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Dorsolateral Striatal proBDNF Improves Reversal Learning by Enhancing Coordination of Neural Activity in Rats

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Abstract

Behavioral flexibility allows individuals to adapt to situations in which rewards and goals change. The dorsolateral striatum (DLS) is part of corticostriatal circuits that is involved in flexible behavior. Pro-brain-derived neurotrophic factor (proBDNF) can enhance fear memory extinction and weaken synaptic transmission, which may enable flexible adaptations. However, the role of proBDNF in cognitive flexibility is unclear. Here, through infusion of cleavage-resistant proBDNF or its antibody into the DLS of rats, we sought evidence for the influences by employing behavioral tests, immunoblotting, immunocytochemistry, and electrophysiological recoding. Infusion of proBDNF significantly facilitated reversal learning while inhibiting DLS proBDNF by anti-proBDNF antibody impaired the behavioral performance. Furthermore, elevation of DLS proBDNF facilitated neural correlate with reversal performance while blocking proBDNF expression decayed the spike-field coupling during the correct turning. Reversal learning induced increases in endogenous neuronal proBDNF, with a strong correlation between DLS and infralimbic cortex (IL), but not prelimbic cortex (PL) or sensory-motor cortex (SM). Importantly, blockade of IL proBDNF disrupted the DLS-mediated reversal learning enhancement, implying the involvement of both IL and DLS regions in reversal habitual behavior. Taken together, our findings provide first evidence for the essential role of the DLS proBDNF in cognitive flexibility and suggest that proBDNF-mediated neural function could be the mechanism.

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Acknowledgments

We thank Dr. Sara Khalaj for her valuable comments on the revised version of the manuscript. We also thank Dr. Xiaoliang Li, Dr. Xuan Zhang, Miss Weiwei Feng, Dr. Yang Hu, and Dongguo Xiao for their help in preparation of the revision.

Funding

This work was supported by Grants from the National Natural Science Foundation of China 31700929 to LA.

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Authors and Affiliations

  1. Behavioral Neuroscience Laboratory, The First Affiliated Hospital of Guizhou University of Traditional Chinese Medicine, Guiyang, 550001, China

    Wei Sun, Hongxia Che, Dongxin Tang & Lei An

  2. College of Acupuncture-Moxibustion and Orthopedics, Guizhou University of Traditional Chinese Medicine, Guiyang, 550025, China

    Hongxia Che, Jia Li & Lei An

  3. Department of Neurology, Jinan Hospital, Jinan, 250013, China

    Xiaoyun Liu, Wenhui Liu & Lei An

  4. Department of Physiology, University of Saskatchewan, Saskatoon, S7N 5E5, Canada

    Lei An

Authors
  1. Wei Sun
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  2. Hongxia Che
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  3. Jia Li
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  4. Dongxin Tang
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  5. Xiaoyun Liu
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  6. Wenhui Liu
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  7. Lei An
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Contributions

Conceived and designed the experiments: WS JL, DXT, and LA; performed the experiments: WS, HXC, XYL, and WHL; analyzed the data: WS, JL, and LA; wrote the manuscript: WS, DXT, and LA.

Corresponding author

Correspondence to Lei An.

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Conflict of Interest

The authors declare that they have no competing interests.

Ethics Statement

All animal experiments and procedures were reviewed and approved by the Experimental Animal Care Committee of Guizhou University of Traditional Chinese Medicine (SCXK-2013-0020).

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Sun, W., Che, H., Li, J. et al. Dorsolateral Striatal proBDNF Improves Reversal Learning by Enhancing Coordination of Neural Activity in Rats. Mol Neurobiol 57, 4642–4656 (2020). https://doi.org/10.1007/s12035-020-02051-9

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