Astrocytes Control Sensory Acuity via Tonic Inhibition in the Thalamus

Hankyul Kwak; Wuhyun Koh; Sangwoo Kim; Kiyeong Song; Jeong Im Shin; Jung Moo Lee; Elliot H. Lee; Jin Young Bae; Go Eun Ha; Ju Eun Oh; Yongmin Mason Park; Sunpil Kim; Jiesi Feng; Seung Eun Lee; Ji Won Choi; Ki Hun Kim; Yoo Sung Kim; Junsung Woo; Dongsu Lee; Taehwang Son; Soon Woo Kwon; Ki Duk Park; Bo Eun Yoon; Jaeick Lee; Yulong Li; Hyunbeom Lee; Yong Chul Bae; C. Justin Lee; Eunji Cheong

doi:10.1016/j.neuron.2020.08.013

Astrocytes Control Sensory Acuity via Tonic Inhibition in the Thalamus

Hankyul Kwak, Wuhyun Koh, Sangwoo Kim, Kiyeong Song, Jeong Im Shin, Jung Moo Lee, Elliot H. Lee, Jin Young Bae, Go Eun Ha, Ju Eun Oh, Yongmin Mason Park, Sunpil Kim, Jiesi Feng, Seung Eun Lee, Ji Won Choi, Ki Hun Kim, Yoo Sung Kim, Junsung Woo, Dongsu Lee, Taehwang SonSoon Woo Kwon, Ki Duk Park, Bo Eun Yoon, Jaeick Lee, Yulong Li, Hyunbeom Lee, Yong Chul Bae, C. Justin Lee, Eunji Cheong

Research output: Contribution to journal › Article › peer-review

33 Citations (Scopus)

Abstract

Sensory discrimination is essential for survival. However, how sensory information is finely controlled in the brain is not well defined. Here, we show that astrocytes control tactile acuity via tonic inhibition in the thalamus. Mechanistically, diamine oxidase (DAO) and the subsequent aldehyde dehydrogenase 1a1 (Aldh1a1) convert putrescine into GABA, which is released via Best1. The GABA from astrocytes inhibits synaptically evoked firing at the lemniscal synapses to fine-tune the dynamic range of the stimulation-response relationship, the precision of spike timing, and tactile discrimination. Our findings reveal a novel role of astrocytes in the control of sensory acuity through tonic GABA release.

Original language	English
Pages (from-to)	691-706.e10
Journal	Neuron
Volume	108
Issue number	4
DOIs	https://doi.org/10.1016/j.neuron.2020.08.013
Publication status	Published - 2020 Nov 25

Bibliographical note

Funding Information:
This research was supported by the National Research Foundation of Korea (NRF) ( 2017R1A5A2015391 , 2014M3A7B4051596 , 2017R1A2B3011098 , 2017M3C7A1023471 , 2015R1A3A2066619 , 2013M3A9C4078145, and 2020R1A4A1019009 ), the Korea Health Technology R&D Project of the Korea Health Industry Development Institute ( HI18C1664 ), the International Collaborative R&D Program funded by the Ministry of Trade, Industry and Energy ( N0001720 ), the General Research Program of the National Natural Science Foundation of China ( 31871087 and 31671118 ), Brain Korea 21 PLUS, and Institute for Basic Science (IBS), Center for Cognition and Sociality (IBS-R001-D2) .

Publisher Copyright:
© 2020 Elsevier Inc.

All Science Journal Classification (ASJC) codes

Neuroscience(all)

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10.1016/j.neuron.2020.08.013

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Kwak, H., Koh, W., Kim, S., Song, K., Shin, J. I., Lee, J. M., Lee, E. H., Bae, J. Y., Ha, G. E., Oh, J. E., Park, Y. M., Kim, S., Feng, J., Lee, S. E., Choi, J. W., Kim, K. H., Kim, Y. S., Woo, J., Lee, D., ... Cheong, E. (2020). Astrocytes Control Sensory Acuity via Tonic Inhibition in the Thalamus. Neuron, 108(4), 691-706.e10. https://doi.org/10.1016/j.neuron.2020.08.013

@article{79f73b4104e64b189ba34685f6df2dc3,

title = "Astrocytes Control Sensory Acuity via Tonic Inhibition in the Thalamus",

abstract = "Sensory discrimination is essential for survival. However, how sensory information is finely controlled in the brain is not well defined. Here, we show that astrocytes control tactile acuity via tonic inhibition in the thalamus. Mechanistically, diamine oxidase (DAO) and the subsequent aldehyde dehydrogenase 1a1 (Aldh1a1) convert putrescine into GABA, which is released via Best1. The GABA from astrocytes inhibits synaptically evoked firing at the lemniscal synapses to fine-tune the dynamic range of the stimulation-response relationship, the precision of spike timing, and tactile discrimination. Our findings reveal a novel role of astrocytes in the control of sensory acuity through tonic GABA release.",

author = "Hankyul Kwak and Wuhyun Koh and Sangwoo Kim and Kiyeong Song and Shin, {Jeong Im} and Lee, {Jung Moo} and Lee, {Elliot H.} and Bae, {Jin Young} and Ha, {Go Eun} and Oh, {Ju Eun} and Park, {Yongmin Mason} and Sunpil Kim and Jiesi Feng and Lee, {Seung Eun} and Choi, {Ji Won} and Kim, {Ki Hun} and Kim, {Yoo Sung} and Junsung Woo and Dongsu Lee and Taehwang Son and Kwon, {Soon Woo} and Park, {Ki Duk} and Yoon, {Bo Eun} and Jaeick Lee and Yulong Li and Hyunbeom Lee and Bae, {Yong Chul} and Lee, {C. Justin} and Eunji Cheong",

note = "Funding Information: This research was supported by the National Research Foundation of Korea (NRF) ( 2017R1A5A2015391 , 2014M3A7B4051596 , 2017R1A2B3011098 , 2017M3C7A1023471 , 2015R1A3A2066619 , 2013M3A9C4078145, and 2020R1A4A1019009 ), the Korea Health Technology R&D Project of the Korea Health Industry Development Institute ( HI18C1664 ), the International Collaborative R&D Program funded by the Ministry of Trade, Industry and Energy ( N0001720 ), the General Research Program of the National Natural Science Foundation of China ( 31871087 and 31671118 ), Brain Korea 21 PLUS, and Institute for Basic Science (IBS), Center for Cognition and Sociality (IBS-R001-D2) . Publisher Copyright: {\textcopyright} 2020 Elsevier Inc.",

year = "2020",

month = nov,

day = "25",

doi = "10.1016/j.neuron.2020.08.013",

language = "English",

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Kwak, H, Koh, W, Kim, S, Song, K, Shin, JI, Lee, JM, Lee, EH, Bae, JY, Ha, GE, Oh, JE, Park, YM, Kim, S, Feng, J, Lee, SE, Choi, JW, Kim, KH, Kim, YS, Woo, J, Lee, D, Son, T, Kwon, SW, Park, KD, Yoon, BE, Lee, J, Li, Y, Lee, H, Bae, YC, Lee, CJ & Cheong, E 2020, 'Astrocytes Control Sensory Acuity via Tonic Inhibition in the Thalamus', Neuron, vol. 108, no. 4, pp. 691-706.e10. https://doi.org/10.1016/j.neuron.2020.08.013

TY - JOUR

T1 - Astrocytes Control Sensory Acuity via Tonic Inhibition in the Thalamus

AU - Kwak, Hankyul

AU - Koh, Wuhyun

AU - Kim, Sangwoo

AU - Song, Kiyeong

AU - Shin, Jeong Im

AU - Lee, Jung Moo

AU - Lee, Elliot H.

AU - Bae, Jin Young

AU - Ha, Go Eun

AU - Oh, Ju Eun

AU - Park, Yongmin Mason

AU - Kim, Sunpil

AU - Feng, Jiesi

AU - Lee, Seung Eun

AU - Choi, Ji Won

AU - Kim, Ki Hun

AU - Kim, Yoo Sung

AU - Woo, Junsung

AU - Lee, Dongsu

AU - Son, Taehwang

AU - Kwon, Soon Woo

AU - Park, Ki Duk

AU - Yoon, Bo Eun

AU - Lee, Jaeick

AU - Li, Yulong

AU - Lee, Hyunbeom

AU - Bae, Yong Chul

AU - Lee, C. Justin

AU - Cheong, Eunji

N1 - Funding Information: This research was supported by the National Research Foundation of Korea (NRF) ( 2017R1A5A2015391 , 2014M3A7B4051596 , 2017R1A2B3011098 , 2017M3C7A1023471 , 2015R1A3A2066619 , 2013M3A9C4078145, and 2020R1A4A1019009 ), the Korea Health Technology R&D Project of the Korea Health Industry Development Institute ( HI18C1664 ), the International Collaborative R&D Program funded by the Ministry of Trade, Industry and Energy ( N0001720 ), the General Research Program of the National Natural Science Foundation of China ( 31871087 and 31671118 ), Brain Korea 21 PLUS, and Institute for Basic Science (IBS), Center for Cognition and Sociality (IBS-R001-D2) . Publisher Copyright: © 2020 Elsevier Inc.

PY - 2020/11/25

Y1 - 2020/11/25

N2 - Sensory discrimination is essential for survival. However, how sensory information is finely controlled in the brain is not well defined. Here, we show that astrocytes control tactile acuity via tonic inhibition in the thalamus. Mechanistically, diamine oxidase (DAO) and the subsequent aldehyde dehydrogenase 1a1 (Aldh1a1) convert putrescine into GABA, which is released via Best1. The GABA from astrocytes inhibits synaptically evoked firing at the lemniscal synapses to fine-tune the dynamic range of the stimulation-response relationship, the precision of spike timing, and tactile discrimination. Our findings reveal a novel role of astrocytes in the control of sensory acuity through tonic GABA release.

AB - Sensory discrimination is essential for survival. However, how sensory information is finely controlled in the brain is not well defined. Here, we show that astrocytes control tactile acuity via tonic inhibition in the thalamus. Mechanistically, diamine oxidase (DAO) and the subsequent aldehyde dehydrogenase 1a1 (Aldh1a1) convert putrescine into GABA, which is released via Best1. The GABA from astrocytes inhibits synaptically evoked firing at the lemniscal synapses to fine-tune the dynamic range of the stimulation-response relationship, the precision of spike timing, and tactile discrimination. Our findings reveal a novel role of astrocytes in the control of sensory acuity through tonic GABA release.

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DO - 10.1016/j.neuron.2020.08.013

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AN - SCOPUS:85091356334

SN - 0896-6273

VL - 108

SP - 691-706.e10

JO - Neuron

JF - Neuron

IS - 4

ER -

Astrocytes Control Sensory Acuity via Tonic Inhibition in the Thalamus

Abstract

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