Dorsolateral Striatal proBDNF Improves Reversal Learning by Enhancing Coordination of Neural Activity in Rats
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Dorsolateral Striatal proBDNF Improves Reversal Learning by Enhancing Coordination of Neural Activity in Rats Wei Sun 1 & Hongxia Che 1,2 & Jia Li 2 & Dongxin Tang 1 & Xiaoyun Liu 3 & Wenhui Liu 3 & Lei An 1,2,3,4 Received: 18 March 2020 / Accepted: 30 July 2020 # Springer Science+Business Media, LLC, part of Springer Nature 2020
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. Keywords Dorsolateral striatum . Infralimbic cortex . Reversal learning . Neural activity . proBDNF
Introduction The dorsolateral striatum (DLS) of the mammalian brain has been implicated in initial acquisition and retrieval of habit memory [1, 2]. For example, lesions or inactivation of the DLS prevents the development of outcome-impervious habit behavior in a rat lever-press operant task [3, 4], which Electronic supplementary material The online version of this article (https://doi.org/10.1007/s12035-020-02051-9) contains supplementary material, which is available to authorized users. * Lei An [email protected]; [email protected] 1
Behavioral Neuroscience Laboratory, The First Affiliated Hospital of Guizhou University of Traditional Chinese Medicine, Guiyang 550001, China
2
College of Acupuncture-Moxibustion and Orthopedics, Guizhou University of Traditional Chinese Medicine, Guiyang 550025, China
3
Department of Neurology, Jinan Hospital, Jinan 250013, China
4
Department of Physiology, University of Saskatchewan, Saskatoon S7N 5E5, Canada
indicates that DLS is associated with stereotyped habit-like behavior [5, 6]. This view is
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