Cortical kainate receptors and behavioral anxiety

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Abstract

The study of glutamatergic synapses mainly focuses on the memory-related hippocampus. Recent studies in the cortical areas such as the anterior cingulate cortex (ACC) show that excitatory synapses can undergo long-term plastic changes in adult animals. Long-term potentiation (LTP) of cortical synapses may play important roles in chronic pain and anxiety. In addition to NMDA and AMPA receptors, kainate (KA) receptors have been found to play roles in synaptic transmission, regulation and presynaptic forms of LTP. In this brief review, I will summarize the new progress made on KA receptors, and propose that ACC synapses may provide a good synaptic model for understanding cortical mechanism for behavioral anxiety, and its related emotional disorders.

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Pain and emotion interactions in subregions of the cingulate gyrus.

Brent Vogt (2005)

Acute pain and emotion are processed in two forebrain networks, and the cingulate cortex is involved in both. Although Brodmann's cingulate gyrus had two divisions and was not based on any functional criteria, functional imaging studies still use this model. However, recent cytoarchitectural studies of the cingulate gyrus support a four-region model, with subregions, that is based on connections and qualitatively unique functions. Although the activity evoked by pain and emotion has been widely reported, some view them as emergent products of the brain rather than of small aggregates of neurons. Here, we assess pain and emotion in each cingulate subregion, and assess whether pain is co-localized with negative affect. Amazingly, these activation patterns do not simply overlap.

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Synaptic plasticity in the anterior cingulate cortex in acute and chronic pain.

Tim Bliss, Graham L. Collingridge, Bong-Kiun Kaang … (2016)

The anterior cingulate cortex (ACC) is activated in both acute and chronic pain. In this Review, we discuss increasing evidence from rodent studies that ACC activation contributes to chronic pain states and describe several forms of synaptic plasticity that may underlie this effect. In particular, one form of long-term potentiation (LTP) in the ACC, which is triggered by the activation of NMDA receptors and expressed by an increase in AMPA-receptor function, sustains the affective component of the pain state. Another form of LTP in the ACC, which is triggered by the activation of kainate receptors and expressed by an increase in glutamate release, may contribute to pain-related anxiety.

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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 … (2015)

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 and article information

Contributors

Min Zhuo: 416-978-4018 , min.zhuo@utoronto.ca

Journal

Journal ID (nlm-ta): Mol Brain

Journal ID (iso-abbrev): Mol Brain

Title: Molecular Brain

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-6606

Publication date (Electronic): 18 May 2017

Publication date PMC-release: 18 May 2017

Publication date Collection: 2017

Volume: 10

Electronic Location Identifier: 16

Affiliations

[1 ]ISNI 0000 0001 0599 1243, GRID grid.43169.39, Center for Neuron and Disease, Frontier Institutes of Science and Technology, , Xi’an Jiaotong University, ; Xi’an, Shanxi 710049 China

[2 ]ISNI 0000 0001 2157 2938, GRID grid.17063.33, Department of Physiology, Faculty of Medicine, , University of Toronto, Medical Science Building, ; Room #3342, 1 King’s College Circle, Toronto, ON M5S 1A8 Canada

Article

Publisher ID: 297

DOI: 10.1186/s13041-017-0297-8

PMC ID: 5437545

PubMed ID: 28521778

SO-VID: 3e5640dc-e13e-47a8-b89e-f63c7d232eda

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 7 February 2017

Date accepted : 10 May 2017

Funding

Funded by: CIHR

Award ID: 148648

Award Recipient : Min Zhuo

Funded by: EJLB foundation

Award ID: none

Award Recipient : Min Zhuo

Funded by: FundRef http://dx.doi.org/10.13039/501100002784, Canada Excellence Research Chairs, Government of Canada;

Award ID: none

Award Recipient : Min Zhuo

Funded by: FundRef http://dx.doi.org/10.13039/100009408, Fondation Brain Canada;

Award ID: none

Award Recipient : Min Zhuo

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ScienceOpen disciplines: Neurosciences

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Cortical kainate receptors and behavioral anxiety

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Most cited references 41

Pain and emotion interactions in subregions of the cingulate gyrus.

Synaptic plasticity in the anterior cingulate cortex in acute and chronic pain.

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

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