Experimental febrile seizures induce age-dependent structural plasticity and improve memory in mice
Highlights • Early-stage febrile seizures improved dentate granule cell-mediated memory. • Increased mossy fiber synapses after febrile seizures underlay memory enhancement. • Late-stage febrile seizures attenuated memory enhancement via granule cell ectopia. • Abolishment of the ectopic granule cel...
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| Published in | Neuroscience Vol. 318; pp. 34 - 44 |
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| Main Authors | , , , , |
| Format | Journal Article |
| Language | English |
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Elsevier Ltd
24.03.2016
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| Abstract | Highlights • Early-stage febrile seizures improved dentate granule cell-mediated memory. • Increased mossy fiber synapses after febrile seizures underlay memory enhancement. • Late-stage febrile seizures attenuated memory enhancement via granule cell ectopia. • Abolishment of the ectopic granule cells rescued memory enhancement. |
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| AbstractList | Population-based studies have demonstrated that children with a history of febrile seizure (FS) perform better than age-matched controls at hippocampus-dependent memory tasks. Here, we report that FSs induce two distinct structural reorganizations in the hippocampus and bidirectionally modify future learning abilities in an age-dependent manner. Compared with age-matched controls, adult mice that had experienced experimental FSs induced by hyperthermia (HT) on postnatal day 14 (P14-HT) performed better in a cognitive task that requires dentate granule cells (DGCs). The enhanced memory performance correlated with an FS-induced persistent increase in the density of large mossy fiber terminals (LMTs) of the DGCs. The memory enhancement was not observed in mice that had experienced HT-induced seizures at P11 which exhibited abnormally located DGCs in addition to the increased LMT density. The ectopic DGCs of the P11-HT mice were abolished by the diuretic bumetanide, and this pharmacological treatment unveiled the masked memory enhancement. Thus, this work provides a novel basis for age-dependent structural plasticity in which FSs influence future brain function. •Early-stage febrile seizures improved dentate granule cell-mediated memory.•Increased mossy fiber synapses after febrile seizures underlay memory enhancement.•Late-stage febrile seizures attenuated memory enhancement via granule cell ectopia.•Abolishment of the ectopic granule cells rescued memory enhancement. Population-based studies have demonstrated that children with a history of febrile seizure (FS) perform better than age-matched controls at hippocampus-dependent memory tasks. Here, we report that FSs induce two distinct structural reorganizations in the hippocampus and bidirectionally modify future learning abilities in an age-dependent manner. Compared with age-matched controls, adult mice that had experienced experimental FSs induced by hyperthermia (HT) on postnatal day 14 (P14-HT) performed better in a cognitive task that requires dentate granule cells (DGCs). The enhanced memory performance correlated with an FS-induced persistent increase in the density of large mossy fiber terminals (LMTs) of the DGCs. The memory enhancement was not observed in mice that had experienced HT-induced seizures at P11 which exhibited abnormally located DGCs in addition to the increased LMT density. The ectopic DGCs of the P11-HT mice were abolished by the diuretic bumetanide, and this pharmacological treatment unveiled the masked memory enhancement. Thus, this work provides a novel basis for age-dependent structural plasticity in which FSs influence future brain function. Highlights • Early-stage febrile seizures improved dentate granule cell-mediated memory. • Increased mossy fiber synapses after febrile seizures underlay memory enhancement. • Late-stage febrile seizures attenuated memory enhancement via granule cell ectopia. • Abolishment of the ectopic granule cells rescued memory enhancement. |
| Author | Ikegaya, Y Ichikawa, J Tao, K Koyama, R Matsuki, N |
| Author_xml | – sequence: 1 fullname: Tao, K – sequence: 2 fullname: Ichikawa, J – sequence: 3 fullname: Matsuki, N – sequence: 4 fullname: Ikegaya, Y – sequence: 5 fullname: Koyama, R |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26794590$$D View this record in MEDLINE/PubMed |
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| Keywords | DG LMTs memory phosphate buffer DGCs HT Trk FS minimal essential medium analyses of variance ANOVA ZnT3 brain-derived neurotrophic factor protein kinase A dentate granule cells 4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid hyperthermia hippocampus BDNF PKA large mossy fiber terminals Hanks’ balanced salt solution tropomyosin receptor kinase structural plasticity dentate gyrus PB MEM HEPES HBSS febrile seizure zinc transporter 3 |
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fullname: Williams |
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| Snippet | Highlights • Early-stage febrile seizures improved dentate granule cell-mediated memory. • Increased mossy fiber synapses after febrile seizures underlay... •Early-stage febrile seizures improved dentate granule cell-mediated memory.•Increased mossy fiber synapses after febrile seizures underlay memory... Population-based studies have demonstrated that children with a history of febrile seizure (FS) perform better than age-matched controls at... |
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| SubjectTerms | Aging Animals Bumetanide - metabolism dentate gyrus Disease Models, Animal febrile seizure Fever - complications hippocampus Hippocampus - metabolism Hippocampus - physiopathology memory Memory - physiology Mice Neurogenesis - physiology Neurology Neuronal Plasticity - physiology Seizures - etiology Seizures - metabolism Seizures - physiopathology structural plasticity |
| Title | Experimental febrile seizures induce age-dependent structural plasticity and improve memory in mice |
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