attention and sensorimotor processes, selectively when speech was potentially intelligible. Altogether, these behavioural and neural findings indicate that people with hallucinatory experiences show distinct responses to meaningful auditory stimuli. A greater weighting towards prior knowledge and expectation might cause non‐veridical auditory sensations in these individuals, but it might also spontaneously facilitate perceptual processing where such knowledge is required. This has implications for the understanding of hallucinations in clinical and non‐clinical populations, and is consistent with current ‘predictive processing’ theories of psychosis.

[1]  R. Kahn,et al.  Aberrations in the arcuate fasciculus are associated with auditory verbal hallucinations in psychotic and in non‐psychotic individuals , 2011, Human brain mapping.

[2]  P. Fletcher,et al.  Prediction error, ketamine and psychosis: An updated model , 2016, Journal of psychopharmacology.

[3]  A. Aleman,et al.  The influence of semantic top-down processing in auditory verbal hallucinations , 2012, Schizophrenia Research.

[4]  Tom Manly,et al.  Musicians and non-musicians are equally adept at perceiving masked speech. , 2015, The Journal of the Acoustical Society of America.

[5]  R. Jardri,et al.  Circular inferences in schizophrenia. , 2013, Brain : a journal of neurology.

[6]  S. Scott,et al.  Inferior Frontal Gyrus Activation Predicts Individual Differences in Perceptual Learning of Cochlear-Implant Simulations , 2010, The Journal of Neuroscience.

[7]  J van Os,et al.  The continuity of psychotic experiences in the general population. , 2001, Clinical psychology review.

[8]  S. Kühn,et al.  Quantitative meta-analysis on state and trait aspects of auditory verbal hallucinations in schizophrenia. , 2012, Schizophrenia bulletin.

[9]  S. Grossberg How hallucinations may arise from brain mechanisms of learning, attention, and volition , 2000, Journal of the International Neuropsychological Society.

[10]  Jane R. Garrison,et al.  The neural mechanisms of hallucinations: A quantitative meta-analysis of neuroimaging studies , 2016, Neuroscience & Biobehavioral Reviews.

[11]  Matthew H. Davis,et al.  Lexical information drives perceptual learning of distorted speech: evidence from the comprehension of noise-vocoded sentences. , 2005, Journal of experimental psychology. General.

[12]  M. Coltheart,et al.  Imaginary companions and young children's responses to ambiguous auditory stimuli: implications for typical and atypical development. , 2007, Journal of child psychology and psychiatry, and allied disciplines.

[13]  Jeffrey N Rouder,et al.  Bayesian Analysis of Factorial Designs , 2017, Psychological methods.

[14]  Renaud Jardri,et al.  Cortical activations during auditory verbal hallucinations in schizophrenia: a coordinate-based meta-analysis. , 2011, The American journal of psychiatry.

[15]  Michael D. Hunter,et al.  Enhanced cortical effects of auditory stimulation and auditory attention in healthy individuals prone to auditory hallucinations during partial wakefulness , 2011, NeuroImage.

[16]  Daniel S. Margulies,et al.  Auditory Hallucinations and the Brain’s Resting-State Networks: Findings and Methodological Observations , 2016, Schizophrenia bulletin.

[17]  R. Bentall,et al.  Dissociation mediates the relationship between childhood trauma and hallucination-proneness , 2011, Psychological Medicine.

[18]  K. Kiehl,et al.  Detection of Sounds in the Auditory Stream: Event-Related fMRI Evidence for Differential Activation to Speech and Nonspeech , 2001, Journal of Cognitive Neuroscience.

[19]  C Nahmias,et al.  Where the imaginal appears real: a positron emission tomography study of auditory hallucinations. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[20]  C. Carter,et al.  Optimizing the Design and Analysis of Clinical Functional Magnetic Resonance Imaging Research Studies , 2008, Biological Psychiatry.

[21]  Jennifer Wiley,et al.  What Are the Odds? A Practical Guide to Computing and Reporting Bayes Factors , 2014, J. Probl. Solving.

[22]  Sebastiaan F W Neggers,et al.  Decreased language lateralization is characteristic of psychosis, not auditory hallucinations. , 2010, Brain : a journal of neurology.

[23]  J. Hohwy The Predictive Mind , 2013 .

[24]  T. Stiles,et al.  Prevalence of auditory verbal hallucinations in a general population: A group comparison study , 2015, Scandinavian journal of psychology.

[25]  Matthew Richardson,et al.  Phonetic processing areas revealed by sinewave speech and acoustically similar non-speech , 2006, NeuroImage.

[26]  Ben Alderson-Day,et al.  Are Hallucinations Due to an Imbalance Between Excitatory and Inhibitory Influences on the Brain? , 2016, Schizophrenia bulletin.

[27]  R. M. Murray,et al.  Functional anatomy of inner speech and auditory verbal imagery , 1995, Schizophrenia Research.

[28]  T. Raij,et al.  Poor supplementary motor area activation differentiates auditory verbal hallucination from imagining the hallucination☆ , 2012, NeuroImage: Clinical.

[29]  J Bamford,et al.  The BKB (Bamford-Kowal-Bench) sentence lists for partially-hearing children. , 1979, British journal of audiology.

[30]  Yinjuan Du,et al.  Noise differentially impacts phoneme representations in the auditory and speech motor systems , 2014, Proceedings of the National Academy of Sciences.

[31]  A. Wells,et al.  Cognitive factors in predisposition to auditory and visual hallucinations. , 2000, The British journal of clinical psychology.

[32]  Renaud Jardri,et al.  Experimental evidence for circular inference in schizophrenia , 2017, Nature Communications.

[33]  Rajesh P. N. Rao,et al.  Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. , 1999 .

[34]  K. Diederen,et al.  Healthy individuals with auditory verbal hallucinations; who are they? Psychiatric assessments of a selected sample of 103 subjects. , 2010, Schizophrenia bulletin.

[35]  Robert E Remez,et al.  Estimating speech spectra for copy synthesis by linear prediction and by hand. , 2011, The Journal of the Acoustical Society of America.

[36]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[37]  P. McGuire,et al.  Clinical, socio‐demographic and psychological characteristics in individuals with persistent psychotic experiences with and without a “need for care” , 2016, World psychiatry : official journal of the World Psychiatric Association.

[38]  Matthew H. Davis,et al.  Hearing speech sounds: Top-down influences on the interface between audition and speech perception , 2007, Hearing Research.

[39]  R. Murray,et al.  Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. , 2000, Archives of general psychiatry.

[40]  Willem M Otte,et al.  Network analysis of auditory hallucinations in nonpsychotic individuals , 2014, Human brain mapping.

[41]  Josef J. Bless,et al.  The role of the primary auditory cortex in the neural mechanism of auditory verbal hallucinations , 2013, Front. Hum. Neurosci..

[42]  Brent A. Vogt,et al.  Midcingulate cortex: Structure, connections, homologies, functions and diseases , 2016, Journal of Chemical Neuroanatomy.

[43]  Karl J. Friston,et al.  The Computational Anatomy of Psychosis , 2013, Front. Psychiatry.

[44]  R. Bentall,et al.  Externalizing biases and hallucinations in source-monitoring, self-monitoring and signal detection studies: a meta-analytic review , 2013, Psychological Medicine.

[45]  S. Eickhoff,et al.  Sustaining attention to simple tasks: a meta-analytic review of the neural mechanisms of vigilant attention. , 2013, Psychological bulletin.

[46]  V. van de Ven,et al.  The brain's voices: comparing nonclinical auditory hallucinations and imagery. , 2011, Cerebral cortex.

[47]  Philip R Corlett,et al.  Hallucinations as top-down effects on perception. , 2016, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[48]  César F. Lima,et al.  Roles of Supplementary Motor Areas in Auditory Processing and Auditory Imagery , 2016, Trends in Neurosciences.

[49]  Karl J. Friston Hallucinations and perceptual inference , 2005, Behavioral and Brain Sciences.

[50]  J. Obleser,et al.  Expectancy constraints in degraded speech modulate the language comprehension network. , 2010, Cerebral cortex.

[51]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[52]  R. Bowtell,et al.  “sparse” temporal sampling in auditory fMRI , 1999, Human brain mapping.

[53]  Sophie K. Scott,et al.  An Application of Univariate and Multivariate Approaches in fMRI to Quantifying the Hemispheric Lateralization of Acoustic and Linguistic Processes , 2012, Journal of Cognitive Neuroscience.

[54]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[55]  James G. Scott,et al.  Auditory Verbal Hallucinations in Persons With and Without a Need for Care , 2014, Schizophrenia bulletin.

[56]  N. Tarrier,et al.  Scales to measure dimensions of hallucinations and delusions: the psychotic symptom rating scales (PSYRATS) , 1999, Psychological Medicine.

[57]  R. Bentall,et al.  Reliability of a scale measuring disposition towards hallucination: A brief report. , 1985 .

[58]  Matthew H. Davis,et al.  Temporal Predictive Codes for Spoken Words in Auditory Cortex , 2012, Current Biology.

[59]  J. Read,et al.  The prevalence of voice-hearers in the general population: A literature review , 2011, Journal of mental health.

[60]  Albert R. Powers,et al.  Varieties of Voice-Hearing: Psychics and the Psychosis Continuum , 2017, Schizophrenia bulletin.

[61]  ChrisD . Frith,et al.  Perceiving is believing: a Bayesian approach to explaining the positive symptoms of schizophrenia , 2009, Nature Reviews Neuroscience.

[62]  D. N. Carss,et al.  Meeting report , 1975, Appetite.

[63]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[64]  R. Kahn,et al.  The same or different? A phenomenological comparison of auditory verbal hallucinations in healthy and psychotic individuals. , 2011, The Journal of clinical psychiatry.

[65]  Willy Serniclaes,et al.  Neural correlates of switching from auditory to speech perception , 2005, NeuroImage.

[66]  Sophie K. Scott,et al.  Hemispheric Asymmetries in Speech Perception: Sense, Nonsense and Modulations , 2011, PloS one.

[67]  D. Sharp,et al.  The role of the posterior cingulate cortex in cognition and disease. , 2014, Brain : a journal of neurology.

[68]  R V Shannon,et al.  Speech Recognition with Primarily Temporal Cues , 1995, Science.

[69]  F. Waters,et al.  The Changing Face of Hallucination Research: The International Consortium on Hallucination Research (ICHR) 2015 Meeting Report. , 2016, Schizophrenia bulletin.

[70]  Joseph M. Orr,et al.  Anterior cingulate cortex makes 2 contributions to minimizing distraction. , 2009, Cerebral cortex.

[71]  Matthew H. Davis,et al.  Predictive Top-Down Integration of Prior Knowledge during Speech Perception , 2012, The Journal of Neuroscience.

[72]  Christoph Teufel,et al.  Shift toward prior knowledge confers a perceptual advantage in early psychosis and psychosis-prone healthy individuals , 2015, Proceedings of the National Academy of Sciences.

[73]  Renaud Jardri,et al.  Computational Models of Hallucinations , 2013 .

[74]  A. Aleman,et al.  Hearing a voice in the noise: auditory hallucinations and speech perception , 2007, Psychological Medicine.

[75]  Hillary C. M. Nelson The National Adult Reading Test , 1982 .

[76]  J. Nazroo,et al.  Occurrence of hallucinations in a community sample , 1998, Schizophrenia Research.

[77]  E. Peters,et al.  Auditory verbal hallucinations and continuum models of psychosis: A systematic review of the healthy voice-hearer literature , 2017, Clinical psychology review.

[78]  D. Pisoni,et al.  Speech perception without traditional speech cues. , 1981, Science.

[79]  A. Clark Whatever next? Predictive brains, situated agents, and the future of cognitive science. , 2013, The Behavioral and brain sciences.

[80]  D. Sharp,et al.  Fractionating the Default Mode Network: Distinct Contributions of the Ventral and Dorsal Posterior Cingulate Cortex to Cognitive Control , 2011, The Journal of Neuroscience.

[81]  Paul Allen,et al.  Inner speech models of auditory verbal hallucinations: Evidence from behavioural and neuroimaging studies , 2007, International review of psychiatry.

[82]  S. McCarthy-Jones,et al.  Emerging Perspectives From the Hearing Voices Movement: Implications for Research and Practice , 2014, Schizophrenia bulletin.

[83]  L. Krabbendam,et al.  FUNCTIONAL MAGNETIC RESONANCE IMAGING OF INNER SPEECH IN SCHIZOPHRENIA , 2010, Schizophrenia Research.

[84]  Daniel M. Corcos,et al.  Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: A meta-analysis , 2006, NeuroImage.

[85]  D. Pins,et al.  The neurodynamic organization of modality-dependent hallucinations. , 2013, Cerebral cortex.

[86]  I D Wilkinson,et al.  Neural activity in speech-sensitive auditory cortex during silence. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[87]  Mikko Sams,et al.  Perceiving identical sounds as speech or non-speech modulates activity in the left posterior superior temporal sulcus , 2006, NeuroImage.

[88]  K. Diederen,et al.  Auditory hallucinations elicit similar brain activation in psychotic and nonpsychotic individuals. , 2012, Schizophrenia bulletin.

[89]  A. Aleman,et al.  Semantic Expectations Can Induce False Perceptions in Hallucination-Prone Individuals , 2008, Schizophrenia bulletin.

[90]  J. Cutting,et al.  Hearing voices. , 1989, BMJ.

[91]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[92]  A. Cavanna,et al.  Functional Connectivity of the Posteromedial Cortex , 2010, PloS one.

[93]  Thomas E. Nichols,et al.  Scanning the horizon: towards transparent and reproducible neuroimaging research , 2016, Nature Reviews Neuroscience.

[94]  C. M. Mooney Age in the development of closure ability in children. , 1957, Canadian journal of psychology.

[95]  C L Ludlow,et al.  Functional neuroanatomy of human vocalization: an H215O PET study. , 2005, Cerebral cortex.

[96]  Matthew H. Davis,et al.  Hierarchical Processing in Spoken Language Comprehension , 2003, The Journal of Neuroscience.