Cortical Activations During Auditory Verbal Hallucinations in Schizophrenia: A Coordinate-Based Meta-Analysis
Abstract
OBJECTIVE: Auditory verbal hallucinations (AVHs) constitute severe, incapacitating symptoms of schizophrenia. Despite increasing interest in the functional exploration of AVHs, the available findings remain difficult to integrate because of their considerable variability. The authors' aim was to perform a robust quantitative review of existing functional data in order to elucidate consistent patterns observed during the emergence of AVHs and to orient new pathophysiological models of hallucinations. METHOD: Ten positron emission tomography or functional magnetic resonance imaging studies were selected for the meta-analysis after systematic review. A total of 68 patients with schizophrenia spectrum disorders experiencing AVHs during scanning were included. According to a random-effects activation likelihood estimation algorithm, stereotaxic coordinates of 129 foci, reported as significant in the source studies, were extracted and computed to estimate the brain locations most consistently associated with AVHs across studies (cluster-extent threshold: 200 mm³). RESULTS: Patients experiencing AVHs demonstrated significantly increased activation likelihoods in a bilateral neural network, including the Broca's area (activation likelihood estimation=1.84×10⁻³), anterior insula (1.78×10⁻³), precentral gyrus (1.46×10⁻³), frontal operculum (1.29×10⁻³), middle and superior temporal gyri (1.59×10⁻³), inferior parietal lobule (1.33×10⁻³), and hippocampus/parahippocampal region (1.90×10⁻³). CONCLUSIONS: This meta-analysis demonstrated that experiencing AVHs is associated with increased activity in fronto-temporal areas involved in speech generation and speech perception, but also within the medial temporal lobe, a structure notably involved in verbal memory. Such findings support a model for AVHs in which aberrant cortical activations emerge within a distributed network involved at different levels of complexity in the brain architecture. Critical future directions are considered.
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Our present study shows commonalities between many of the neural regions activated during AVH (such as left STG, left insula, left IFG) and those strongly activated during dialogic inner speech.
“Our present study extends this by showing commonalities between many of the neural regions activated during AVH (such as left STG, left insula, left IFG) and those strongly activated during dialogic inner speech (Jardri et al., 2011; Kühn and Gallinat, 2012).”
From The brain's conversation with itself: neural substrates of dialogic inner speech (2016) · cites this paper as Jardri et al., 2011
Meta-analyses of symptom-capture studies have only partially overlapping conclusions.
“Recent meta-analyses of symptom-capture studies have come to only partially overlapping conclusions: while Jardri et al. (2011) found AVHs to be associated with activation in left IFG, anterior insula, superior temporal, and hippocampal areas, Kühn and Gallinat (2012) could only find consistent results for bilateral IFG, postcentral gyrus, and parietal areas.”
From Inner Speech: Development, Cognitive Functions, Phenomenology, and Neurobiology (2015) · cites this paper as Jardri et al. (2011)
Increased activation within a bilateral frontotemporal network is confirmed by meta-analysis of the auditory hallucination state.
“Increased activation within a bilateral frontotemporal network was confirmed by coordinate-based metaanalysis of the auditory hallucination (AH) state.27”
From Are hallucinations due to an imbalance between excitatory and inhibitory influences on the brain? (2016) · cites this paper as [27]
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Stephane, M., Hagen, M. C., Lee, J. T., Uecker, J., Pardo, P. J., Kuskowski, M. A., & Pardo, J. V. (2006) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0644 · Cited by 34 · see citing works
A Case of fMRI-Guided rTMS Treatment of Coenesthetic Hallucinations
Jardri, R., Pins, D., & Thomas, P. M. (2008) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2008.08040504 · Cited by 33 · see citing works
Self-citationParellada, E., Lomeña, F., Font, M., Pareto, D., Gutiérrez, F., Simó, M., Fernández-Egea, E., Pavı́a, J., Ros, D., & Bernardo, M. (2008) · Nuclear Medicine Communications · doi:10.1097/mnm.0b013e328302cd10 · Cited by 32 · see citing works
Differences in regional cerebral blood flow during musical and verbal hallucinations
Izumi, Y., Terao, T., Ishino, Y., & Nakamura, J. (2002) · Psychiatry Research Neuroimaging · doi:10.1016/s0925-4927(02)00083-5 · Cited by 30 · see citing works
Sommer, I. E., & Diederen, K. M. (2009) · Brain · doi:10.1093/brain/awp040 · Cited by 30 · see citing works
Regional cerebral blood flow change in a case of Alzheimer's disease with musical hallucinations
Mori, T., Ikeda, M., Fukuhara, R., Sugawara, Y., Nakata, S., Matsumoto, N., Nestor, P. J., & Tanabe, H. (2005) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-005-0631-5 · Cited by 27 · see citing works
Fu, C. H. Y., Brammer, M. J., Yágüez, L., Allen, P., Matsumoto, K., Johns, L., Weinstein, S., Borgwardt, S., Broome, M. R., McGuire, P. K., et al. (2007) · Schizophrenia Research · doi:10.1016/j.schres.2007.10.023 · Cited by 27 · see citing works
Cortical response to exogenous visual stimulation during visual hallucinations
Howard, R. J., Williams, S., Bullmore, E. T., Brammer, M. J., Mellers, J. D. C., Woodruff, P. W. R., & David, A. S. (1995) · The Lancet · doi:10.1016/s0140-6736(95)91198-7 · Cited by 25 · see citing works
Neural Correlates of Successful Declarative Memory Formation and Retrieval: The Anatomical Overlap
WEIS, S., Klaver, P., REUL, J., Elger, C. E., & Fernández, G. (2004) · Cortex · doi:10.1016/s0010-9452(08)70950-x · Cited by 19 · see citing works
The physiological basis of visual hallucinations after damage to the primary visual cortex
de Haan, E. H. F., Nys, G. M. S., van Zandvoort, M. J. E., & Ramsey, N. F. (2007) · Neuroreport · doi:10.1097/wnr.0b013e32820049d3 · Cited by 18 · see citing works
Holroyd, S., & Wooten, G. F. (2006) · Journal of Neuropsychiatry · doi:10.1176/appi.neuropsych.18.3.402 · Cited by 16 · see citing works
18FDG PET in hallucinating and non-hallucinating patients.
Kopeček, M., Španiel, F., Novák, T., Tislerova, B., Bělohlávek, O., & Horáček, J. (2007) · PubMed · Cited by 15 · see citing works
Thalamic Hyperperfusion in Verbal Hallucination of Parkinsonian Patients
Matsui, H., Nishinaka, K., Miyoshi, T., Hara, N., Oda, M., Kubori, T., & Udaka, F. (2007) · Internal Medicine · doi:10.2169/internalmedicine.46.0191 · Cited by 13 · see citing works
(2005) · Clinical EEG and Neuroscience · doi:10.1177/155005940503600111 · Cited by 1 · see citing works
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Large-scale brain networks and psychopathology: a unifying triple network model
Menon, V. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.08.003 · Cited by 4,168 · see citing works
Inner Speech: Development, Cognitive Functions, Phenomenology, and Neurobiology
Alderson-Day, B., & Fernyhough, C. (2015) · Psychological Bulletin · doi:10.1037/bul0000021 · Cited by 808 · see citing works
“Recent meta-analyses of symptomcapture studies have come to only partially overlapping conclusions: while Jardri et al. (2011) found AVHs to be associated with activation in left IFG, anterior insula, superior temporal, and hippocampal areas, Kühn and Gallinat (2012) could only find consistent…”
ResultFregni, F., El-Hagrassy, M. M., Pacheco‐Barrios, K., Carvalho, S., Leite, J., Simis, M., Brunelin, J., Nakamura-Palacios, E. M., Marangolo, P., Venkatasubramanian, G., et al. (2020) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyaa051 · Cited by 617 · see citing works
Hallucinations and strong priors
Corlett, P. R., Horga, G., Fletcher, P. C., Alderson-Day, B., Schmack, K., & Powers, A. R. (2019) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.12.001 · Cited by 534 · see citing works
“Critically, the neural circuit underlying these conditioned phenomena, including superior temporal gyrus and insula, largely overlapped with the circuit engaged when patients report hearing voices in the scanner [34,35].”
Brunelin, J., Mondino, M., Gassab, L., Haesebaert, F., Gaha, L., Suaud-Chagny, M.-F., Saoud, M., Mechri, A., & Poulet, E. (2012) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2012.11071091 · Cited by 520 · see citing works
Palaniyappan, L., & Liddle, P. F. (2012) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.100176 · Cited by 548 · see citing works
Waters, F., Allen, P., Aleman, A., Fernyhough, C., Woodward, T. S., Badcock, J. C., Barkus, E., Johns, L., Varese, F., Menon, M., et al. (2012) · Schizophrenia Bulletin · doi:10.1093/schbul/sbs045 · Cited by 423 · see citing works
“deficits in AH.(22) While cognitive evidence for attention and working memory updating remains inconclusive, the role of attention is clearly relevant in early auditory sensory detection mechanisms.”
BackgroundNeuroanatomical Maps of Psychosis Onset: Voxel-wise Meta-Analysis of Antipsychotic-Naive VBM Studies
Fusar‐Poli, P., Raduà, J., McGuire, P. K., & Borgwardt, S. (2011) · Schizophrenia Bulletin · doi:10.1093/schbul/sbr134 · Cited by 291 · see citing works
McCarthy‐Jones, S., Trauer, T., Mackinnon, A. J., Sims, E., Thomas, N., & Copolov, D. (2012) · Schizophrenia Bulletin · doi:10.1093/schbul/sbs156 · Cited by 282 · see citing works
Kompus, K., Westerhausen, R., & Hugdahl, K. (2011) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2011.08.010 · Cited by 274 · see citing works
Allen, P., Modinos, G., Hubl, D., Shields, G., Cachia, A., Jardri, R., Thomas, P., Woodward, T., Shotbolt, P., Plaze, M., et al. (2012) · Schizophrenia Bulletin · doi:10.1093/schbul/sbs066 · Cited by 240 · see citing works
“In addition to changes in these speech and language areas, changes to a range of other cortical and subcortical regions are widely reported; these findings are detailed in previous reviews.(1,2) In the current review, we largely focus on more recent studies and include neurochemical and gyrification studies for the fi…”
BackgroundResultInfluentialSelf-citationde Leede-Smith, S., & Barkus, E. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00367 · Cited by 222 · see citing works
“In a recent meta-analysis Jardri et al. (2011) noted several brain networks to be activated (fMRI, PET) during AVH, including fronto-temporal brain regions, and hippocampal/parrahippocampal regions.”
BackgroundModinos, G., Costafreda, S. G., van Tol, M., McGuire, P. K., Aleman, A., & Allen, P. (2012) · Cortex · doi:10.1016/j.cortex.2012.01.009 · Cited by 230 · see citing works
“A more recent meta-analysis based on functional imaging studies of patients who were experiencing AVHs during scanning highlighted aberrant activations in frontal, temporal and hippocampal regions (Jardri et al., 2011).”
The neural mechanisms of hallucinations: A quantitative meta-analysis of neuroimaging studies
Zmigrod, L., Garrison, J. R., Carr, J., & Simons, J. S. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.037 · Cited by 226 · see citing works
Interaction of language, auditory and memory brain networks in auditory verbal hallucinations
Ćurčić-Blake, B., Ford, J. M., Hubl, D., Orlov, N. D., Sommer, I. E., Waters, F., Allen, P., Jardri, R., Woodruff, P. W., David, O., et al. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2016.11.002 · Cited by 224 · see citing works
“One possible consequence is a predisposition to the over-activation of language regions in the absence of correct input (Jardri et al., 2011).”
BackgroundInfluentialSelf-citationSkipper, J. I., Devlin, J. T., & Lametti, D. R. (2016) · Brain and Language · doi:10.1016/j.bandl.2016.10.004 · Cited by 220 · see citing works
Qin, P., Wang, M., & Northoff, G. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.05.004 · Cited by 220 · see citing works
Mondino, M., Jardri, R., Suaud‐Chagny, M., Saoud, M., Poulet, E., & Brunelin, J. (2015) · Schizophrenia Bulletin · doi:10.1093/schbul/sbv114 · Cited by 217 · see citing works
“areas (middle and superior temporal gyri and Wernicke’s area), left inferior frontal areas (Broca’s area, frontal operculum, anterior insula, precentral gyrus), as well as in their right homologues.(1) These findings suggested aberrant activations within speech perception and production brain areas during the occurren…”
BackgroundSelf-citationSystematic Meta-Analysis of Insula Volume in Schizophrenia
Shepherd, A. M., Matheson, S. L., Laurens, K. R., Carr, V. J., & Green, M. J. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.04.020 · Cited by 207 · see citing works
“Clinically, dysfunctional insular cortex can plausibly account for several characteristic signs of schizophrenia and other psychoses: aberrant structure or function of the insula is associated with psychotic symptoms (3,4), deficits in social cognition and emotion regulation (5), facial and prosodic affect perception…”
The Challenges and Promise of Neuroimaging in Psychiatry
Linden, D. E. J. (2012) · Neuron · doi:10.1016/j.neuron.2011.12.014 · Cited by 204 · see citing works
Canuet, L., Ishii, R., Pascual-Marqui, R. D., Iwase, M., Kurimoto, R., Aoki, Y., Ikeda, S., Takahashi, H., Nakahachi, T., & Takeda, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027863 · Cited by 198 · see citing works
Deficits in predictive coding underlie hallucinations in schizophrenia
Horga, G., Schatz, K. C., Abi-Dargham, A., & Peterson, B. S. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0200-14.2014 · Cited by 176 · see citing works
“These studies have identified increased activity during AVHs in the auditory cortex and other brain regions involved in speech perception (Sommer et al., 2008; Hoffman et al., 2011; Jardri et al., 2011).”
BackgroundThe Neurodynamic Organization of Modality-Dependent Hallucinations
Jardri, R., Thomas, P., Delmaire, C., Delion, P., & Pins, D. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs082 · Cited by 177 · see citing works
“tional disturbances in sensory cortices have been proposed to be centrally involved in their pathogenesis (Allen et al. 2008; Jardri et al. 2011).”
BackgroundResultSelf-citationAcevedo, B. P., Aron, E. N., Pospos, S., & Jessen, D. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2017.0161 · Cited by 181 · see citing works
Alderson-Day, B., McCarthy-Jones, S., & Fernyhough, C. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.04.016 · Cited by 165 · see citing works
Are hallucinations due to an imbalance between excitatory and inhibitory influences on the brain?
Jardri, R., Hugdahl, K., Hughes, M., Brunelin, J., Waters, F., Alderson-Day, B., Smailes, D., Sterzer, P., Corlett, P. R., Leptourgos, P., et al. (2016) · Schizophrenia Bulletin · doi:10.1093/schbul/sbw075 · Cited by 157 · see citing works
Self-citationStructural correlates of auditory hallucinations in schizophrenia: a meta-analysis.
Palaniyappan, L., Balain, V., Radua, J., & Liddle, P. (2012) · Schizophrenia Research · doi:10.1016/j.schres.2012.01.038 · Cited by 156 · see citing works
Childhood trauma and auditory verbal hallucinations
Daalman, K., Diederen, K. M. J., Derks, E. M., van Lutterveld, R., Kahn, R. S., & Sommer, I. E. C. (2012) · Psychological Medicine · doi:10.1017/s0033291712000761 · Cited by 153 · see citing works
“…: pronounced deactivation in the left parahippocampal gyrus has been found to precede AVH in patients with a psychotic disorder (Hoffman et al. 2008 ; Diederen et al. 2010b), and activity in this structure and the hippocampus has also been related to the presence of AVH itself (Jardri et al. 2011).”
Transcranial direct current stimulation in psychiatric disorders
Tortella, G. (2015) · World Journal of Psychiatry · doi:10.5498/wjp.v5.i1.88 · Cited by 154 · see citing works
Zhao, C., Zhu, J., Liu, X., Pu, C., Lai, Y., Chen, L., Yu, X., & Hong, N. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.12.017 · Cited by 153 · see citing works
“Increased hippocampal ALFF and activation in schizophrenia are associated with cognitive and emotional dysfunction, especially hallucinations (Jardri et al., 2011; Turner et al., 2013).”
BackgroundUnderstanding auditory verbal hallucinations: a systematic review of current evidence
Upthegrove, R., Broome, M. R., Caldwell, K., Ives, J., Oyebode, F., & Wood, S. J. (2015) · Acta Psychiatrica Scandinavica · doi:10.1111/acps.12531 · Cited by 150 · see citing works
“Hippocampal hyperactivation is apparent during hallucinations, supporting this model of AVHs as traumatic intrusions (88).”
Resting-state thalamic dysconnectivity in schizophrenia and relationships with symptoms
Ferri, J. M., Ford, J. M., Roach, B. J., Turner, J. A., van Erp, T. G., Voyvodic, J. T., Preda, A., Belger, A., Bustillo, J., OʼLeary, D. S., et al. (2018) · Psychological Medicine · doi:10.1017/s003329171800003x · Cited by 147 · see citing works
“Importantly, abnormal activation, structure, and connectivity with regions of the brain associated with language and memory, including middle and superior temporal gyrus, have been proposed to underlie some positive symptoms of SZ, including hallucinations (Allen et al. 2008; Jardri et al. 2011).”
Multisensory Integration as a Window into Orderly and Disrupted Cognition and Communication
Wallace, M. T., Woynaroski, T. G., & Stevenson, R. A. (2019) · Annual Review of Psychology · doi:10.1146/annurev-psych-010419-051112 · Cited by 155 · see citing works
“…of the sensory features of SZ, with neuroimaging evidence showing that such hallucinations are frequently accompanied by activity changes in the areas of the brain linked to the perception of speech, including areas of the superior temporal and inferior frontal cortices ( Jardri et al. 2011).”
BackgroundBridging disparate symptoms of schizophrenia: a triple network dysfunction theory
Nekovářová, T., Fajnerová, I., Horáček, J., & Španiel, F. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00171 · Cited by 145 · see citing works
“Along a somewhat different line, both structural and functional changes within the SN key node, the insular region, correlate with the occurrence of AVH in schizophrenia (Jardri et al., 2011; Palaniyappan et al., 2012a) and positive symptoms in general (Moran et al., 2014).”
The associations between multisensory temporal processing and symptoms of schizophrenia
Stevenson, R. A., Park, S., Cochran, C., McIntosh, L. G., Noel, J., Barense, M. D., Ferber, S., & Wallace, M. T. (2016) · Schizophrenia Research · doi:10.1016/j.schres.2016.09.035 · Cited by 145 · see citing works
“Direct stimulation of STS induces auditory hallucinations (Postmes et al., 2014), and during hallucinations in individuals with SCZ, there are changes in the neural activation patterns in STS (Jardri et al., 2011; Shergill et al., 2000).”
InfluentialAuditory hallucinations elicit similar brain activation in psychotic and nonpsychotic individuals
Diederen, K. M. J., Daalman, K., de Weijer, A. D., Neggers, S. F. W., van Gastel, W., Blom, J. D., Kahn, R. S., & Sommer, I. E. C. (2012) · Schizophrenia Bulletin · doi:10.1093/schbul/sbr033 · Cited by 138 · see citing works
Hurlburt, R. T., Alderson-Day, B., Kühn, S., & Fernyhough, C. (2016) · PLOS ONE · doi:10.1371/journal.pone.0147932 · Cited by 131 · see citing works
“For example, auditory verbal hallucinations (AVH) have been hypothesized to result from a misattribution of inner speech to an external source [50, 51], a theory that is based largely on the fact that left IFG is activated both in neuroimaging studies of AVH (see meta-analyses in [52, 53]) and in neuroimaging studies…”
BackgroundIncreased Resting-State Gamma-Band Connectivity in First-Episode Schizophrenia
Andreou, C., Nolte, G., Leicht, G., Polomac, N., Hanganu-Opatz, I. L., Lambert, M., Engel, A. K., & Mulert, C. (2015) · Schizophrenia Bulletin · doi:10.1093/schbul/sbu121 · Cited by 129 · see citing works
The multimodal connectivity of the hippocampal complex in auditory and visual hallucinations
Amad, A., Cachia, A., Gorwood, P. A. P. M., Pins, D., Delmaire, C., Rolland, B., Mondino, M., Thomas, P., & Jardri, R. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.181 · Cited by 137 · see citing works
Self-citationPractical recommendations to conduct a neuroimaging meta-analysis for neuropsychiatric disorders
Tahmasian, M., Sepehry, A. A., Samea, F., Khodadadifar, T., Soltaninejad, Z., Javaheripour, N., Khazaie, H., Zarei, M., Eickhoff, S. B., & Eickhoff, C. R. (2019) · Human Brain Mapping · doi:10.1002/hbm.24746 · Cited by 126 · see citing works
Network Localization of State and Trait of Auditory Verbal Hallucinations in Schizophrenia
Mo, F., Zhao, H., Li, Y., Cai, H., Song, Y., Wang, R., Yu, Y., & Zhu, J. (2024) · Schizophrenia Bulletin · doi:10.1093/schbul/sbae020 · Cited by 135 · see citing works
Gao, X., Zhang, W., Li, Y., Xiao, Y., Liu, L., Liu, J., Li, S., Bo, T., Shah, C., Gong, Q., et al. (2018) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.160219 · Cited by 132 · see citing works
Childhood-Onset Schizophrenia and Early-onset Schizophrenia Spectrum Disorders
Driver, D. I., Thomas, S., Gogtay, N., & Rapoport, J. L. (2019) · Child and Adolescent Psychiatric Clinics of North America · doi:10.1016/j.chc.2019.08.017 · Cited by 132 · see citing works
Cui, L., Liu, K., Li, C., Wang, L., Guo, F., Tian, P., Wu, Y.-J., Guo, L., Liu, W.-M., Xi, Y., et al. (2016) · Schizophrenia Research · doi:10.1016/j.schres.2016.02.039 · Cited by 131 · see citing works
“, 2012) and altered brain activation (Hugdahl, 2015; Jardri et al., 2011; van den Heuvel and Fornito, 2014).”
BackgroundAlderson‐Day, B., Diederen, K. M. J., Fernyhough, C., Ford, J. M., Horga, G., Margulies, D. S., McCarthy‐Jones, S., Northoff, G., Shine, J. M., Turner, J. A., et al. (2016) · Schizophrenia Bulletin · doi:10.1093/schbul/sbw078 · Cited by 129 · see citing works
Self-citationKarcher, N. R., O’Brien, K. J., Kandala, S., & Barch, D. M. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.01.013 · Cited by 131 · see citing works
“Hypoconnectivity of the CON was more strongly associated with perceptual distortions, consistent with evidence that the CON, and specifically the insula, is activated during hallucinations (89).”
ResultLanius, R. A. (2015) · European Journal of Psychotraumatology · doi:10.3402/ejpt.v6.27905 · Cited by 127 · see citing works
Shinn, A. K., Baker, J. T., Cohen, B. M., & Öngür, D. (2012) · Schizophrenia Research · doi:10.1016/j.schres.2012.11.037 · Cited by 128 · see citing works
“AH in SZ (Jardri et al., 2010).”
BackgroundInfluentialDysconnectivity of Large-Scale Functional Networks in Early Psychosis: A Meta-analysis
O’Neill, A., Mechelli, A., & Bhattacharyya, S. (2018) · Schizophrenia Bulletin · doi:10.1093/schbul/sby094 · Cited by 127 · see citing works
Alonso-Solís, A., Vives‐Gilabert, Y., Grasa, E., Portella, M. J., Rabella, M., Sauras-Quetcuti, R. B., Roldán, A., Núñez-Marín, F., Gómez‐Ansón, B., Pérez, V., et al. (2014) · Schizophrenia Research · doi:10.1016/j.schres.2014.10.047 · Cited by 124 · see citing works
“Consistent to these findings, a meta-analysis of the existing functional data during AVH in patients with schizophrenia reported prominent involvement of the anterior insula, precentral gyrus, frontal opercular cortex, hippocampus and auditory cortex (Jardri et al., 2011).”
ResultKraguljac, N. V., White, D. M., Hadley, N. T., Hadley, J. A., Hoef, L. V., Davis, E., & Lahti, A. C. (2016) · Schizophrenia Bulletin · doi:10.1093/schbul/sbv228 · Cited by 123 · see citing works
McCarthy‐Jones, S., Thomas, N., Strauss, C., Dodgson, G., Jones, N., Woods, A., Brewin, C. R., Hayward, M., Stephane, M., Barton, J. C., et al. (2014) · Schizophrenia Bulletin · doi:10.1093/schbul/sbu018 · Cited by 120 · see citing works
Padmanabhan, J. L., Tandon, N., Haller, C. S., Mathew, I. T., Eack, S. M., Clementz, B. A., Pearlson, G. D., Sweeney, J. A., Tamminga, C. A., & Keshavan, M. S. (2014) · Schizophrenia Bulletin · doi:10.1093/schbul/sbu075 · Cited by 120 · see citing works
What is the link between hallucinations, dreams, and hypnagogic–hypnopompic experiences?
Waters, F., Blom, J. D., Dang-Vu, T. T., Cheyne, A. J., Alderson-Day, B., Woodruff, P., & Collerton, D. (2016) · Schizophrenia Bulletin · doi:10.1093/schbul/sbw076 · Cited by 119 · see citing works
Knöchel, C., Oertel‐Knöchel, V., Schönmeyer, R., Rotarska-Jagiela, A., van de Ven, V. G., Prvulovic, D., Haenschel, C., Uhlhaas, P. J., Pantel, J., Hampel, H. J., et al. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.07.088 · Cited by 116 · see citing works
“Changes in frontal cortex have also been implicated in the generation of hallucinations (e.g., Allen et al., 2008; Jardri et al., 2011), for example through deficits in source monitoring and cognitive control, which might explain a contribution of impaired integrity of the genu, which carries frontal fibers, to halluc…”
BackgroundLesions causing hallucinations localize to one common brain network
Kim, N. Y., Hsu, J., Talmasov, D., Joutsa, J., Soussand, L., Wu, O., Rost, N. S., Morenas‐Rodríguez, E., Martí‐Fábregas, J., Pascual‐Leone, Á., et al. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0565-3 · Cited by 117 · see citing works
Mondino, M., Bennabi, D., Poulet, E., Galvão, F., Brunelin, J., & Haffen, É. (2014) · The World Journal of Biological Psychiatry · doi:10.3109/15622975.2013.876514 · Cited by 114 · see citing works
“In these studies, cathodal-tDCS was applied over the left temporoparietal junction (TPJ) according to neuroimaging studies incriminating a hyperactivation of the left TPJ during hallucinations (Jardri et al. 2011).”
MethodMoseley, P., Fernyhough, C., & Ellison, A. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.10.001 · Cited by 113 · see citing works
An integrative framework for perceptual disturbances in psychosis
Horga, G., & Abi-Dargham, A. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0234-1 · Cited by 103 · see citing works
Distinct processing of ambiguous speech in people with non-clinical auditory verbal hallucinations
Alderson-Day, B., Lima, C. F., Evans, S., Krishnan, S., Shanmugalingam, P., Fernyhough, C., & Scott, S. K. (2017) · Brain · doi:10.1093/brain/awx206 · Cited by 108 · see citing works
“…in a number of early symptomcapture studies of people hearing voices while being scanned (Shergill et al., 2000), although later meta-analyses have failed to consistently identify this region during the hallucinatory state (Jardri et al., 2011; Kühn and Gallinat, 2012; Zmigrod et al., 2016).”
BackgroundWalton, E., Hibar, D., van Erp, T. V., Potkin, S., Roiz-Santiañez, R., Crespo-Facorro, B., Suárez-Pinilla, P., van Haren, N. V., de Zwarte, S. D., Kahn, R. S., et al. (2017) · Acta Psychiatrica Scandinavica · doi:10.1111/acps.12718 · Cited by 108 · see citing works
“Based on (i) well-replicated structural deficits in the STG in patients with schizophrenia, and (ii) a link between functional and volumetric measures in the STG and positive symptom dimensions (9, 19, 22, 28) we followed a region-of-interest (ROI) approach, focusing on cortical thickness in the STG.”
Not on speaking terms: hallucinations and structural network disconnectivity in schizophrenia
Ćurĉić‐Blake, B., Nanetti, L., van der Meer, L., Cerliani, L., Renken, R. J., Pijnenborg, G. H. M., & Aleman, A. (2013) · Brain Structure and Function · doi:10.1007/s00429-013-0663-y · Cited by 104 · see citing works
Resting State Functional Connectivity in Patients with Chronic Hallucinations
Sommer, I. E., Clos, M., Meijering, A. L., Diederen, K. M. J., & Eickhoff, S. B. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043516 · Cited by 103 · see citing works
Orlov, N., Giampietro, V., O'Daly, O., Lam, S.-L., Barker, G., Rubia, K., McGuire, P., Shergill, S., & Allen, P. (2018) · Translational Psychiatry · doi:10.1038/s41398-017-0067-5 · Cited by 82 · see citing works
Lefebvre, S., Demeulemeester, M., Leroy, A., Delmaire, C., Lopes, R., Pins, D., Thomas, P., & Jardri, R. (2016) · Human Brain Mapping · doi:10.1002/hbm.23197 · Cited by 99 · see citing works
“A majority of these areas are known to be involved in auditory hallucinations [Diederen et al., 2010; Jardri et al., 2011], while additional areas such as the cingulate cortex, the parietal cortex and the dorsolateral prefrontal cortex (DLPFC) were also observed to be active during this period.”
BackgroundMethodInfluentialSelf-citationRolland, B., Amad, A., Poulet, E., Bordet, R., Vignaud, A., Bation, R., Delmaire, C., Thomas, P., Cottencin, O., & Jardri, R. (2015) · Schizophrenia bulletin · doi:10.1093/schbul/sbu097 · Cited by 98 · see citing works
“Conversely, reduced connectivity strength was evidenced by the NAcc seeds in schizophrenia patients at the level of the (4) dorsal anterior cingulate cortex, (5) associative striatum, and (6) left anterior insula.”
BackgroundSelf-citationHow do auditory verbal hallucinations in patients differ from those in non-patients?
Larøi, F. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00025 · Cited by 98 · see citing works
“Recently, Jardri et al. (2011) performed a meta-analysis of studies ( n = 10) examining cortical activation (fMRI, PET) during AVHs and found that they were associated with increased activity in fronto-temporal (especially those involved in speech generation and perception) and medial temporal…”
The brain's conversation with itself: neural substrates of dialogic inner speech
Alderson-Day, B., Weis, S., McCarthy-Jones, S., Moseley, P., Smailes, D., & Fernyhough, C. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsv094 · Cited by 94 · see citing works
“insula, left IFG) and those strongly activated during dialogic inner speech (Jardri et al., 2011; Kühn and Gallinat, 2012).”
Functional neuroimaging as a catalyst for integrated neuroscience
Finn, E. S., Poldrack, R. A., & Shine, J. M. (2023) · Nature · doi:10.1038/s41586-023-06670-9 · Cited by 95 · see citing works
“Older neuro-imaging studies were concerned with identifying loci of activity associated with hallucinations 125 to understand the extent to which hallucinations resemble true sensory experiences in their functional neuroanatomy, whereas more recent fMRI studies are leveraging methodological…”
BackgroundFusar‐Poli, P., Smieskova, R., Serafini, G., Politi, P., & Borgwardt, S. (2012) · The World Journal of Biological Psychiatry · doi:10.3109/15622975.2011.630408 · Cited by 94 · see citing works
de Weijer, A. D., Mandl, R. C. W., Diederen, K. M. J., Neggers, S. F. W., Kahn, R. S., Pol, H. E. H., & Sommer, I. E. (2011) · Schizophrenia Research · doi:10.1016/j.schres.2011.05.010 · Cited by 95 · see citing works
“Several brain areas consistently showed activation during AVH (Jardri et al., 2010), such as the right and left temporo-parietal cortices and Broca's area and its right-sided homologue (Shergill et al.”
From Phenomenology to Neurophysiological Understanding of Hallucinations in Children and Adolescents
Jardri, R., Bartels‐Velthuis, A. A., Debbané, M., Jenner, J. A., Kelleher, I., Dauvilliers, Y. A., Plazzi, G., Demeulemeester, M., David, C. N., Rapoport, J. L., et al. (2014) · Schizophrenia Bulletin · doi:10.1093/schbul/sbu029 · Cited by 93 · see citing works
Self-citationCognitive mechanisms of auditory verbal hallucinations in psychotic and non-psychotic groups
Badcock, J. C., & Hugdahl, K. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.07.010 · Cited by 92 · see citing works
Mondino, M., Haesebaert, F., Poulet, E., Suaud‐Chagny, M., & Brunelin, J. (2014) · Schizophrenia Research · doi:10.1016/j.schres.2014.10.054 · Cited by 92 · see citing works
“Auditory verbal hallucinations (AVH) in patients with schizophrenia have been associated with abnormal activity within the frontal and temporo-parietal areas (Jardri et al., 2011) and with a failure in source-monitoring processes (Frith, 1995; Waters et al., 2012).”
BackgroundFord, J. M., Palzes, V. A., Roach, B. J., Potkin, S. G., van Erp, T. G. M., Turner, J. A., Mueller, B. A., Calhoun, V. D., Voyvodic, J. T., Belger, A., et al. (2014) · Schizophrenia Bulletin · doi:10.1093/schbul/sbu031 · Cited by 90 · see citing works
Abnormalities in structural covariance of cortical gyrification in schizophrenia
Palaniyappan, L. K., Park, B., Balain, V., Dangi, R., & Liddle, P. F. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0772-2 · Cited by 92 · see citing works
“guage-processing regions that are repeatedly implicated in the generation of psychotic symptoms (Jardri et al. 2011; Li et al. 2012; Modinos et al. 2013).”
BackgroundGeoffroy, P. A., Houenou, J., Duhamel, A., Amad, A., De Weijer, A. D., Ćurčić-Blake, B., Linden, D. E. J., Thomas, P., & Jardri, R. (2014) · Schizophrenia Research · doi:10.1016/j.schres.2014.07.014 · Cited by 90 · see citing works
“Auditory-verbal hallucinations (AVHs), i.e., hearing voices in the absence of external stimuli, can be observed trans-diagnostically, although they are notably present in the schizophrenia spectrum (SZ) (Jardri et al., 2013).”
ResultInfluentialSelf-citationThe role of the primary auditory cortex in the neural mechanism of auditory verbal hallucinations
Kompus, K., Falkenberg, L. E., Bless, J. J., Johnsen, E., Kroken, R. A., Kråkvik, B., Larøi, F., Løberg, E.-M., Vedul-Kjelsås, E., Westerhausen, R., et al. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00144 · Cited by 91 · see citing works
“…by the wide-spread activation networks observed during the experience of ongoing AVHs, including higher auditory areas in the STG, but also parietal and frontal areas, and subcortical structures (Jardri et al., 2011; Kompus et al., 2011; Allen et al., 2012; see van Lutterveld et al., 2013).”
BackgroundTomescu, M. I., Rihs, T. A., Roinishvili, M., Karahanoğlu, F. I., Schneider, M., Menghetti, S., Ville, D. V. D., Brand, A., Chkonia, E. D., D, S. E. M., et al. (2015) · Schizophrenia Research Cognition · doi:10.1016/j.scog.2015.04.005 · Cited by 91 · see citing works
“Hence, the salience network dysfunction would be responsible for the emergence of psychotic symptoms, such as active auditory hallucinations, which were associated with increased activation in nodes of the SN (Jardri et al., 2011; Palaniyappan and Liddle, 2012).”
BackgroundFrӧhlich, F., Burrello, T. N., Mellin, J. M., Cordle, A. L., Lustenberger, C., Gilmore, J. H., & Jarskog, L. F. (2016) · European Psychiatry · doi:10.1016/j.eurpsy.2015.11.005 · Cited by 91 · see citing works
“Specifically, auditory cortical areas in the left temporo-parietal region have been shown to be hyperactive during auditory hallucinations in functional magnetic resonance imaging (fMRI) studies [8,9].”
BackgroundLeptourgos, P., Fortier, M., Carhart-Harris, R. L., Corlett, P. R., Dupuis, D., Halberstadt, A. L., Kometer, M., Kozáková, E., Larøi, F., Noorani, T. N., et al. (2020) · Schizophrenia Bulletin · doi:10.1093/schbul/sbaa117 · Cited by 87 · see citing works
Self-citationAuditory hallucinations: A review of the ERC “VOICE” project
Hugdahl, K. (2015) · World Journal of Psychiatry · doi:10.5498/wjp.v5.i2.193 · Cited by 88 · see citing works
Mallikarjun, P., Lalousis, P., Dunne, T. F., Heinze, K., Reniers, R., Broome, M., Farmah, B., Oyebode, F., Wood, S., & Upthegrove, R. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0118-6 · Cited by 84 · see citing works
“To give some address to this we have corrected for multiple comparisons using family- Table 2 Coordinates of brain regions activated during auditory verbal hallucinations (n= 9) Region of interest (BA) MNI Coordinates (x y z) Cluster size, p value (uncorr) Cluster 1 (left) Lingual gyrus (18) -24 -58 -4 k= 121 p 0.001*…”
InfluentialPalaniyappan, L., White, T., & Liddle, P. (2012) · Current Topics in Medicinal Chemistry · doi:10.2174/156802612805289881 · Cited by 81 · see citing works
Bose, A., Shivakumar, V., Agarwal, S. M., Kalmady, S. V., Shenoy, S., Sreeraj, V. S., Narayanaswamy, J. C., & Venkatasubramanian, G. (2017) · Schizophrenia Research · doi:10.1016/j.schres.2017.08.047 · Cited by 84 · see citing works
Billig, A. J., Lad, M., Sedley, W., & Griffiths, T. D. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102326 · Cited by 84 · see citing works
Beyond differences between the body schema and the body image: insights from body hallucinations
Pitron, V., & de Vignemont, F. (2017) · Consciousness and Cognition · doi:10.1016/j.concog.2017.06.006 · Cited by 86 · see citing works
Bauer, C. C. C., Okano, K., Ghosh, S., Lee, Y. J., Melero, H., Angeles, C. D. L., Nestor, P. G., del Re, E. C., Northoff, G., Niznikiewicz, M. A., et al. (2020) · Psychiatry Research · doi:10.1016/j.psychres.2020.112770 · Cited by 76 · see citing works
Hoffman, R. E., Wu, K., Pittman, B., Cahill, J. D., Hawkins, K. A., Fernandez, T., & Hannestad, J. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.01.016 · Cited by 82 · see citing works
Whalley, H. C., Papmeyer, M., Romaniuk, L., Sprooten, E., Johnstone, E. C., Hall, J., Lawrie, S. M., Evans, K. L., Blumberg, H. P., Sussmann, J. E., et al. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.137 · Cited by 81 · see citing works
“…2008), and there are reports of associations of abnormalities in this region with clinical symptoms seen in the disorder (Kircher et al, 2001; Zhou et al, 2005; Nenadic et al, 2010; Jardri et al, 2011) together with neurological soft signs such as sensory integration deficits (Dazzan et al, 2004).”
BackgroundEchoes of the spoken past: how auditory cortex hears context during speech perception
Skipper, J. I. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0297 · Cited by 82 · see citing works
Auditory Verbal Hallucinations in Schizophrenia From a Levels of Explanation Perspective.
Hugdahl, K., & Sommer, I. (2018) · Schizophrenia bulletin · doi:10.1093/schbul/sbx142 · Cited by 83 · see citing works
de Weijer, A. D., Neggers, S. F. W., Diederen, K. M. J., Mandl, R. C. W., Kahn, R. S., Pol, H. E. H., & Sommer, I. E. (2011) · Human Brain Mapping · doi:10.1002/hbm.21463 · Cited by 81 · see citing works
“Its exact pathophysiology remains elusive, although functional MRI studies suggest the involvement of the language system [Diederen et al., 2010; Ford et al., 2007; Heinks-Maldonado et al., 2007; Jardri et al., 2010; Shergill et al., 2000; Sommer et al., 2008; Whitford et al., 2010].”
BackgroundKubera, K., Sambataro, F., Vasić, N., Wolf, N. D., Frasch, K., Hirjak, D., Thomann, P. A., & Wolf, R. C. (2014) · Progress in Neuro-psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2013.11.015 · Cited by 83 · see citing works
Curcic-Blake, B., Liemburg, E., Vercammen, A., Swart, M., Knegtering, H., Bruggeman, R., & Aleman, A. (2013) · Schizophrenia Bulletin · doi:10.1093/schbul/sbs107 · Cited by 78 · see citing works
“Age in years 31 (10) 30 (5) 34 (13) F(2,44) = 0.”
A 20-year multi-follow-up of hallucinations in schizophrenia, other psychotic, and mood disorders
Goghari, V. M., Harrow, M., Grossman, L. S., & Rosen, C. (2012) · Psychological Medicine · doi:10.1017/s0033291712002206 · Cited by 78 · see citing works
“Last, there is an increasing literature documenting biological mechanisms that may be involved in hallucinations (Shergill et al. 2000 ; Hubl et al. 2004 ; Goghari et al. 2010 ; Jardri et al. 2011) ; however, this literature needs to be supplemented with research on the phenomenology and theoretical significance of ha…”
BackgroundTranscranial direct-current stimulation in ultra-treatment-resistant schizophrenia
Lindenmayer, J., Kulsa, M. K. C., Sultana, T., Kaur, A., Yang, R., Ljuri, I., Parker, B., & Khan, A. (2018) · Brain stimulation · doi:10.1016/j.brs.2018.10.002 · Cited by 76 · see citing works
Horga, G., Cassidy, C., Xu, X., Moore, H. M., Slifstein, M., Snellenberg, J. X. V., & Abi‐Dargham, A. (2016) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2016.0178 · Cited by 76 · see citing works
Transcranial Magnetic Stimulation for Positive Symptoms in Schizophrenia: A Systematic Review
Marzouk, T., Homan, S., Azizi, H., Malhotra, A. K., & Homan, P. (2019) · Neuropsychobiology · doi:10.1159/000502148 · Cited by 76 · see citing works
Cui, Y. J., Liu, B., Song, M., Lipnicki, D. M., Li, J., Xie, S., Chen, Y., Li, P., Lü, L., Lv, L., et al. (2017) · Psychological Medicine · doi:10.1017/s0033291717001520 · Cited by 74 · see citing works
“In addition, functional activity analyses using functional MRI or positron emission tomography have demonstrated dysfunctional activations associated with auditory hallucinations in the MTG (McGuire et al. 1995; Woodruff et al. 1995; Lennox et al. 1999; Jardri et al. 2011).”
- Authors
- Jardri, R., Pouchet, A., Pins, D., & Thomas, P.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Venue
- American Journal of Psychiatry
- Published
- 2011-01
- Volume
- 168
- Issue
- 1
- Pages
- 73-81
- ISSN
- 0002-953X (ISSN-L)
- 1535-7228
- OpenAlex
- W2142837020
- Cited by
- 651
- References
- 99
- Citations by year
- 2026: 25 · 2025: 34 · 2024: 31 · 2023: 26 · 2022: 42 · 2021: 43 · 2020: 50 · 2019: 51 · 2018: 50 · 2017: 36 · 2016: 54 · 2015: 30 · 2014: 43 · 2013: 38 · 2012: 72
- FWCI
- 3.17
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Hallucinations in medical conditions
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Social Sciences › Arts and Humanities › Philosophy › Mental Health and Psychiatry
- Keywords
- auditory verbal hallucinations, schizophrenia, schizophrenia spectrum disorders, cortical activation, activation likelihood estimation, Broca's area, anterior insula, frontal operculum, temporal lobe, hippocampus, parahippocampal region, speech generation, speech perception, verbal memory, fronto-temporal network, medial temporal lobe
- MeSH terms
- Brain Mapping, Cerebral Cortex, Hallucinations, Humans, Magnetic Resonance Imaging, Schizophrenia, Schizophrenic Psychology, Positron-Emission Tomography
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