Coexistence of two forms of LTP in ACC provides a synaptic mechanism for the interactions between anxiety and chronic pain

Kohei Koga; Giannina Descalzi; Tao Chen; Hyoung-Gon Ko; Jinshan Lu; Shermaine Li; Junehee Son; TaeHyun Kim; Chuljung Kwak; Richard L Huganir; Ming-Gao Zhao; Bong-Kiun Kaang; Graham L Collingridge; Min Zhuo

doi:10.1016/j.neuron.2014.12.021

Coexistence of two forms of LTP in ACC provides a synaptic mechanism for the interactions between anxiety and chronic pain

Kohei Koga, Giannina Descalzi, Tao Chen, Hyoung-Gon Ko, Jinshan Lu, Shermaine Li, Junehee Son, TaeHyun Kim, Chuljung Kwak, Richard L Huganir, Ming-Gao Zhao, Bong-Kiun Kaang, Graham L Collingridge, Min Zhuo

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Abstract

Chronic pain can lead to anxiety and anxiety can enhance the sensation of pain. Unfortunately, little is known about the synaptic mechanisms that mediate these re-enforcing interactions. Here we characterized two forms of long-term potentiation (LTP) in the anterior cingulate cortex (ACC); a presynaptic form (pre-LTP) that requires kainate receptors and a postsynaptic form (post-LTP) that requires N-methyl-D-aspartate receptors. Pre-LTP also involves adenylyl cyclase and protein kinase A and is expressed via a mechanism involving hyperpolarization-activated cyclic nucleotide-gated (HCN) channels. Interestingly, chronic pain and anxiety both result in selective occlusion of pre-LTP. Significantly, microinjection of the HCN blocker ZD7288 into the ACC in vivo produces both anxiolytic and analgesic effects. Our results provide a mechanism by which two forms of LTP in the ACC may converge to mediate the interaction between anxiety and chronic pain.

Original language	English
Pages (from-to)	377-389
Number of pages	13
Journal	Neuron
Volume	85
Issue number	2
Early online date	31 Dec 2014
DOIs	https://doi.org/10.1016/j.neuron.2014.12.021
Publication status	Published - 21 Jan 2015

Keywords

Analgesics
Animals
Anti-Anxiety Agents
Anxiety
Chronic Pain
Gyrus Cinguli
Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
Long-Term Potentiation
Mice
Neurons
Pyrimidines
Receptors, Kainic Acid
Receptors, N-Methyl-D-Aspartate
Synaptic Transmission

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Molecular mechanisms of long-term Depression int the hippocampus
Collingridge, G. L. (Principal Investigator)
1/05/13 → 30/04/18
Project: Research

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title = "Coexistence of two forms of LTP in ACC provides a synaptic mechanism for the interactions between anxiety and chronic pain",

abstract = "Chronic pain can lead to anxiety and anxiety can enhance the sensation of pain. Unfortunately, little is known about the synaptic mechanisms that mediate these re-enforcing interactions. Here we characterized two forms of long-term potentiation (LTP) in the anterior cingulate cortex (ACC); a presynaptic form (pre-LTP) that requires kainate receptors and a postsynaptic form (post-LTP) that requires N-methyl-D-aspartate receptors. Pre-LTP also involves adenylyl cyclase and protein kinase A and is expressed via a mechanism involving hyperpolarization-activated cyclic nucleotide-gated (HCN) channels. Interestingly, chronic pain and anxiety both result in selective occlusion of pre-LTP. Significantly, microinjection of the HCN blocker ZD7288 into the ACC in vivo produces both anxiolytic and analgesic effects. Our results provide a mechanism by which two forms of LTP in the ACC may converge to mediate the interaction between anxiety and chronic pain.",

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author = "Kohei Koga and Giannina Descalzi and Tao Chen and Hyoung-Gon Ko and Jinshan Lu and Shermaine Li and Junehee Son and TaeHyun Kim and Chuljung Kwak and Huganir, {Richard L} and Ming-Gao Zhao and Bong-Kiun Kaang and Collingridge, {Graham L} and Min Zhuo",

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AU - Koga, Kohei

AU - Descalzi, Giannina

AU - Chen, Tao

AU - Ko, Hyoung-Gon

AU - Lu, Jinshan

AU - Li, Shermaine

AU - Son, Junehee

AU - Kim, TaeHyun

AU - Kwak, Chuljung

AU - Huganir, Richard L

AU - Zhao, Ming-Gao

AU - Kaang, Bong-Kiun

AU - Collingridge, Graham L

AU - Zhuo, Min

PY - 2015/1/21

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N2 - Chronic pain can lead to anxiety and anxiety can enhance the sensation of pain. Unfortunately, little is known about the synaptic mechanisms that mediate these re-enforcing interactions. Here we characterized two forms of long-term potentiation (LTP) in the anterior cingulate cortex (ACC); a presynaptic form (pre-LTP) that requires kainate receptors and a postsynaptic form (post-LTP) that requires N-methyl-D-aspartate receptors. Pre-LTP also involves adenylyl cyclase and protein kinase A and is expressed via a mechanism involving hyperpolarization-activated cyclic nucleotide-gated (HCN) channels. Interestingly, chronic pain and anxiety both result in selective occlusion of pre-LTP. Significantly, microinjection of the HCN blocker ZD7288 into the ACC in vivo produces both anxiolytic and analgesic effects. Our results provide a mechanism by which two forms of LTP in the ACC may converge to mediate the interaction between anxiety and chronic pain.

AB - Chronic pain can lead to anxiety and anxiety can enhance the sensation of pain. Unfortunately, little is known about the synaptic mechanisms that mediate these re-enforcing interactions. Here we characterized two forms of long-term potentiation (LTP) in the anterior cingulate cortex (ACC); a presynaptic form (pre-LTP) that requires kainate receptors and a postsynaptic form (post-LTP) that requires N-methyl-D-aspartate receptors. Pre-LTP also involves adenylyl cyclase and protein kinase A and is expressed via a mechanism involving hyperpolarization-activated cyclic nucleotide-gated (HCN) channels. Interestingly, chronic pain and anxiety both result in selective occlusion of pre-LTP. Significantly, microinjection of the HCN blocker ZD7288 into the ACC in vivo produces both anxiolytic and analgesic effects. Our results provide a mechanism by which two forms of LTP in the ACC may converge to mediate the interaction between anxiety and chronic pain.

KW - Analgesics

KW - Animals

KW - Anti-Anxiety Agents

KW - Anxiety

KW - Chronic Pain

KW - Gyrus Cinguli

KW - Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels

KW - Long-Term Potentiation

KW - Mice

KW - Neurons

KW - Pyrimidines

KW - Receptors, Kainic Acid

KW - Receptors, N-Methyl-D-Aspartate

KW - Synaptic Transmission

U2 - 10.1016/j.neuron.2014.12.021

DO - 10.1016/j.neuron.2014.12.021

M3 - Article (Academic Journal)

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SN - 0896-6273

VL - 85

SP - 377

EP - 389

JO - Neuron

JF - Neuron

IS - 2

ER -

Coexistence of two forms of LTP in ACC provides a synaptic mechanism for the interactions between anxiety and chronic pain

Abstract

Keywords

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Molecular mechanisms of long-term Depression int the hippocampus

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