Excitation-Inhibition Imbalance Leads to Alteration of Neuronal Coherence and Neurovascular Coupling under Acute Stress

Han, Kayoung; Lee, Myung‐Hee; Lim, Hyun-Kyoung; Jang, Minwoo Wendy; Kwon, Jea; Lee, C. Justin; Kim, Seong‐Gi; Suh, Minah

doi:10.1523/jneurosci.1553-20.2020

Cited by 24 publications

(22 citation statements)

References 54 publications

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“…Moreover, the PSD analysis provided novel insights into the physiology where a significantly lower relative power in 0.021-0.052 Hz (smooth muscle autonomic innervation) frequency band in elderly subjects with T2DM during the Mini-Cog three-item recall test potentially due to small fiber neuropathy [13] in the pial vessels. Furthermore, a drop in the oscillatory power in the 0.01-0.02-Hz frequency band during Mini-Cog three-item recall test due to cognitive load likely under acute stress [18], where the drop was more pronounced in the elderly subjects with T2DM, possibly because of glucocorticoid receptor signaling in T2DM [19]. Notably, transcranial electrical stimulation induces brain energy consumption that promotes systemic glucose uptake [20].…”

Section: Discussionmentioning

confidence: 99%

Functional Near-infrared Spectroscopy Of Prefrontal Cortex During Memory Encoding And Recall In Elderly With Type 2 Diabetes Mellitus

Zhao¹,

Tomita²,

Dutta³

2022

Preprint

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Abstract—Low-frequency Fahræus–Lindqvist-driven (not blood pressure-driven) oscillations in the small vessels are crucial because oscillations in small vessels support nutrient supply. Understanding of this is critical in type 2 diabetes mellitus (T2DM) to develop therapeutic measures to prevent Alzheimer's Disease Related Dementias: vascular factors contribute to cerebrovascular disease as well as mild cognitive impairment and dementia, which are predicted to affect 152 million people by 2050 (Alzheimer's Disease International London, UK, 2019). In this clinical study, we performed functional near-infrared spectroscopy (fNIRS) of the forehead to investigate the effect of the Mini-Cog with three-item recall test on the prefrontal cortex (PFC) activation and the relative oscillatory power in the 0.01–0.02-Hz (Fahræus–Lindqvist effect) and 0.021–0.052 Hz (smooth muscle autonomic innervation) frequency bands in elderly (60 years and older) T2DM and age-matched controls. We found a significant (p<0.01) difference in the PFC activation between elderly subjects with T2DM and age-matched elderly controls. Moreover, power spectral density (PSD) analysis revealed a significantly lower relative power in 0.021–0.052 Hz (smooth muscle autonomic innervation) frequency band in elderly subjects with T2DM during the Mini-Cog three-item recall test. Furthermore, a drop in the oscillatory power in the 0.01–0.02-Hz frequency band during Mini-Cog three-item recall test was found more pronounced in the elderly subjects with T2DM. Therefore, our study highlighted portable brain imaging to capture cerebrovascular reactivity to cognitive load that may provide a biomarker of cerebrovascular dysfunction in T2DM.Clinical Relevance— Our study establishes forehead portable brain imaging for monitoring cerebrovascular function in T2DM under cognitive load.

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Section: Discussionmentioning

confidence: 99%

Functional Near-infrared Spectroscopy Of Prefrontal Cortex During Memory Encoding And Recall In Elderly With Type 2 Diabetes Mellitus

Zhao¹,

Tomita²,

Dutta³

2022

Preprint

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“…Its activity reflects the influences of neurotransmitters and other vasoactive mediators on each of these cell types as well as metabolic demand ( 51 , 52 ). In a mouse model, Han et al ( 53 ) demonstrated that stress could disrupt the neuronal excitatory-inhibitory relationship changing the relationship between neuronal activity and the associated vascular response (neurovascular coupling). While STN-DBS might affect neurovascular coupling on a global or multi-regional basis during speech, neuronal coupling between blood flow and metabolism has been shown to be affected by levodopa, especially in individuals with levodopa induced dyskinesia, but not STN-DBS during the rest state ( 54 ).…”

Section: Discussionmentioning

confidence: 99%

Stimulation of the Subthalamic Nucleus Changes Cortical-Subcortical Blood Flow Patterns During Speech: A Positron Emission Tomography Study

Sidtis

Dhawan

et al. 2021

Front. Neurol.

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Background: Deep brain stimulation of the subthalamic nucleus (STN-DBS) is an effective treatment for Parkinson's disease (PD) but can have an adverse effect on speech. In normal speakers and in those with spinocerebellar ataxia, an inverse relationship between regional cerebral blood flow (rCBF) in the left inferior frontal (IFG) region and the right caudate (CAU) is associated with speech rate. This pattern was examined to determine if it was present in PD, and if so, whether it was altered by STN-DBS.Methods: Positron Emission Tomography (PET) measured rCBF during speech in individuals with PD not treated with STN-DBS (n = 7), and those treated with bilateral STN-DBS (n = 7). Previously reported results from non-PD control subjects (n = 16) were reported for comparison. The possible relationships between speech rate during scanning and data from the left and right IFG and CAU head regions were investigated using a step-wise multiple linear regression to identify brain regions that interacted to predict speech rate.Results: The multiple linear regression analysis replicated previously reported predictive coefficients for speech rate involving the left IFG and right CAU regions. However, the relationships between these predictive coefficients and speech rates were abnormal in both PD groups. In PD who had not received STN-DBS, the right CAU coefficient decreased normally with increasing speech rate but the left IFG coefficient abnormally decreased. With STN-DBS, this pattern was partially normalized with the addition of a left IFG coefficient that increased with speech rate, as in normal controls, but the abnormal left IFG decreasing coefficient observed in PD remained. The magnitudes of both cortical predictive coefficients but not the CAU coefficient were exaggerated with STN-DBS.Conclusions: STN-DBS partially corrects the abnormal relationships between rCBF and speech rate found in PD by introducing a left IFG subregion that increases with speech rate, but the conflicting left IFG subregion response remained. Conflicting IFG responses may account for some of the speech problems observed after STN-DBS. Cortical and subcortical regions may be differentially affected by STN-DBS.

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“…Thus, capillary flow was recently suggested not to be a passive consequence of the flow in upstream smooth muscle-unsheathed arterioles, but vice versa; capillary dilation may be a primary event preceding arteriole dilatation ( Kisler et al, 2017 ). In this scenario, capillary dilation would occur as a result of the relaxation of pericytes, and this local dilation would spread from capillaries toward larger arterioles in a secondary step ( Hall et al, 2014 ; Lendahl et al, 2019 ; Han et al, 2020 ). A crucial role of pericytes for capillary vasodilation during hemodynamic responses has been shown in numerous previous studies ( Lourenco et al, 2014 ; Sweeney-Reed et al, 2016 ; Caporarello et al, 2019 ; Alarcon-Martinez et al, 2020 ), although others failed to demonstrate this ( Fernandez-Klett et al, 2010 ; Hill et al, 2015 ; Wei et al, 2016 ; Cudmore et al, 2017 ; Iadecola, 2017 ).…”

Section: Coupling Of Inhibitory/excitatory Circuit Activation To Cerebral Blood Flowmentioning

confidence: 99%

“…On the other hand, pericytes have been shown to express NO-responsive enzymes ( Friebe et al, 2018 ). Also, a pericyte-induced role for vasodilation through capillaries would become feasible, since the large surface area of capillaries and minimal changes in their diameter would produce a large change in blood flow ( Han et al, 2020 ).…”

Section: Coupling Of Inhibitory/excitatory Circuit Activation To Cerebral Blood Flowmentioning

confidence: 99%

Disturbed Balance of Inhibitory Signaling Links Hearing Loss and Cognition

Knipper

Singer

Schwabe

et al. 2022

Front. Neural Circuits

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Neuronal hyperexcitability in the central auditory pathway linked to reduced inhibitory activity is associated with numerous forms of hearing loss, including noise damage, age-dependent hearing loss, and deafness, as well as tinnitus or auditory processing deficits in autism spectrum disorder (ASD). In most cases, the reduced central inhibitory activity and the accompanying hyperexcitability are interpreted as an active compensatory response to the absence of synaptic activity, linked to increased central neural gain control (increased output activity relative to reduced input). We here suggest that hyperexcitability also could be related to an immaturity or impairment of tonic inhibitory strength that typically develops in an activity-dependent process in the ascending auditory pathway with auditory experience. In these cases, high-SR auditory nerve fibers, which are critical for the shortest latencies and lowest sound thresholds, may have either not matured (possibly in congenital deafness or autism) or are dysfunctional (possibly after sudden, stressful auditory trauma or age-dependent hearing loss linked with cognitive decline). Fast auditory processing deficits can occur despite maintained basal hearing. In that case, tonic inhibitory strength is reduced in ascending auditory nuclei, and fast inhibitory parvalbumin positive interneuron (PV-IN) dendrites are diminished in auditory and frontal brain regions. This leads to deficits in central neural gain control linked to hippocampal LTP/LTD deficiencies, cognitive deficits, and unbalanced extra-hypothalamic stress control. Under these conditions, a diminished inhibitory strength may weaken local neuronal coupling to homeostatic vascular responses required for the metabolic support of auditory adjustment processes. We emphasize the need to distinguish these two states of excitatory/inhibitory imbalance in hearing disorders: (i) Under conditions of preserved fast auditory processing and sustained tonic inhibitory strength, an excitatory/inhibitory imbalance following auditory deprivation can maintain precise hearing through a memory linked, transient disinhibition that leads to enhanced spiking fidelity (central neural gain⇑) (ii) Under conditions of critically diminished fast auditory processing and reduced tonic inhibitory strength, hyperexcitability can be part of an increased synchronization over a broader frequency range, linked to reduced spiking reliability (central neural gain⇓). This latter stage mutually reinforces diminished metabolic support for auditory adjustment processes, increasing the risks for canonical dementia syndromes.

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Excitation-Inhibition Imbalance Leads to Alteration of Neuronal Coherence and Neurovascular Coupling under Acute Stress

Abstract: Planning & Evaluation (IITP) grant funded by the Korea government (MSIT) (No.

Cited by 24 publications

References 54 publications

Functional Near-infrared Spectroscopy Of Prefrontal Cortex During Memory Encoding And Recall In Elderly With Type 2 Diabetes Mellitus

Functional Near-infrared Spectroscopy Of Prefrontal Cortex During Memory Encoding And Recall In Elderly With Type 2 Diabetes Mellitus

Stimulation of the Subthalamic Nucleus Changes Cortical-Subcortical Blood Flow Patterns During Speech: A Positron Emission Tomography Study

Disturbed Balance of Inhibitory Signaling Links Hearing Loss and Cognition

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