The Anterior Cingulate Cortex Promotes Long-Term Auditory Cortical Responses through an Indirect Pathway via the Rhinal Cortex in Mice

Ye Liang; Jing Li; Yu Tian; Peng Tang; Chunhua Liu; Xi Chen

doi:10.1523/JNEUROSCI.2252-22.2023

The Anterior Cingulate Cortex Promotes Long-Term Auditory Cortical Responses through an Indirect Pathway via the Rhinal Cortex in Mice

Ye Liang
, Jing Li
, Yu Tian
, Peng Tang
, Chunhua Liu
, Xi Chen^*

^*Corresponding author for this work

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

4 Citations (Scopus)

140 Downloads (CityUHK Scholars)

Abstract

Sensory cortical areas are robustly modulated by higher-order cortices. Our previous study shows that the anterior cingulate cortex(ACC) can immediately and transiently enhance responses in the mouse auditory cortex (ACx). Here, we further examined whetherstrong activation of ACC neurons can induce long-term effects in mice of both sexes. To our surprise, only stimulation of cell bodiesin the ACC, but not ACC-to-ACx terminal activation, induced long-term enhancement of auditory responses in the ACx. Anatomicalexamination showed that the ACC indirectly projects to the ACx via the rhinal cortex (RCx). High-frequency stimulation of ACC-projecting terminals to the RCx or RCx-projecting terminals to the ACx induced a similar effect as the cell body activation of ACC neurons, whereas silencing the RCx blocked this long-term enhancement. High-frequency stimulation of ACC projections to the RCx alsoinduced long-term augmentation of sound-evoked flight behavior in male mice. These results show that the ACC promotes the longterm enhancement of auditory responses in the ACx through an indirect pathway via the RCx.
© 2023 Liang, Li et al.

Original language	English
Pages (from-to)	4262-4278
Number of pages	17
Journal	The Journal of Neuroscience
Volume	43
Issue number	23
Online published	9 May 2023
DOIs	https://doi.org/10.1523/JNEUROSCI.2252-22.2023
Publication status	Published - 7 Jun 2023

Bibliographical note

Funding

This work was supported by the Hong Kong Research Grants Council, General Research Fund: 11103220 Jufang He [JFH], 11101521 (JFH), 11103922 (JFH), and 11101818 (JFH); Hong Kong Research Grants Council, Collaborative Research Fund: C1043-21G (JFH); Hong Kong Research Grants Council, Theme-Based Research Scheme: T13-605/18-W (JFH); Innovation and Technology Fund: GHP_075_19GD (JFH); Health and Medical Research Fund: 09203656 (JFH) and 06172456 to X.C.; and Guangdong Province Science and Technology Program: 2020A0505140007 (JFH).

Research Keywords

Female
Animals
Mice
Male
Gyrus Cinguli/physiology
Auditory Cortex/physiology
Neurons/physiology
Sound

Publisher's Copyright Statement

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

RGC Funding Information

RGC-funded

Access Output

10.1523/JNEUROSCI.2252-22.2023

153563201.pdfFinal Published version, 7.08 MBLicence: CC BY

Other Access Options

Check CityUHK Library

Permanent Link

Right click to copy link

Cite this

@article{781037344a70402c95e594680c72ba8b,

title = "The Anterior Cingulate Cortex Promotes Long-Term Auditory Cortical Responses through an Indirect Pathway via the Rhinal Cortex in Mice",

abstract = "Sensory cortical areas are robustly modulated by higher-order cortices. Our previous study shows that the anterior cingulate cortex(ACC) can immediately and transiently enhance responses in the mouse auditory cortex (ACx). Here, we further examined whetherstrong activation of ACC neurons can induce long-term effects in mice of both sexes. To our surprise, only stimulation of cell bodiesin the ACC, but not ACC-to-ACx terminal activation, induced long-term enhancement of auditory responses in the ACx. Anatomicalexamination showed that the ACC indirectly projects to the ACx via the rhinal cortex (RCx). High-frequency stimulation of ACC-projecting terminals to the RCx or RCx-projecting terminals to the ACx induced a similar effect as the cell body activation of ACC neurons, whereas silencing the RCx blocked this long-term enhancement. High-frequency stimulation of ACC projections to the RCx alsoinduced long-term augmentation of sound-evoked flight behavior in male mice. These results show that the ACC promotes the longterm enhancement of auditory responses in the ACx through an indirect pathway via the RCx. {\textcopyright} 2023 Liang, Li et al.",

keywords = "Female, Animals, Mice, Male, Gyrus Cinguli/physiology, Auditory Cortex/physiology, Neurons/physiology, Sound",

author = "Ye Liang and Jing Li and Yu Tian and Peng Tang and Chunhua Liu and Xi Chen",

note = "Copyright {\textcopyright} 2023 Liang, Li et al.",

year = "2023",

month = jun,

day = "7",

doi = "10.1523/JNEUROSCI.2252-22.2023",

language = "English",

volume = "43",

pages = "4262--4278",

journal = "The Journal of Neuroscience",

issn = "0270-6474",

publisher = "Society for Neuroscience",

number = "23",

}

TY - JOUR

T1 - The Anterior Cingulate Cortex Promotes Long-Term Auditory Cortical Responses through an Indirect Pathway via the Rhinal Cortex in Mice

AU - Liang, Ye

AU - Li, Jing

AU - Tian, Yu

AU - Tang, Peng

AU - Liu, Chunhua

AU - Chen, Xi

PY - 2023/6/7

Y1 - 2023/6/7

N2 - Sensory cortical areas are robustly modulated by higher-order cortices. Our previous study shows that the anterior cingulate cortex(ACC) can immediately and transiently enhance responses in the mouse auditory cortex (ACx). Here, we further examined whetherstrong activation of ACC neurons can induce long-term effects in mice of both sexes. To our surprise, only stimulation of cell bodiesin the ACC, but not ACC-to-ACx terminal activation, induced long-term enhancement of auditory responses in the ACx. Anatomicalexamination showed that the ACC indirectly projects to the ACx via the rhinal cortex (RCx). High-frequency stimulation of ACC-projecting terminals to the RCx or RCx-projecting terminals to the ACx induced a similar effect as the cell body activation of ACC neurons, whereas silencing the RCx blocked this long-term enhancement. High-frequency stimulation of ACC projections to the RCx alsoinduced long-term augmentation of sound-evoked flight behavior in male mice. These results show that the ACC promotes the longterm enhancement of auditory responses in the ACx through an indirect pathway via the RCx. © 2023 Liang, Li et al.

AB - Sensory cortical areas are robustly modulated by higher-order cortices. Our previous study shows that the anterior cingulate cortex(ACC) can immediately and transiently enhance responses in the mouse auditory cortex (ACx). Here, we further examined whetherstrong activation of ACC neurons can induce long-term effects in mice of both sexes. To our surprise, only stimulation of cell bodiesin the ACC, but not ACC-to-ACx terminal activation, induced long-term enhancement of auditory responses in the ACx. Anatomicalexamination showed that the ACC indirectly projects to the ACx via the rhinal cortex (RCx). High-frequency stimulation of ACC-projecting terminals to the RCx or RCx-projecting terminals to the ACx induced a similar effect as the cell body activation of ACC neurons, whereas silencing the RCx blocked this long-term enhancement. High-frequency stimulation of ACC projections to the RCx alsoinduced long-term augmentation of sound-evoked flight behavior in male mice. These results show that the ACC promotes the longterm enhancement of auditory responses in the ACx through an indirect pathway via the RCx. © 2023 Liang, Li et al.

KW - Female

KW - Animals

KW - Mice

KW - Male

KW - Gyrus Cinguli/physiology

KW - Auditory Cortex/physiology

KW - Neurons/physiology

KW - Sound

UR - https://www.scopus.com/pages/publications/85163238931

UR - https://www.scopus.com/record/pubmetrics.uri?eid=2-s2.0-85163238931&origin=recordpage

U2 - 10.1523/JNEUROSCI.2252-22.2023

DO - 10.1523/JNEUROSCI.2252-22.2023

M3 - RGC 21 - Publication in refereed journal

C2 - 37160368

SN - 0270-6474

VL - 43

SP - 4262

EP - 4278

JO - The Journal of Neuroscience

JF - The Journal of Neuroscience

IS - 23

ER -

The Anterior Cingulate Cortex Promotes Long-Term Auditory Cortical Responses through an Indirect Pathway via the Rhinal Cortex in Mice

Abstract

Bibliographical note

Funding

Research Keywords

Publisher's Copyright Statement

RGC Funding Information

Access Output

Other Access Options

Permanent Link

Other Files and Links

Fingerprint

The Anterior Cingulate Cortex Top-down Modulates Auditory Responses in the Auditory Cortex through Direct and Indirect Pathways in Mice

GRF: Heterosynaptic Neuroplasticity of the Ascending Inputs in the Auditory Thalamus by Corticothalamic Modulation

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

CRF: Synthesized CCK-B Receptor Agonists to Alleviate Anterograde Amnesia in Animal Models

Cite this

The Anterior Cingulate Cortex Promotes Long-Term Auditory Cortical Responses through an Indirect Pathway via the Rhinal Cortex in Mice

Abstract

Bibliographical note

Funding

Research Keywords

Publisher's Copyright Statement

RGC Funding Information

Access Output

Other Access Options

Permanent Link

Other Files and Links

Fingerprint

Research output

The Anterior Cingulate Cortex Top-down Modulates Auditory Responses in the Auditory Cortex through Direct and Indirect Pathways in Mice

Projects

GRF: Heterosynaptic Neuroplasticity of the Ascending Inputs in the Auditory Thalamus by Corticothalamic Modulation

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

CRF: Synthesized CCK-B Receptor Agonists to Alleviate Anterograde Amnesia in Animal Models

Cite this