Activation of brain‐derived neurotrophic factor signaling in the basal forebrain reverses acute sleep deprivation‐induced fear memory impairments

Introduction The mechanisms underlying sleep deprivation‐induced memory impairments and relevant compensatory signaling pathways remain elusive. We tested the hypothesis that increased brain‐derived neurotrophic factor (BDNF) expression in the basal forebrain following acute sleep deprivation was a...

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Vydáno v:Brain and behavior Ročník 10; číslo 4; s. e01592 - n/a
Hlavní autoři: Ma, Tao, Zhang, Hao, Xu, Zhi‐Peng, Lu, Yan, Fu, Qiang, Wang, Wei, Li, Guan‐Hua, Wang, Ying‐Ying, Yang, Yi‐Tian, Mi, Wei‐Dong
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States John Wiley & Sons, Inc 01.04.2020
John Wiley and Sons Inc
Wiley
Témata:
Animals
Azepines - pharmacology
Azepines - therapeutic use
basal forebrain
Basal Forebrain - drug effects
Basal Forebrain - metabolism
Benzamides - pharmacology
Benzamides - therapeutic use
Brain research
Brain-derived neurotrophic factor
Brain-Derived Neurotrophic Factor - pharmacology
Brain-Derived Neurotrophic Factor - therapeutic use
Experiments
Eye movements
Fear - physiology
fear memory
Kinases
Laboratory animals
Male
Medical research
Memory
Memory Disorders - drug therapy
Memory Disorders - etiology
Memory Disorders - metabolism
Original Research
Phosphorylation - drug effects
Rats
Rats, Wistar
Receptor, trkB - antagonists & inhibitors
Receptor, trkB - metabolism
Signal Transduction - drug effects
Signal Transduction - physiology
Sleep - physiology
Sleep deprivation
Sleep Deprivation - complications
Sleep Deprivation - metabolism
Surgery
Treatment Outcome
China
sleep deprivation
brain-derived neurotrophic factor
fear memory
basal forebrain
ISSN:2162-3279, 2162-3279
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Shrnutí:Introduction The mechanisms underlying sleep deprivation‐induced memory impairments and relevant compensatory signaling pathways remain elusive. We tested the hypothesis that increased brain‐derived neurotrophic factor (BDNF) expression in the basal forebrain following acute sleep deprivation was a compensatory mechanism to maintain fear memory performance. Methods Adult male Wistar rats were deprived of 6‐hr total sleep from the beginning of the light cycle. The effects of sleep deprivation on BDNF protein expression and activation of downstream tropomyosin receptor kinase B (TrkB)/phospholipase C‐γ1 (PLCγ1) signaling in the basal forebrain and fear memory consolidation were examined. BDNF or selective downstream TrkB receptor antagonist ANA‐12 was further injected into the basal forebrain bilaterally to observe the changes in fear memory consolidation in response to modulation of the BDNF/TrkB signaling. Results Six hours of sleep deprivation‐induced both short‐ and long‐term fear memory impairments. Increased BDNF protein expression and TrkB and PLCγ1 phosphorylation in the basal forebrain were observed after sleep deprivation. Microinjection of BDNF into the basal forebrain partly reversed fear memory deficits caused by sleep deprivation, which were accompanied by increased BDNF protein levels and TrkB/PLCγ1 activation. After ANA‐12 microinjection, sleep deprivation‐induced activation of the BDNF/TrkB pathway was inhibited and impairments of fear memory consolidation were further aggravated. Conclusions Acute sleep deprivation induces compensatory increase of BDNF expression in the basal forebrain. Microinjection of BDNF into the basal forebrain mitigates the fear memory impairments caused by sleep deprivation by activating TrkB/PLCγ1 signaling. We found that acute sleep deprivation could increase BDNF protein expression and downstream TrkB/PLCγ1 activation robustly in the basal forebrain area. Microinjection of BDNF into basal forebrain could further activate TrkB/PLCγ1 signaling and reverse the decline in fear memory consolidation. Moreover, microinjection of TrkB receptor antagonist ANA‐12 could aggravate sleep deprivation‐induced memory impairments.
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Tao Ma and Hao Zhang contributed equally to this work.
The peer review history for this article is available at https://publons.com/publon/10.1002/brb3.1592
ISSN:2162-3279
2162-3279
DOI:10.1002/brb3.1592