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Research Articles, Behavioral/Cognitive

Sustained Activity of Hippocampal Parvalbumin-Expressing Interneurons Supports Trace Eyeblink Conditioning in Mice

Rongrong Li, Weiwei Zhang, Jie Zhang, Haibo Zhang, Hui Chen, Zhian Hu, Zhongxiang Yao, Hao Chen and Bo Hu
Journal of Neuroscience 2 November 2022, 42 (44) 8343-8360; DOI: https://doi.org/10.1523/JNEUROSCI.0834-22.2022
Rongrong Li
1Department of Physiology, College of Basic Medical Sciences, Army Medical University, Chongqing 400038, China
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Weiwei Zhang
1Department of Physiology, College of Basic Medical Sciences, Army Medical University, Chongqing 400038, China
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  • ORCID record for Weiwei Zhang
Jie Zhang
1Department of Physiology, College of Basic Medical Sciences, Army Medical University, Chongqing 400038, China
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Haibo Zhang
1Department of Physiology, College of Basic Medical Sciences, Army Medical University, Chongqing 400038, China
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Hui Chen
1Department of Physiology, College of Basic Medical Sciences, Army Medical University, Chongqing 400038, China
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Zhian Hu
1Department of Physiology, College of Basic Medical Sciences, Army Medical University, Chongqing 400038, China
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Zhongxiang Yao
1Department of Physiology, College of Basic Medical Sciences, Army Medical University, Chongqing 400038, China
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Hao Chen
2Experimental Center of Basic Medicine, College of Basic Medical Sciences, Army Medical University, Chongqing 400038, China
3Brain and Intelligence Research Key Laboratory of Chongqing Education Commission, Army Medical University, Chongqing 400038, China
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Bo Hu
1Department of Physiology, College of Basic Medical Sciences, Army Medical University, Chongqing 400038, China
3Brain and Intelligence Research Key Laboratory of Chongqing Education Commission, Army Medical University, Chongqing 400038, China
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Abstract

Although recent studies have revealed an involvement of hippocampal interneurons in learning the association among time-separated events, its underlying cellular mechanisms remained not fully clarified. Here, we combined multichannel recording and optogenetics to elucidate how the hippocampal parvalbumin-expressing interneurons (PV-INs) support associative learning. To address this issue, we trained the mice (both sexes) to learn hippocampus-dependent trace eyeblink conditioning (tEBC) in which they associated a light flash conditioned stimulus (CS) with a corneal air puff unconditioned stimuli (US) separated by a 250 ms time interval. We found that the hippocampal PV-INs exhibited learning-associated sustained activity at the early stage of tEBC acquisition. Moreover, the PV-IN sustained activity was positively correlated with the occurrence of conditioned eyeblink responses at the early learning stage. Suppression of the PV-IN sustained activity impaired the acquisition of tEBC, whereas the PV-IN activity suppression had no effect on the acquisition of delay eyeblink conditioning, a hippocampus-independent learning task. Learning-associated augmentation in the excitatory pyramidal cell-to-PVIN drive may contribute to the formation of PV-IN sustained activity. Suppression of the PV-IN sustained activity disrupted hippocampal gamma but not theta band oscillation during the CS-US interval period. Gamma frequency (40 Hz) activation of the PV-INs during the CS-US interval period facilitated the acquisition of tEBC. Our current findings highlight the involvement of hippocampal PV-INs in tEBC acquisition and reveal insights into the PV-IN activity kinetics which are of key importance for the hippocampal involvement in associative learning.

SIGNIFICANCE STATEMENT The cellular mechanisms underlying associative learning have not been fully clarified. Previous studies focused on the involvement of hippocampal pyramidal cells in associative learning, whereas the activity and function of hippocampal interneurons were largely neglected. We herein demonstrated the hippocampal PV-INs exhibited learning-associated sustained activity, which was required for the acquisition of tEBC. Furthermore, we showed evidence that the PV-IN sustained activity might have arisen from the learning-associated augmentation in excitatory pyramidal cell-to-PVIN drive and contributed to learning-associated augmentation in gamma band oscillation during tEBC acquisition. Our findings provide more mechanistic understanding of the cellular mechanisms underlying the hippocampal involvement in associative learning.

  • associative learning
  • hippocampus
  • interneuron
  • mouse
  • multichannel recording
  • trace conditioning

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The Journal of Neuroscience: 42 (44)
Journal of Neuroscience
Vol. 42, Issue 44
2 Nov 2022
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Sustained Activity of Hippocampal Parvalbumin-Expressing Interneurons Supports Trace Eyeblink Conditioning in Mice
Rongrong Li, Weiwei Zhang, Jie Zhang, Haibo Zhang, Hui Chen, Zhian Hu, Zhongxiang Yao, Hao Chen, Bo Hu
Journal of Neuroscience 2 November 2022, 42 (44) 8343-8360; DOI: 10.1523/JNEUROSCI.0834-22.2022

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Sustained Activity of Hippocampal Parvalbumin-Expressing Interneurons Supports Trace Eyeblink Conditioning in Mice
Rongrong Li, Weiwei Zhang, Jie Zhang, Haibo Zhang, Hui Chen, Zhian Hu, Zhongxiang Yao, Hao Chen, Bo Hu
Journal of Neuroscience 2 November 2022, 42 (44) 8343-8360; DOI: 10.1523/JNEUROSCI.0834-22.2022
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Keywords

  • associative learning
  • hippocampus
  • interneuron
  • mouse
  • multichannel recording
  • trace conditioning

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