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New Research, Cognition and Behavior

Developing of focal ischemia in the hippocampus or the amygdala reveals a regional compensation rule for fear memory acquisition

Cheng-Long Yu, Jin-Nan Li, Ping Gan, Li-Ping Wang, Yue-Xiong Yang, Da-Fu Yu, Rong-Rong Mao, Fu-Qiang Xu, Qi-Xin Zhou, Gal Richter-Levin, Lin Xu and Heng Zhou
eNeuro 30 March 2021, ENEURO.0398-20.2021; DOI: https://doi.org/10.1523/ENEURO.0398-20.2021
Cheng-Long Yu
1Kunming Institute of Zoology and Key Laboratory of Animal Models and Human Disease Mechanisms, CAS, Kunming, China
7the Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences
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Jin-Nan Li
1Kunming Institute of Zoology and Key Laboratory of Animal Models and Human Disease Mechanisms, CAS, Kunming, China
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Ping Gan
2Department of Biochemistry and Molecular Biology, College of Basic Medicine, Kunming Medical University, China
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Li-Ping Wang
1Kunming Institute of Zoology and Key Laboratory of Animal Models and Human Disease Mechanisms, CAS, Kunming, China
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Yue-Xiong Yang
1Kunming Institute of Zoology and Key Laboratory of Animal Models and Human Disease Mechanisms, CAS, Kunming, China
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Da-Fu Yu
3Department of Nuclear Medicine, First People’s Hospital of Yunnan Province, and Key Laboratory of Medical Imaging, Kunming University of Science and Technology, Kunming, China
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Rong-Rong Mao
1Kunming Institute of Zoology and Key Laboratory of Animal Models and Human Disease Mechanisms, CAS, Kunming, China
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Fu-Qiang Xu
4Wuhan Institute of Physics and Mathematics, CAS, Wuhan, 430071, China
7the Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences
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Qi-Xin Zhou
1Kunming Institute of Zoology and Key Laboratory of Animal Models and Human Disease Mechanisms, CAS, Kunming, China
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Gal Richter-Levin
5Department of Neurobiology and Ethology, and Department of Psychology, University of Haifa, Haifa, Israel
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Lin Xu
1Kunming Institute of Zoology and Key Laboratory of Animal Models and Human Disease Mechanisms, CAS, Kunming, China
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Heng Zhou
1Kunming Institute of Zoology and Key Laboratory of Animal Models and Human Disease Mechanisms, CAS, Kunming, China
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Abstract

Circuit compensation is often observed in patients with acute ischemic stroke, suggesting the importance of the interaction between brain regions. Also, contextual fear memory is an association between multisensory contexts and fearful stimuli, for which the interaction between the hippocampus and the amygdala is believed to be critical. To understand how focal ischemia in one region could influence the other region, we used a modified photo-thrombosis to induce focal ischemia in the hippocampus or the amygdala or both in freely-moving rats. We found that the learning curve and short-term memory were not affected in the rats although focal ischemia was induced 5 hrs before learning in either the hippocampus or the amygdala; these were impaired by the induction of ischemia in both the regions. Furthermore, the learning curve and short-term memory were impaired when ischemia was induced 24 hrs before learning in either the hippocampus or the amygdala when the synaptic transmission was altered in one region due to ischemia in the other region. These results suggest that the circuit compensation between the hippocampus and the amygdala is critical for fear memory acquisition.

Significance Statement

Contextual fear memory needs the interconnection between the hippocampus and the amygdala. However, it is unclear whether and how the two regions produce circuit compensation under an ischemic situation. Here, we employed the developing of ischemia in the hippocampus or the amygdala or both in freely moving rats. We found that memory acquisition was not affected 5 hrs post-ischemia, but it was impaired 24 hrs post-ischemia when the synaptic transmission was impaired in one region due to ischemia in the other region. Furthermore, ischemia in both brain regions impaired memory acquisition. These results indicate a circuit compensation between the hippocampus and the amygdala in memory acquisition if one with ischemia does not affect the function of the other.

  • Amygdala
  • Circuits
  • Fear memory
  • Hippocampus
  • Ishcemia

Footnotes

  • The authors declare no competing interests.

  • This study was supported by the Natural Science Foundation of China (31100775 and 31371141 to Q.X.Z., U15022058 to L.X., 31860272 to P.G., and 31861143037 to both L.X. and G.R.-L.), and Strategic Priority Research Program of the Chinese Academy of Sciences (XDB32020000 to L.X.), and Department of Science and Technology Program of Yunnan Province (2016HA002 to L.X.), and External Cooperation Program BIC of the Chinese Academy of Sciences (GJHZ1549 to G.R.-L.), and Youth Innovation Promotion Association of the Chinese Academy of Sciences (2013250 to Q.X.Z.).

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Developing of focal ischemia in the hippocampus or the amygdala reveals a regional compensation rule for fear memory acquisition
Cheng-Long Yu, Jin-Nan Li, Ping Gan, Li-Ping Wang, Yue-Xiong Yang, Da-Fu Yu, Rong-Rong Mao, Fu-Qiang Xu, Qi-Xin Zhou, Gal Richter-Levin, Lin Xu, Heng Zhou
eNeuro 30 March 2021, ENEURO.0398-20.2021; DOI: 10.1523/ENEURO.0398-20.2021

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Developing of focal ischemia in the hippocampus or the amygdala reveals a regional compensation rule for fear memory acquisition
Cheng-Long Yu, Jin-Nan Li, Ping Gan, Li-Ping Wang, Yue-Xiong Yang, Da-Fu Yu, Rong-Rong Mao, Fu-Qiang Xu, Qi-Xin Zhou, Gal Richter-Levin, Lin Xu, Heng Zhou
eNeuro 30 March 2021, ENEURO.0398-20.2021; DOI: 10.1523/ENEURO.0398-20.2021
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Keywords

  • Amygdala
  • Circuits
  • Fear memory
  • hippocampus
  • Ishcemia

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