Gamma-Band Auditory Steady-State Response as a Neurophysiological Marker for Excitation and Inhibition Balance: A Review for Understanding Schizophrenia and Other Neuropsychiatric Disorders

Tada, Mariko; Kirihara, Kazuhiro; Koshiyama, Daisuke; Fujioka, Masahiro; Usui, Kaori; Uka, Takanori; Komatsu, Misako; Kunii, Naoto; Araki, Tsuyoshi; Kasai, Kiyoto

doi:10.1177/1550059419868872

Cited by 60 publications

(46 citation statements)

References 116 publications

(155 reference statements)

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“…Although speculative, locations of smaller local networks may spatially vary in individuals compared to those of macro networks via large structures. Lastly, findings of resting-state gamma abnormalities may not generalize to more commonly studied stimulus-driven forms of gamma-band responses (54,(57)(58)(59). Future studies are needed to assess the relationships among spontaneous gamma activity at rest with gamma oscillations that are generated in response to 40-Hz stimulation.…”

Section: Discussionmentioning

confidence: 99%

Abnormal Spontaneous Gamma Power Is Associated With Verbal Learning and Memory Dysfunction in Schizophrenia

et al. 2020

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Background: Schizophrenia patients exhibit cognitive deficits across multiple domains, including verbal memory, working memory, and executive function, which substantially contribute to psychosocial disability. Gamma oscillations are associated with a wide range of cognitive operations, and are important for cortico-cortical transmission and the integration of information across neural networks. While previous reports have shown that schizophrenia patients have selective impairments in the ability to support gamma oscillations in response to 40-Hz auditory stimulation, it is unclear if patients show abnormalities in gamma power at rest, or whether resting-state activity in other frequency bands is associated with cognitive functioning in schizophrenia patients. Methods: Resting-state electroencephalogram (EEG) was assessed over 3 min in 145 healthy comparison subjects and 157 schizophrenia patients. Single-word reading ability was measured via the reading subtest of the Wide Range Achievement Test-3 (WRAT). Auditory attention and working memory were evaluated using Letter-Number Span and Letter-Number Sequencing. Executive function was assessed via perseverative responses on the Wisconsin Card Sorting Test (WCST). Verbal learning performance was measured using the California Verbal Learning Test second edition (CVLT-II). Results: Schizophrenia patients showed normal levels of delta-band power but abnormally elevated EEG power in theta, alpha, beta, and gamma bands. An exploratory correlation analysis showed a significant negative correlation of gammaband power and verbal learning performance in schizophrenia patients. Conclusions: Patients with schizophrenia have abnormal resting-state EEG power across multiple frequency bands; gamma-band abnormalities were selectively and

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Section: Discussionmentioning

confidence: 99%

Abnormal Spontaneous Gamma Power Is Associated With Verbal Learning and Memory Dysfunction in Schizophrenia

et al. 2020

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“…Electroencephalographic and magnetoencephalographic recordings can be used to noninvasively detect ASSRs in humans, which show a peak frequency at 40 Hz ( Pastor et al, 2002 ). A number of studies on the 40-Hz ASSR have reported reductions in the evoked power and phase-locking measures (i.e., inter-trial phase coherence) in individuals with schizophrenia (SZ) ( Thune et al, 2016 ; Tada et al, 2019 ). The reduction of 40-Hz ASSR has been proposed as a biomarker of the N-methyl-D-aspartate receptor (NMDAR) hypofunction in SZ patients ( Sivarao et al, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Aberrant Auditory Steady-State Response of Awake Mice After Single Application of the NMDA Receptor Antagonist MK-801 Into the Medial Geniculate Body

Wang

Chen

et al. 2020

International Journal of Neuropsychopharmacology

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Background Systemic administration of noncompetitive N-methyl-D-aspartate receptor (NMDAR) antagonists such as MK-801 is widely used to model psychosis of schizophrenia (SZ). Acute systemic MK-801 in rodents caused an increase of the auditory steady-state responses (ASSRs), the oscillatory neural responses to periodic auditory stimulation, while most studies in patients with SZ reported a decrease of ASSRs. This inconsistency may be attributable to the comprehensive effects of systemic administration of MK-801. Here, we examined how the ASSR is affected by selectively blocking NMDAR in the thalamus. Methods We implanted multiple electrodes in the auditory cortex (AC) and prefrontal cortex to simultaneously record the local field potential and spike activity (SA) of multiple sites from awake mice. Click-trains at a 40-Hz repetition rate were used to evoke the ASSR. We compared the mean trial power and phase-locking factor and the firing rate of SA before and after microinjection of MK-801 (1.5 µg) into the medial geniculate body (MGB). Results We found that both the AC and prefrontal cortex showed a transient local field potential response at the onset of click-train stimulus, which was less affected by the application of MK-801 in the MGB. Following the onset response, the AC also showed a response continuing throughout the stimulus period, corresponding to the ASSR, which was suppressed by the application of MK-801. Conclusion Our data suggest that the MGB is one of the generators of ASSR, and NMDAR hypofunction in the thalamocortical projection may account for the ASSR deficits in SZ.

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“…Alternatively, long ISI (20 s) used in this study might decay the noise level at the mid-time point of ISI. An increase in induced gamma power has been reported in schizophrenia in relatively short ISIs (~1-3 s) during auditory steadystate stimulation [37][38][39]. Regardless, it suggests that the evokedgamma power deficit is not simply caused by elevation of spontaneous power during the click-train stimulus period.…”

Section: Discussionmentioning

confidence: 91%

“…Time 0 is tone onset. The red dashed area(35)(36)(37)(38)(39)(40)(41)(42)(43)(44) Hz frequency and during 200 ms before cessation of the click train) was for the following ASSR analyses. b Evoked-power amplitudes at 35-44 Hz during 200 ms before cessation of click-train stimuli were obtained by time-frequency decomposition of averaged LFP trace across 50 trains of stimuli following subtraction of spontaneous power amplitude (z-score, 200-ms segment) at the midtime point of the ISIs (20-s duration) from LFP power amplitude (z-score…”

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confidence: 99%

GSK3β inhibition restores cortical gamma oscillation and cognitive behavior in a mouse model of NMDA receptor hypofunction relevant to schizophrenia

Nakao

Singh

Sapkota

et al. 2020

Neuropsychopharmacol.

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Cortical gamma oscillations are believed to be involved in mental processes which are disturbed in schizophrenia. For example, the magnitudes of sensory-evoked oscillations, as measured by auditory steady-state responses (ASSRs) at 40 Hz, are robustly diminished, whereas the baseline gamma power is enhanced in schizophrenia. Such dual gamma oscillation abnormalities are also present in a mouse model of N-methyl-D-aspartate receptor hypofunction (Ppp1r2cre/Grin1 knockout mice). However, it is unclear whether the abnormal gamma oscillations are associated with dysfunction in schizophrenia. We found that glycogen synthase kinase-3 (GSK3) is overactivated in corticolimbic parvalbumin-positive GABAergic interneurons in Grin1 mutant mice. Here we addressed whether GSK3β inhibition reverses both abnormal gamma oscillations and behavioral deficits with high correlation by pharmacological and genetic approach. We demonstrated that the paralog selective-GSK3β inhibitor, but not GSK3α inhibitor, normalizes the diminished ASSRs, excessive baseline gamma power, and deficits in spatial working memory and prepulse inhibition (PPI) of acoustic startle in Grin1 mutant mice. Cell-type specific GSK3B knockdown, but not GSK3A knockdown, also reversed abnormal gamma oscillations and behavioral deficits. Moreover, GSK3B knockdown, but not GSK3A knockdown, reverses the mutants’ in vivo spike synchrony deficits. Finally, ex vivo patch-clamp recording from pairs of neighboring cortical pyramidal neurons showed a reduction of synchronous spontaneous inhibitory-postsynaptic-current events in mutants, which was reversed by GSK3β inhibition genetically and pharmacologically. Together, GSK3β inhibition in corticolimbic interneurons ameliorates the deficits in spatial working memory and PPI, presumably by restoration of synchronous GABA release, synchronous spike firing, and evoked-gamma power increase with lowered baseline power.

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Gamma-Band Auditory Steady-State Response as a Neurophysiological Marker for Excitation and Inhibition Balance: A Review for Understanding Schizophrenia and Other Neuropsychiatric Disorders

Cited by 60 publications

References 116 publications

Abnormal Spontaneous Gamma Power Is Associated With Verbal Learning and Memory Dysfunction in Schizophrenia

Abnormal Spontaneous Gamma Power Is Associated With Verbal Learning and Memory Dysfunction in Schizophrenia

Aberrant Auditory Steady-State Response of Awake Mice After Single Application of the NMDA Receptor Antagonist MK-801 Into the Medial Geniculate Body

GSK3β inhibition restores cortical gamma oscillation and cognitive behavior in a mouse model of NMDA receptor hypofunction relevant to schizophrenia

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