Nicotine Facilitates Facial Stimulation-Evoked Mossy Fiber-Granule Cell Long-Term Potentiation in vivo in Mice

Nicotine is a psychoactive component of tobacco that plays critical roles in the regulation of neuronal circuit function and neuroplasticity and contributes to the improvement of working memory performance and motor learning function via nicotinic acetylcholine receptors (nAChRs). Under in vivo cond...

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Main Authors: Li-Xin Cao, Yan-Hua Bing, Yin-Hua Xu, Guang-Jian Zhang, Chun-Ping Chu, Lan Hong, De-Lai Qiu
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-07-01
Series:Frontiers in Cellular Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fncel.2022.905724/full
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author Li-Xin Cao
Yan-Hua Bing
Yin-Hua Xu
Guang-Jian Zhang
Chun-Ping Chu
Lan Hong
De-Lai Qiu
author_facet Li-Xin Cao
Yan-Hua Bing
Yin-Hua Xu
Guang-Jian Zhang
Chun-Ping Chu
Lan Hong
De-Lai Qiu
author_sort Li-Xin Cao
collection DOAJ
description Nicotine is a psychoactive component of tobacco that plays critical roles in the regulation of neuronal circuit function and neuroplasticity and contributes to the improvement of working memory performance and motor learning function via nicotinic acetylcholine receptors (nAChRs). Under in vivo conditions, nicotine enhances facial stimulation-evoked mossy fiber-granule cell (MF-GrC) synaptic transmission, which suggests that nicotine regulates MF-GrC synaptic plasticity in the mouse cerebellar cortex. In this study, we investigated the effects of nicotine on facial stimulation-induced long-term potentiation (LTP) of MF-GrC synaptic transmission in urethane-anesthetized mice. Our results showed that facial stimulation at 20 Hz induced an MF-GrC LTP in the mouse cerebellar granular layer that was significantly enhanced by the application of nicotine (1 μM). Blockade of α4β2 nAChRs, but not α7 nAChRs, during delivery of 20 Hz facial stimulation prevented the nicotine-induced facilitation of MF-GrC LTP. Notably, the facial stimulation-induced MF-GrC LTP was abolished by an N-methyl-D-aspartate (NMDA) receptor antagonist, but it was restored by additional application of nicotine during delivery of 20 Hz facial stimulation. Furthermore, antagonism of α4β2 nAChRs, but not α7 nAChRs, during delivery of 20 Hz facial stimulation prevented nicotine-induced MF-GrC LTP. Moreover, inhibition of nitric oxide synthase (NOS) abolished the facial stimulation-induced MF-GrC LTP, as well as the effect of nicotine on it. Our results indicated that 20 Hz facial stimulation induced MF-GrC LTP via an NMDA receptor/nitric oxide (NO) cascade, but MF-GrC LTP was enhanced by nicotine through the α4β2 AChR/NO signaling pathway. These results suggest that nicotine-induced facilitation of MF-GrC LTP may play a critical role in the improvement of working memory performance and motor learning function.
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spelling doaj.art-756e0e3f5fcb44debfcf358f13e8ffe22022-12-22T01:20:33ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022022-07-011610.3389/fncel.2022.905724905724Nicotine Facilitates Facial Stimulation-Evoked Mossy Fiber-Granule Cell Long-Term Potentiation in vivo in MiceLi-Xin Cao0Yan-Hua Bing1Yin-Hua Xu2Guang-Jian Zhang3Chun-Ping Chu4Lan Hong5De-Lai Qiu6Department of Physiology and Pathophysiology, College of Medicine, Yanbian University, Yanji, ChinaDepartment of Physiology and Pathophysiology, College of Medicine, Yanbian University, Yanji, ChinaDepartment of Neurology, Affiliated Hospital of Yanbian University, Yanji, ChinaDepartment of Pain, Affiliated Hospital of Yanbian University, Yanji, ChinaDepartment of Physiology, College of Basic Medicine, Jilin Medical University, Jilin City, ChinaDepartment of Physiology and Pathophysiology, College of Medicine, Yanbian University, Yanji, ChinaDepartment of Physiology, College of Basic Medicine, Jilin Medical University, Jilin City, ChinaNicotine is a psychoactive component of tobacco that plays critical roles in the regulation of neuronal circuit function and neuroplasticity and contributes to the improvement of working memory performance and motor learning function via nicotinic acetylcholine receptors (nAChRs). Under in vivo conditions, nicotine enhances facial stimulation-evoked mossy fiber-granule cell (MF-GrC) synaptic transmission, which suggests that nicotine regulates MF-GrC synaptic plasticity in the mouse cerebellar cortex. In this study, we investigated the effects of nicotine on facial stimulation-induced long-term potentiation (LTP) of MF-GrC synaptic transmission in urethane-anesthetized mice. Our results showed that facial stimulation at 20 Hz induced an MF-GrC LTP in the mouse cerebellar granular layer that was significantly enhanced by the application of nicotine (1 μM). Blockade of α4β2 nAChRs, but not α7 nAChRs, during delivery of 20 Hz facial stimulation prevented the nicotine-induced facilitation of MF-GrC LTP. Notably, the facial stimulation-induced MF-GrC LTP was abolished by an N-methyl-D-aspartate (NMDA) receptor antagonist, but it was restored by additional application of nicotine during delivery of 20 Hz facial stimulation. Furthermore, antagonism of α4β2 nAChRs, but not α7 nAChRs, during delivery of 20 Hz facial stimulation prevented nicotine-induced MF-GrC LTP. Moreover, inhibition of nitric oxide synthase (NOS) abolished the facial stimulation-induced MF-GrC LTP, as well as the effect of nicotine on it. Our results indicated that 20 Hz facial stimulation induced MF-GrC LTP via an NMDA receptor/nitric oxide (NO) cascade, but MF-GrC LTP was enhanced by nicotine through the α4β2 AChR/NO signaling pathway. These results suggest that nicotine-induced facilitation of MF-GrC LTP may play a critical role in the improvement of working memory performance and motor learning function.https://www.frontiersin.org/articles/10.3389/fncel.2022.905724/fullcerebellarfacial stimulationmossy fiber-granular celllong-term potentiation (LTP)nicotineneuropharmacology
spellingShingle Li-Xin Cao
Yan-Hua Bing
Yin-Hua Xu
Guang-Jian Zhang
Chun-Ping Chu
Lan Hong
De-Lai Qiu
Nicotine Facilitates Facial Stimulation-Evoked Mossy Fiber-Granule Cell Long-Term Potentiation in vivo in Mice
Frontiers in Cellular Neuroscience
cerebellar
facial stimulation
mossy fiber-granular cell
long-term potentiation (LTP)
nicotine
neuropharmacology
title Nicotine Facilitates Facial Stimulation-Evoked Mossy Fiber-Granule Cell Long-Term Potentiation in vivo in Mice
title_full Nicotine Facilitates Facial Stimulation-Evoked Mossy Fiber-Granule Cell Long-Term Potentiation in vivo in Mice
title_fullStr Nicotine Facilitates Facial Stimulation-Evoked Mossy Fiber-Granule Cell Long-Term Potentiation in vivo in Mice
title_full_unstemmed Nicotine Facilitates Facial Stimulation-Evoked Mossy Fiber-Granule Cell Long-Term Potentiation in vivo in Mice
title_short Nicotine Facilitates Facial Stimulation-Evoked Mossy Fiber-Granule Cell Long-Term Potentiation in vivo in Mice
title_sort nicotine facilitates facial stimulation evoked mossy fiber granule cell long term potentiation in vivo in mice
topic cerebellar
facial stimulation
mossy fiber-granular cell
long-term potentiation (LTP)
nicotine
neuropharmacology
url https://www.frontiersin.org/articles/10.3389/fncel.2022.905724/full
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