Tactile modulation of memory and anxiety requires dentate granule cells along the dorsoventral axis

Chi Wang, Hui Liu, Kun Li, Zhen-Zhen Wu, Chen Wu, Jing-Ying Yu, Qian Gong, Ping Fang, Xing-Xing Wang, Shu-Min Duan, Hao Wang, Yan Gu, Ji Hu, Bing-Xing Pan, Mathias V. Schmidt, Yi-Jun Liu and Xiao-Dong Wang ()
Additional contact information
Chi Wang: Zhejiang University School of Medicine
Hui Liu: Zhejiang University School of Medicine
Kun Li: Zhejiang University School of Medicine
Zhen-Zhen Wu: Zhejiang University School of Medicine
Chen Wu: Zhejiang University School of Medicine
Jing-Ying Yu: Zhejiang University School of Medicine
Qian Gong: Zhejiang University School of Medicine
Ping Fang: Zhejiang University School of Medicine
Xing-Xing Wang: Technische Universität München/Klinikum Rechts der Isar
Shu-Min Duan: NHC and CAMS Key Laboratory of Medical Neurobiology, MOE Frontier Science Center for Brain Research and Brain-Machine Integration, School of Brain Science and Brain Medicine, Zhejiang University
Hao Wang: NHC and CAMS Key Laboratory of Medical Neurobiology, MOE Frontier Science Center for Brain Research and Brain-Machine Integration, School of Brain Science and Brain Medicine, Zhejiang University
Yan Gu: Center of Stem Cell and Regenerative Medicine, and Department of Neurology of the Second Affiliated Hospital, Zhejiang University School of Medicine
Ji Hu: ShanghaiTech University
Bing-Xing Pan: Laboratory of Fear and Anxiety Disorders, Institute of Life Science, Nanchang University
Mathias V. Schmidt: Max Planck Institute of Psychiatry
Yi-Jun Liu: Zhejiang University School of Medicine
Xiao-Dong Wang: Zhejiang University School of Medicine

Nature Communications, 2020, vol. 11, issue 1, 1-18

Abstract: Abstract Touch can positively influence cognition and emotion, but the underlying mechanisms remain unclear. Here, we report that tactile experience enrichment improves memory and alleviates anxiety by remodeling neurons along the dorsoventral axis of the dentate gyrus (DG) in adult mice. Tactile enrichment induces differential activation and structural modification of neurons in the dorsal and ventral DG, and increases the presynaptic input from the lateral entorhinal cortex (LEC), which is reciprocally connected with the primary somatosensory cortex (S1), to tactile experience-activated DG neurons. Chemogenetic activation of tactile experience-tagged dorsal and ventral DG neurons enhances memory and reduces anxiety respectively, whereas inactivation of these neurons or S1-innervated LEC neurons abolishes the beneficial effects of tactile enrichment. Moreover, adulthood tactile enrichment attenuates early-life stress-induced memory deficits and anxiety-related behavior. Our findings demonstrate that enriched tactile experience retunes the pathway from S1 to DG and enhances DG neuronal plasticity to modulate cognition and emotion.

Date: 2020
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DOI: 10.1038/s41467-020-19874-8

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