Interhemispheric cortical long-term potentiation in the auditory cortex requires heterosynaptic activation of entorhinal projection

Xiao Li; Ling He; Xiaohan Hu; Fengwen Huang; Xue Wang; Mengying Chen; Ezra Ginn Yoon; Stephen Temitayo Bello; Tao Chen; Xi Chen; Peng Tang; Congping Chen; Jianan Qu; Jufang He

doi:10.1016/j.isci.2023.106542

Interhemispheric cortical long-term potentiation in the auditory cortex requires heterosynaptic activation of entorhinal projection

Xiao Li^*, Ling He, Xiaohan Hu, Fengwen Huang, Xue Wang, Mengying Chen, Ezra Ginn Yoon, Stephen Temitayo Bello, Tao Chen, Xi Chen, Peng Tang, Congping Chen, Jianan Qu, Jufang He^*

^*Corresponding author for this work

Research output: Journal Publications and Reviews › RGC 21 - Publication in refereed journal › peer-review

5 Citations (Scopus)

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Abstract

Long-term potentiation (LTP), which underlies learning and memory, can be induced by high-frequency electrical stimulation (HFS or HFES) and is thought to occur at the synapses of efferent projection. Here, the contralateral connectivity in mice auditory cortex was investigated to reveal the fundamental corticocortical connection properties. After HFES, plasticity was not observed at the terminal synapses at the recording site. The optogenetic HFS at the recording site of the interhemispheric cortical projections could not induce LTP, but HFES at the recording site could induce the interhemispheric cortical LTP. Our subsequent results uncovered that it is the cholecystokinin (CCK) released from the entorhino-neocortical pathway induced by HEFS that modulates the neuroplasticity of the afferent projections, including interhemispheric auditory cortical afferents. Our study illustrates a heterosynaptic mechanism as the basis for cortical plasticity. This regulation might contribute new spots for the understanding and treatment of neurological disorders. © 2023 The Authors.

Original language	English
Article number	106542
Journal	iScience
Volume	26
Issue number	4
Online published	31 Mar 2023
DOIs	https://doi.org/10.1016/j.isci.2023.106542
Publication status	Published - 21 Apr 2023

Funding

Hong Kong Research Grants Council, General Research Fund: 11101215M, 11103220M, 11101818M, 11102417M, 11101521M (GRF, JFH); Hong Kong Research Grants Council, Collaborative Research Fund: C1014-15g, C7048-16g (CRF, JFH); Innovation and Technology Fund: MRP/053/18X, MRP/101/17X, GHP_075_19GD (ITF, JFH); Health and Medical Research Fund: 08194106, 03141196, 06172456, 09203656 (HMRF, XL,XC, JFH); National Natural Science Foundation of China: 31671102 (NSFC, JFH); Key Area Research and Development Program of Guangdong Province, 2018B030340001 (XL).

Research Keywords

Cellular neuroscience
Physiology
Sensory neuroscience

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This full text is made available under CC-BY-NC-ND 4.0. https://creativecommons.org/licenses/by-nc-nd/4.0/

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title = "Interhemispheric cortical long-term potentiation in the auditory cortex requires heterosynaptic activation of entorhinal projection",

abstract = "Long-term potentiation (LTP), which underlies learning and memory, can be induced by high-frequency electrical stimulation (HFS or HFES) and is thought to occur at the synapses of efferent projection. Here, the contralateral connectivity in mice auditory cortex was investigated to reveal the fundamental corticocortical connection properties. After HFES, plasticity was not observed at the terminal synapses at the recording site. The optogenetic HFS at the recording site of the interhemispheric cortical projections could not induce LTP, but HFES at the recording site could induce the interhemispheric cortical LTP. Our subsequent results uncovered that it is the cholecystokinin (CCK) released from the entorhino-neocortical pathway induced by HEFS that modulates the neuroplasticity of the afferent projections, including interhemispheric auditory cortical afferents. Our study illustrates a heterosynaptic mechanism as the basis for cortical plasticity. This regulation might contribute new spots for the understanding and treatment of neurological disorders. {\textcopyright} 2023 The Authors.",

keywords = "Cellular neuroscience, Physiology, Sensory neuroscience",

author = "Xiao Li and Ling He and Xiaohan Hu and Fengwen Huang and Xue Wang and Mengying Chen and Yoon, {Ezra Ginn} and Bello, {Stephen Temitayo} and Tao Chen and Xi Chen and Peng Tang and Congping Chen and Jianan Qu and Jufang He",

year = "2023",

month = apr,

day = "21",

doi = "10.1016/j.isci.2023.106542",

language = "English",

volume = "26",

number = "4",

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TY - JOUR

T1 - Interhemispheric cortical long-term potentiation in the auditory cortex requires heterosynaptic activation of entorhinal projection

AU - Li, Xiao

AU - He, Ling

AU - Hu, Xiaohan

AU - Huang, Fengwen

AU - Wang, Xue

AU - Chen, Mengying

AU - Yoon, Ezra Ginn

AU - Bello, Stephen Temitayo

AU - Chen, Tao

AU - Chen, Xi

AU - Tang, Peng

AU - Chen, Congping

AU - Qu, Jianan

AU - He, Jufang

PY - 2023/4/21

Y1 - 2023/4/21

N2 - Long-term potentiation (LTP), which underlies learning and memory, can be induced by high-frequency electrical stimulation (HFS or HFES) and is thought to occur at the synapses of efferent projection. Here, the contralateral connectivity in mice auditory cortex was investigated to reveal the fundamental corticocortical connection properties. After HFES, plasticity was not observed at the terminal synapses at the recording site. The optogenetic HFS at the recording site of the interhemispheric cortical projections could not induce LTP, but HFES at the recording site could induce the interhemispheric cortical LTP. Our subsequent results uncovered that it is the cholecystokinin (CCK) released from the entorhino-neocortical pathway induced by HEFS that modulates the neuroplasticity of the afferent projections, including interhemispheric auditory cortical afferents. Our study illustrates a heterosynaptic mechanism as the basis for cortical plasticity. This regulation might contribute new spots for the understanding and treatment of neurological disorders. © 2023 The Authors.

AB - Long-term potentiation (LTP), which underlies learning and memory, can be induced by high-frequency electrical stimulation (HFS or HFES) and is thought to occur at the synapses of efferent projection. Here, the contralateral connectivity in mice auditory cortex was investigated to reveal the fundamental corticocortical connection properties. After HFES, plasticity was not observed at the terminal synapses at the recording site. The optogenetic HFS at the recording site of the interhemispheric cortical projections could not induce LTP, but HFES at the recording site could induce the interhemispheric cortical LTP. Our subsequent results uncovered that it is the cholecystokinin (CCK) released from the entorhino-neocortical pathway induced by HEFS that modulates the neuroplasticity of the afferent projections, including interhemispheric auditory cortical afferents. Our study illustrates a heterosynaptic mechanism as the basis for cortical plasticity. This regulation might contribute new spots for the understanding and treatment of neurological disorders. © 2023 The Authors.

KW - Cellular neuroscience

KW - Physiology

KW - Sensory neuroscience

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U2 - 10.1016/j.isci.2023.106542

DO - 10.1016/j.isci.2023.106542

M3 - RGC 21 - Publication in refereed journal

C2 - 37123227

SN - 2589-0042

VL - 26

JO - iScience

JF - iScience

IS - 4

M1 - 106542

ER -

Interhemispheric cortical long-term potentiation in the auditory cortex requires heterosynaptic activation of entorhinal projection

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HMRF: CCK-B Receptor Antagonist for the Treatment of Depression in the Mouse Model

GRF: Gene Therapy for Epilepsy through Enhancing Inhibition with High-Frequency Activation of GABAergic Neurons in Mice

HMRF: Cholecystokinin Receptor Agonists as Potential New Drugs for Rescuing Learning and Memory Deficiency in Aged Wild Type and Alzheimer’s Disease Animals

Cite this

Interhemispheric cortical long-term potentiation in the auditory cortex requires heterosynaptic activation of entorhinal projection

Abstract

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Research Keywords

Publisher's Copyright Statement

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Projects

HMRF: CCK-B Receptor Antagonist for the Treatment of Depression in the Mouse Model

GRF: Gene Therapy for Epilepsy through Enhancing Inhibition with High-Frequency Activation of GABAergic Neurons in Mice

HMRF: Cholecystokinin Receptor Agonists as Potential New Drugs for Rescuing Learning and Memory Deficiency in Aged Wild Type and Alzheimer’s Disease Animals

Cite this