Neural Signature for Auditory Hallucinations in Schizophrenia: A High-Resolution Positron Emission Tomography Study with Fludeoxyglucose (F)

Overview

Journal Clin Psychopharmacol Neurosci

Specialty Psychiatry

Date 2018 Aug 21

PMID 30121983

Citations 4

Authors

Jong-Hoon Kim

Young Don Son

Jeong-Hee Kim

Hyo-Jong Lee

Nam-In Kang

Gyung Ho Chung

Jong-Il Park

Yin Cui

Woo-Sung Kim

Young-Chul Chung

Affiliations

Soon will be listed here.

Abstract

Objective: Auditory hallucinations (AHs) are a core symptom of schizophrenia. We investigated the neural signature of AHs by comparing hallucinating patients with schizophrenia with non-hallucinating patients with schizophrenia.

Methods: We recruited hallucinating patients with schizophrenia meeting the criteria for persistent, prominent, and predominant AHs (n=10) and non-hallucinating patients with schizophrenia (n=12). Various clinical assessments were performed incluing Psychotic Symptom Rating Scale for Auditory Hallucinations. Using fludeoxyglucose (F) positron emission tomography, regional differences in neural activity between the groups were analyzed.

Results: The regions of interest analysis showed significantly lower standardized uptake value ratio (SUVR) in the superior, middle, and inferior frontal gyri, and higher SUVR in the putamen in patients with AHs versus patients without AHs. These findings were confirmed in the voxel-wise analysis.

Conclusion: Our findings indicate that hypoactivity in the frontal and cingulate gyri, coupled with hyperactivity in the temporal gyrus and putamen, may contribute to the pathophysiology of AHs.

Citing Articles

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References

Posner M, Dehaene S . Attentional networks. Trends Neurosci. 1994; 17(2):75-9. DOI: 10.1016/0166-2236(94)90078-7. View

Pantelis C, Barnes T . Drug strategies and treatment-resistant schizophrenia. Aust N Z J Psychiatry. 1996; 30(1):20-37. DOI: 10.3109/00048679609076070. View

Barta P, Pearlson G, Powers R, RICHARDS S, Tune L . Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia. Am J Psychiatry. 1990; 147(11):1457-62. DOI: 10.1176/ajp.147.11.1457. View

Shergill S, Bullmore E, Simmons A, Murray R, McGuire P . Functional anatomy of auditory verbal imagery in schizophrenic patients with auditory hallucinations. Am J Psychiatry. 2000; 157(10):1691-3. DOI: 10.1176/appi.ajp.157.10.1691. View

Copolov D, Seal M, Maruff P, Ulusoy R, Wong M, Tochon-Danguy H . Cortical activation associated with the experience of auditory hallucinations and perception of human speech in schizophrenia: a PET correlation study. Psychiatry Res. 2003; 122(3):139-52. DOI: 10.1016/s0925-4927(02)00121-x. View

van Os J, Linscott R, Myin-Germeys I, Delespaul P, Krabbendam L . A systematic review and meta-analysis of the psychosis continuum: evidence for a psychosis proneness-persistence-impairment model of psychotic disorder. Psychol Med. 2008; 39(2):179-95. DOI: 10.1017/S0033291708003814. View

Paus T . Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat Rev Neurosci. 2001; 2(6):417-24. DOI: 10.1038/35077500. View

Harkavy-Friedman J, Kimhy D, Nelson E, Venarde D, Malaspina D, Mann J . Suicide attempts in schizophrenia: the role of command auditory hallucinations for suicide. J Clin Psychiatry. 2003; 64(8):871-4. View

Parellada E, Lomena F, Font M, Pareto D, Gutierrez F, Simo M . Fluordeoxyglucose-PET study in first-episode schizophrenic patients during the hallucinatory state, after remission and during linguistic-auditory activation. Nucl Med Commun. 2008; 29(10):894-900. DOI: 10.1097/MNM.0b013e328302cd10. View

10.

PENFIELD W . SOME MECHANISMS OF CONSCIOUSNESS DISCOVERED DURING ELECTRICAL STIMULATION OF THE BRAIN. Proc Natl Acad Sci U S A. 1958; 44(2):51-66. PMC: 335365. DOI: 10.1073/pnas.44.2.51. View

11.

Allen P, Laroi F, McGuire P, Aleman A . The hallucinating brain: a review of structural and functional neuroimaging studies of hallucinations. Neurosci Biobehav Rev. 2007; 32(1):175-91. DOI: 10.1016/j.neubiorev.2007.07.012. View

12.

Ueda Y, Kimura M . Encoding of direction and combination of movements by primate putamen neurons. Eur J Neurosci. 2003; 18(4):980-94. DOI: 10.1046/j.1460-9568.2003.02814.x. View

13.

Crawford J, Smith G, Maylor E, Della Sala S, Logie R . The Prospective and Retrospective Memory Questionnaire (PRMQ): Normative data and latent structure in a large non-clinical sample. Memory. 2003; 11(3):261-75. DOI: 10.1080/09658210244000027. View

14.

Silbersweig D, Stern E, Frith C, Cahill C, Holmes A, Grootoonk S . A functional neuroanatomy of hallucinations in schizophrenia. Nature. 1995; 378(6553):176-9. DOI: 10.1038/378176a0. View

15.

Horga G, Parellada E, Lomena F, Fernandez-Egea E, Mane A, Font M . Differential brain glucose metabolic patterns in antipsychotic-naïve first-episode schizophrenia with and without auditory verbal hallucinations. J Psychiatry Neurosci. 2011; 36(5):312-21. PMC: 3163647. DOI: 10.1503/jpn.100085. View

16.

Goldman H, Skodol A, Lave T . Revising axis V for DSM-IV: a review of measures of social functioning. Am J Psychiatry. 1992; 149(9):1148-56. DOI: 10.1176/ajp.149.9.1148. View

17.

McGuire P, Silbersweig D, Murray R, David A, Frackowiak R, Frith C . Functional anatomy of inner speech and auditory verbal imagery. Psychol Med. 1996; 26(1):29-38. DOI: 10.1017/s0033291700033699. View

18.

Falquez R, Couto B, Ibanez A, Freitag M, Berger M, Arens E . Detaching from the negative by reappraisal: the role of right superior frontal gyrus (BA9/32). Front Behav Neurosci. 2014; 8:165. PMC: 4023069. DOI: 10.3389/fnbeh.2014.00165. View

19.

Sommer I, Diederen K, Blom J, Willems A, Kushan L, Slotema K . Auditory verbal hallucinations predominantly activate the right inferior frontal area. Brain. 2008; 131(Pt 12):3169-77. DOI: 10.1093/brain/awn251. View

20.

Koechlin E, Jubault T . Broca's area and the hierarchical organization of human behavior. Neuron. 2006; 50(6):963-74. DOI: 10.1016/j.neuron.2006.05.017. View