Written by Guan Ao, Wang Shaoshuang, Huang Ailing, Deng Bin, Wang Qiang

Editor-in-charge - Wang Sizhen

Editor — Binwei Yang

Neural oscillations are rhythmic fluctuations over time in the firing activity of local populations of neurons or sets of neurons in multiple brain intervals, and can be recorded at the local field potential, cortical, EEG, and magnetoencephalography levels, with frequencies including Delta (1–4Hz), Theta (4–8Hz), Alpha (8–12 Hz), Beta (15–30 Hz), Gamma (30– 30– Hz) 90Hz) and high gamma (>50Hz

In July 2022, Professor Wang Qiang and Deputy Chief Physician Deng Bin of the First Affiliated Hospital of Xi'an Jiaotong University published a review article entitled "The role of gamma oscillations in central nervous system diseases: Mechanism and treatment" at Frontiers in Cellular Neuroscience

Gamma oscillations can be generated by pyramidal-interneuron network gamma oscillations (PING) or interneuron network gamma oscillations (ING)[1].

In addition to GABA energy signals, NMDA receptors in PV+ cells that produce relatively slow post-synaptic currents are also involved in regulating spontaneous and induced Gamma oscillations, and are important targets for NMDA receptor blockers (such as ketamine, MK-801, PCP, etc.

Figure 1 Neural circuits generated by Gamma oscillations: There are rich excitatory-inhibitory functional connections between pyramidal neurons and inhibitory interneurons, involving GABA energy and glutamatergic signals, which jointly regulate the synchronous firing activity of the Gamma frequency, that is, Gamma oscillation

(Source: Guan A.

2.
Abnormal gamma oscillations in central nervous system diseases

Gamma oscillations are widely present in multiple brain regions such as the cerebral cortex, hippocampus, olfactory bulb, amygdala, striatum, brainstem, etc.
, and are associated
with functions such as sensation, cognition and memory, movement, mood, and sleep-wake.

Because the generation of gamma oscillations is highly dependent on accurate synaptic transmission, adequate energy supply, and central nervous system microenvironment homeostasis, gamma oscillations can even occur before the prodromal symptoms of neurodegenerative lesions, so they can be used as a sensitive indicator
of neurological dysfunction to some extent.

The variation of gamma oscillations under different physiological or pathological conditions is complex, including its frequency, power, cross-frequency coupling, etc
.
(Table 1).

Table 1 Abnormal manifestations of Gamma oscillations in central nervous system diseases

(Table source: Guan, A.
et al.
, Front Cell Neurosci, 2022)

1.
Neuroinflammation and oxidative stress

As a high-speed electrical activity of neurons, gamma oscillation abnormalities are sensitive manifestations of microenvironmental disturbances in the central nervous system at the level of neuronal networks
.

Gamma network activity disorder has been reported in animal models of infectious inflammation, inflammaging, and neuroinflammation or oxidative stress caused by antibiotic-associated intestinal flora disorders [14-16].


Current animal and clinical trials have found that treatment with anti-inflammatory drugs such as ibuprofen and minocycline helps restore gamma oscillations and improve cognitive function [14,15].

2.
Hyperalgesia

Human EEG data show that the intensity of pain is encoded by gamma oscillations in the medial prefrontal cortex and is selective, i.
e.
, gamma oscillations do not track the intensity of visual, auditory, and non-injurious somatosensory stimuli [17,18].


Gamma oscillations that are significantly enhanced prior to pain perception can be recorded in the insula of epilepsy patients
.

Rodent studies support the amplification of gamma oscillations in the mediating of acute pain perception and disgust, as well as the regulation of allergic reactions to chronic pain [19].


Mice experiencing mechanical injury or inflammation in the primary somatosensory cortex (S1) Gamma oscillation is enhanced, susceptibility to pain sensation is enhanced
.

Inducing Gamma oscillations by S1 by optogenetic means improves pain sensitivity in mice and produces aversive avoidance behavior [20].

3.
Learning, memory and cognitive impairment

Gamma oscillations in the cortex and hippocampus are the basis for the network activity of
neuronal precise communication and information processing during attention, cognition, and memory.

A decrease in fast-rhythm oscillations (alpha, Beta, and Gamma frequencies) and a general increase in slow rhythms (Delta and Theta frequencies) are the most common neurological oscillatory changes in resting EEG/MAGNETO in AD patients [21].


Gaubert et al.
found that the amyloid β (Aβ) load in the brain of patients with neurodegenerative lesions showed an inverted U-shaped relationship with the Gamma oscillation power spectrum density recorded on EEG, reflecting the compensatory effects of the brain in the preclinical stage and the accelerated lesions after late decompensation [22].


Aβ, apoE4, tau protein and other AD pathogenic factors can destroy synaptic function through different molecular mechanisms, affecting the occurrence of Gamma oscillations
.

In addition, some patients with AD have developed olfactory dysfunction prior to the onset of Aβ plaque deposition and learning and memory deficits, which may be associated with abnormal gamma oscillations in the olfactory nervous system, suggesting that gamma oscillations may be a potential early electrophysiological marker of AD [23,24].

4.
Movement disorders

The basal ganglia-thalamus-cortical neural circuit is involved in motor control, and there are gamma oscillations at multiple nodes in this loop
.

Beta event-associated desynchronization and gamma event-associated synchronization in the medial part of the globule paleo are involved in the preparation process for spontaneous actions and the execution of spontaneous or externally triggered actions
.

Motor dysfunction in patients with PD is associated with imbalances in the "anti-motility" beta oscillation and "pro-motility" gamma oscillation patterns in the basal ganglia-thalamus-cortical network, and insufficient recruitment of gamma frequency synchronization outbreaks during exercise may be the basis for the onset of dyskinesia in patients with PD [25,26].


However, excessively strong gamma oscillations can also disrupt the physiological function of motor nerve circuits
.

Güttler et al.
found that patients with PD who had been treated with levodopa for a long time developed levodopa-induced dyskinesia, which was associated with sustained enhancement of Gamma oscillations in the narrowband of the M1 region [27].

5.
Negative emotional and mental disorders

The fear memory formation and regression loops are centered on the inner prefrontal lobe, amygdala, and hippocampus, and the neural oscillation changes mainly by the intensity of low-frequency or high-frequency gamma oscillations and their transverse coupling changes with Theta oscillations [28].


Murthy et al.
found that early weaned male mice had anxiety and hyperactivity susceptibility, and that the ventral Theta oscillation and Theta-Gamma transgenetic coupling of the hippocampus increased after mice entered the new environment, and that a decrease in the density of PV+ and SST+ interneurons on the dented ileolar ventral side of mice and an increase in the perneuronal networks of PV+ neurons suggested changes in neuronal plasticity [29].

ABNORMAL GABA energy signaling and hypofunction of NMDA receptors are closely related to schizophrenia (SCZ), an important manifestation of changes in the excitatory-inhibitory balance of cortical and subcortical networks, namely neurotic oscillations
.

The auditory steady-state response (ASSR) is commonly used in SCZ studies, and the 40-Hz ASSR spectral power and lock-in phase are significantly reduced in patients [30
].

Dysbindin-1 is a potential risk gene for SCZ, and the Gamma frequency neuronal firing mediates the transposition of dysbindin-1 into the mitochondria to interact with Drp1 and its receptors, promoting the formation of OLIGODs in Drp1 to drive mitochondrial division, a molecular defect that can lead to mitochondrial division disorders and weakening of Gamma oscillations [31].


In addition, patients with autism spectrum disorder (ASD) have a decrease in the number of interneurons, decreased expression of GABA receptor subunits, and decreased GABA levels, suggesting an imbalance of gabaergic excitatory-inhibitory.


Deficits in social novelty and impaired cognitive abilities exhibited in animal models of ASD are also associated with weakened Gamma oscillations [33-35].

Iii.
Therapeutic potential of Gamma
entrainment for diseases of the central nervous system 1.
Improving learning memory and cognitive function During emotional memory consolidation, gamma oscillations within the basolateral amygdala (BLA) are enhanced, while induction enhancement within BLA during memory consolidation enhances the sequential memory effect, whereas inhibition of gamma oscillations at this stage impairs subsequent memory intensity [36].


The use of optogenetic means to give 40Hz stimulation to medial septal nucleus PV+ neurons is conducive to restoring the hippocampal low-frequency Gamma oscillation and Theta-Gamma phase amplitude coupling in AD mice, and improving spatial memory [37].


Gamma entrainment using sensory stimulus (GENUS) uses patterned sensor stimuli such as visual or auditory to induce neural activity and gamma entrainment
.

A series of studies by Li-Huei Tsai's team have shown that GENUS can induce Guma oscillations in the visual cortex, auditory cortex, hippocampus, and mPFC regions of mice in AD model mice, improving cognitive and spatial memory function in mice [38-40].


Given the limited sample size of existing clinical trials, the treatment regimen and evaluation criteria are not uniform, the effect of Gamma entrainment on human cognitive memory impairment is still lacking a stable phenotype
.

2.
Promote the recovery of motor function

Deep brain stimulation (DBS) and transcranial alternating current stimulation (tACS) are major breakthroughs in PD treatment, and their possible mechanisms of action include the rebalancing
of neural oscillations.

DBS inhibits the "anti-dynamism" beta rhythm and enhances the "pro-dynamism" gamma rhythm [41,42].


TACS entrainment gamma oscillation is effective in improving bradykinesia in patients with PD [43].


In addition, post-stroke survivors are often accompanied by motor disability, and magnetoencephalography shows selective defects in Gamma's oscillatory reserves
.

The stronger the reserve of gamma oscillations produced in the cerebral hemispheres, the better the prognosis of the patient, suggesting that gamma oscillations accompany the entire recovery process of stroke [44].


Stimulation of inhibitory interneurons in the M1 region at 40 Hz during the acute phase of ischemic stroke in mice reduces the occurrence of diffuse depolarization of ischemic foci, relieves cerebral edema, increases cerebral blood flow, and promotes motor function recovery [45].

3.
Relieve negative emotions and mental disorders

Previous studies have elucidated patterns of Gamma oscillation regulation in neural circuits related to emotion and social behavior, but it remains unclear
whether Gamma entrainment has a therapeutic effect on negative mood and psychiatric disorders.

Previous research in this group has found that visual stimulation at 40Hz reduces anxiety and depression susceptibility to stress exposure in mice after cortical infarction in the hypocortex (histone deacetylase 3, HDAC3), cyclooxygenase 1 (cyclooxygenase 1, Cox1), and EPE2 expression levels in the amygdala [46].


Cao et al.
found that 40Hz optogenetic stimulation of PV+ interneurons nested at 8Hz frequencies on PV+ interneurons in the mPFC region of NL3R451-KI mice was effective in enhancing the social novelty preference of mice [35].

Table 2 Therapeutic effect of Gamma entrainment on diseases of the central nervous system

(Table source: Guan, A.
et al.
, Front Cell Neurosci, 2022)

Cellular mechanisms of Gamma entrainment therapy: neurons and glial cells

1.
Gamma entrainment provides neuroprotective

In animal models of AD, 40 Hz visual stimulation significantly reduced neuronal loss in brain regions such as V1 and CA1, and also alleviated the degenerative death of CA1 excitatory neurons in ischemic stroke animals, but the specific mechanism of this neuroprotective effect is still unknown
.

Adaikkan et al.
found that GENUS downregulated inflammatory gene expression while reducing DNA damage [40].


However, in the case of cerebral ischemic injury, the neuroprotective effect of GENUS does not stem from changes in cerebral blood flow or microglia responses, suggesting that gamma frequency visual stimulation may have a direct effect
on neurons.

Zheng et al.
speculate that Gamma entrainment may improve ca1 neurons' tolerance to ischemia-reperfusion injury by enhancing the pro-survival signals sent by CA3 transsynaptas to CA1 neurons [47].

2.
Gamma entrainment regulates synaptic plasticity

Neural oscillations are rhythmic voltage fluctuations at the local field potential level, and synchronized synaptic activity of a large number of neurons is the main microscopic event that triggers neural oscillations [48].


Activity-dependent changes in the intensity of internnal connections, known as synaptic plasticity, are complexly linked
to oscillations.

For example, synaptic plasticity in the hippocampus is regulated by the metabolic glutamate receptor 5 (mGlu5), while electrophysiology suggests that hippocampal Theta and Gamma oscillations induced by high-frequency afferent stimulation rely on mGlu5
.

This change in neurovibbing not only reflects the magnitude and persistence of changes in hippocampal synaptic efficacy, but is intrinsically linked to the successful occurrence of hippocampal LTP [48].


PV+ interneurons are mediated by gamma-CaMKII to produce excitatory synapse enhancement (LTPE→I) that maintains the Oscillation of the Theta and Gamma nerves, which is important for the establishment of hippocampal-dependent long-term memory [49].


_AβO1–42 interferes with the deuppressive effect of SST+ interneurons on the proximal DENDs of CA1 PC, thereby impairing the timing-dependent LTP (timing-dependent LTP) induced by nested Gamma oscillations, and optogenetic activation of PV+ and SST+ interneurons restores Gamma oscillations and gamma oscillation-induced tLTP effects [50
。

In the context of whole-brain crosstalk between neural oscillation and synaptic plasticity, it is worth exploring
whether enhancing gamma oscillation can promote the expression of synaptic plasticity-related molecules.

Studies by Adaikkan et al.
have shown that GENUS upregulates genes related to multiple synaptic transmission, intracellular, and vesicle transport, with the ability to regulate the phosphorylation status of neurons and synaptic proteins [40].


Zheng et al.
found that 40Hz visual stimulation helps to restore dendritic spine density in ca1 area, increase the level of G protein signaling regulator factor 12 (RGS12) in the hippocampus, and enhance CA3-CA1 synaptic LTP through the RGS12-N voltage-gated calcium channel-dependent pathway, which indicates that synchronized gamma oscillations in the brain can change hippocampal protein expression and enhance CA3-CA1 synaptic efficiency [47].

3.
Gamma oscillates with astrocytes

Although the direct effectors that produce neural oscillations are neurons, glial cells play an important role in supporting neuronal energy metabolism, synaptic plasticity, and microenvironment, and the discovery of gliotransmitters systems, the direct or indirect role of glial cells in neural oscillation and information processing is worth examining
.

The transient increase in calcium concentration in astrocytes precedes the onset of oscillating activity, and vesicle release is necessary for cholinergic induction of gamma oscillation maintenance (rather than triggering) and normal cognitive memory function [51].


Mederos et al.
found that PV interneurons in the mPFC region recruit astrocytes by activating GABA_BR, supporting the generation of Gamma oscillations and correct decision-making behavior
.

Selective ablation of mPFC astrocyte GABA_BR results in weakened gumma oscillations, impaired decision-making and working memory in mice during the T-maze cognitive task, and selective activation of astrocytes (rather than GABA-capable interneurons) to save mice from cognitive deficits [52].


Astrocyte GFAP and S100B in 5XFAD mice treated with GENUS were upregulated with vasodilation, which may contribute to Aβ clearance and cognitive improvement [39].

4.
Gamma entrainment regulates microglia

During brain development, microglia are both bidirectional regulators of synaptic plasticity and monitors of electrical activity in neurons
.

NMDA-induced gamma oscillations can be recorded in cortical organoids, which is closely related to microglia support for neuronal maturation and differentiation [53].


For mature brains, the interaction between steady-state microglia and synaptic structures promotes the synchronous firing of neuronal populations, while LPS-activated microglia lose this function [54].

Tsai's team's research showed that GENUS can promote the conversion of microglia to a phagocytic state, which is manifested in the form of enlarged cells, shortened protrusions, and increased
phagocytic activity of Aβ plaques.

At the same time, the number of rod microglia decreases and CD40 and C1q levels decrease, indicating that GENUS helps to downregulate the microglia inflammatory response [38-40].


The neuroinflammation mechanism studies of post-stroke anxiety in the previous research group showed that the activation of intraglial HDAC3 in the cortex of ischemic injury was upregulated, the p65 deacetylation was increased, the NF-κB pathway was activated, and the expression of downstream molecules Cox1 and PGE2 was promoted, and PGE2 then acted on the amygdala EP2 to induce susceptibility
to animals to stress exposure after stroke.

It is worth noting that we found that 40Hz visual stimulation can inhibit cortical microglia activation, downregulate the HDAC3/Cox1/PGE2/EP2 signaling pathway, and improve anxiety-like behavior in post-stroke animals, which means that GENUS may be an effective means of manipulating microglia immune responses and providing neuroprotective, the study was published in Frontiers in Immunology in February 2022 [46
。
It is important to note that GENUS has no significant effect on the number, morphology, and neuroinflammatory markers of microglia in older C57BL/6J mice (changes observed in P301S and CK-p25 mice), suggesting that microglia response to GENUS may vary depending on disease status or genetic background [40].

Fig.
2 Therapeutic effect
of Gamma entrainment on diseases of the central nervous system.

Invasive or non-invasive means are used to induce gamma entrainment in multiple brain regions, which can directly act on neurons and synapses to provide neuroprotective, or regulate the response state of astrocytes and microglia, thereby improving learning memory, movement, emotion and other neural functions
.

(Source: Guan A.
et al.
, Front Cell Neurosci, 2022)

V.
Summary and Outlook

In recent years, the influence of gamma oscillations on advanced functions such as learning and memory, pain, movement, and emotion has been continuously recognized, and gamma entrainment has shown therapeutic potential
in a number of neuropsychiatric diseases represented by cognitive memory impairment.

Using optogenetics and even more sophisticated techniques, we are able to customize the activation of brain regions and cells of interest, and explore the function and rescue measures of Gamma's neural oscillations
.

Cortical organoid technology allows us to observe and manipulate neural oscillation dynamics as well as microscale neurotransmitter signals
during the dynamics of brain development.

The pathological manifestations of Gamma oscillation in various disease groups, the effects of different entrainment modalities, and the effectiveness of the transition from animal experiments to clinical treatment remain to be explored
.

These research bases will help us deeply understand the connection between gamma oscillations and central nervous system diseases, and promote the application
of gamma entrainment in future diagnosis and treatment.
"

Original link: https://doi.
org/10.
3389/fncel.
2022.
962957

Fund support: National Natural Science Foundation of China (81974540), Fujian Provincial Natural Science Foundation of China (2021J01018), Xiamen University "College Students Innovation and Entrepreneurship Training Program" Innovation Training Project (2021X1073, S202110384894), etc
.

Guan Ao (first from left), Huang Ailing (second from left), Wang Shaoshuang (middle), Deng Bin (second from right), Wang Qiang (first from right)

(Photo courtesy of: Wang Qiang/Deng Bin team of the First Affiliated Hospital of Xi'an Jiaotong University)

About the Author (swipe up and down to read)

Wang Qiang, M.
D.
, Professor, Chief Physician, Doctoral Supervisor, Director of the Department of Anesthesiology and Anesthesiology, Head of the Science and Technology Innovation Team of Shaanxi Province, Director of the Key Research Office of Shaanxi Provincial Administration of Traditional Chinese Medicine, Member of the Teaching Guidance Sub-Committee of Anesthesiology of the Ministry of Education, Member of the Expert Committee of Capacity Building and Continuing Education anesthesiology of the National Health Commission, Member of the Anesthesiology Branch of the Chinese Medical Association (CSA), and Member of the Anesthesiologist Branch (CAA) of the Chinese Medical Doctor Association , Vice Chairman of the Anesthesiology Professional Committee of the Chinese Association of Integrative Traditional and Western Medicine, etc.
, Member of the Standing Committee of the International Journal of Anesthesiology and Resuscitation and the Chinese Journal of Anesthesiology
.

He has presided over 15 projects of the National Natural Science Foundation of China and the National Science and Technology Support Program, and published 127 SCI papers, of which 87 PAPERS were included in SCI in Neurosci Biobehav Rev, Biomaterials, Stroke, Anesthesiology, etc.
, and were published by Annu Rev Immunol and Nat Rev as the first author or corresponding author Neurosci and other SCI papers have been cited 1973 times, written into 30 monographs in Chinese and English, and the research results have won 1 first prize of the National Science and Technology Award (2011-7), 3 first prizes of Shaanxi Provincial Science and Technology Progress Award (2005-2, 2008-3 and 2016-3), etc.
, and 26 national patents (6 invention patents).

Deng Bin, MD, Deputy Chief Physician, Master Supervisor, Cooperative Academic Doctoral Supervisor, Department of Anesthesiology, First Affiliated Hospital of Xi'an Jiaotong University, engaged in medical, teaching and research work
.

He is committed to the key molecular regulatory mechanisms and translational medicine research
of central nervous system injury repair.

He has presided over 8 national natural science foundation projects and provincial and ministerial scientific research projects, and published 21 SCI papers, including 17 first or corresponding authors.
The highest SINGLE IF is 15.
3; 8 authorized national invention or utility model patents; he serves as a standing committee member of the Oral Anesthesia Committee of the Chinese Stomatology Association, a national member of the Thoracic Anesthesia Branch of the Chinese Society of Cardiothoracic and Anesthesiology, a national member of the Tumor Anesthesia and Analgesia Committee of the Chinese Anti-Cancer Association, and an editorial board or reviewer of many internationally renowned journals; and has won more than 20 academic awards
.

He won the third class merit once, the Shaanxi Provincial Natural Science Outstanding Academic Paper Award, and the Shaanxi Provincial Outstanding Doctoral Dissertation Award
.

Selected articles from previous issues

[1] The NAR-He Cheng/Su Zhida team found that topoisomerase IIA can regulate adult neurogenesis in the subependymal region

[2] The Sci Adv-Liao Wenbo team has made important progress in the adaptive evolution of amphibian brain volume

[3] J Neuroinflammation—From Changchun/Jian Zhang's team found that targeting proteoglycan receptors after hemorrhagic stroke protects white matter integrity and promotes the recovery of neurological function

[4] Front Aging Neurosci—Zeng Yanbing's team established a predictive model and revealed the effects of behavioral changes on cognitive impairment in the elderly

[5] The Sci Adv-Zhao Cunyou/Chen Rongqing team revealed the mechanism of microRNA inducing social and memory abnormalities in mice: miR-501-3p expression defects enhance glutamate delivery

[6] Sci Adv-Zhang Yi's research group found important neurons that regulate drug addiction behavior

[7] J Infect-Yifei Wang's team revealed that mamdc2, a highly expressed gene in Alzheimer's disease microglia, positively regulates the innate antiviral response of neurovirus infection

[8] Sci Adv—Xia Kun/Shen Yiping/Guo Hui revealed the relationship between key regulatory genes of stress particles and neurodevelopmental disorders

[9] Cell Prolif-Lai Liangxue/Zhang Kun/Zou Qingjian team worked together to successfully build a safe and efficient technology system for directional induction of motor neurons in vivo

[10] Nat Commun– Peng Yueqing's team discovered a new brain region that controls non-REM sleep

Recommended for high-quality scientific research training courses

【1】Special Training on Biomedical Statistics for Clinical Prediction of R Language (October 15-16, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing)

Forum/Seminar Preview

【1】2022 World Artificial Intelligence Conference | Brain-Machine Intelligent Fusion - Connecting the Brain to the Future (Shanghai World Expo Center, September 2)

Welcome to "Logical Neuroscience" [1] Talent Recruitment—"Logical Neuroscience" Recruitment Article Interpretation/Writing Positions ( Online Part-time, Online Office)

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