Enhanced Beta2-band Oscillations Denote Auditory Hallucination in Schizophrenia Patients and a Monkey Model of Psychosis

 Shuo Ma1  · Tianzhen Chen2  · Wenjun Jia3  · Jie Liu1  · Shihan Ding4  · Puzhe Li5,6,7 · Hong Gan2  · Dapeng Zhang8  · Shuxin Shao2  · Mu‑Ming Poo3,5,6,7 · Min Zhao2,6,9,10 · Bomin Sun1  · Jian Jiang3,11
1 Department of Neurosurgery, Ruijin Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai 200020, China 
2 Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai 200030, China 
3 Shanghai Center for Brain Science and Brain-inspired Technology, Lingang Laboratory, Shanghai 201602, China 
4 University of California at Berkeley, Berkeley, CA 94720, USA 
5 School of Life Science and Technology, ShanghaiTech University, Shanghai 201210, China 
6 Institute of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, CAS Key Laboratory of Primate Neurobiology, State Key Laboratory of Neuroscience, Chinese Academy of Sciences, Shanghai 200031, China 
7 Shanghai Center for Brain Science and Brain-Inspired Intelligence Technology, Lingang Laboratory, Shanghai 201210, China 
8 Fuyang Third People’s Hospital, Fuyang Mental Health Center, Fuyang 236052, China 
9 Shanghai Key Laboratory of Psychotic Disorders, Shanghai 200030, China 
10 Institute of Psychological and Behavioral Science, Shanghai Jiao Tong University, Shanghai 200030, China 11 Shanghai Quanlan Technology Co., Ltd, Shanghai 201602, China

An electroencephalographic (EEG) signature of auditory hallucinations (AHs) is important for facilitating the diagnosis and treatment of AHs in schizophrenia. We recorded EEG from 25 schizophrenia patients with recurrent AHs. During the period of AHs, EEG recordings exhibited significantly elevated beta2-band power in the temporal region, as compared to those recorded in the absence of AHs or during stimulation with verbal sounds. We further generated methamphetamine-treated rhesus monkeys exhibiting psychosis-like behaviors, including repetitive sudden searching actions in the absence of external intrusion, suggesting the occurrence of AHs. Epidural EEG beta2-band power in the temporal region of these monkeys was enhanced immediately after methamphetamine treatment and positively correlated with the frequency of sudden searching actions. Thus, the enhancement of temporal beta2-band oscillations represents a signature for AHs in both patients and a monkey model of psychosis, and this monkey model can be used for developing closed-loop neuromodulation approaches for the treatment of refractory AHs in schizophrenia.

Schizophrenia; Auditory hallucinations; Non-human primate; Methamphetamine; Electroencephalography