Program in Neurobiology and Behavior, University of Washington, Seattle, WA 98195, USA.
Proc Natl Acad Sci U S A. 2012 Feb 7;109(6):E368-77. doi: 10.1073/pnas.1115729109. Epub 2012 Jan 5.
Na(V)1.1 is the primary voltage-gated Na(+) channel in several classes of GABAergic interneurons, and its reduced activity leads to reduced excitability and decreased GABAergic tone. Here, we show that Na(V)1.1 channels are expressed in the suprachiasmatic nucleus (SCN) of the hypothalamus. Mice carrying a heterozygous loss of function mutation in the Scn1a gene (Scn1a(+/-)), which encodes the pore-forming α-subunit of the Na(V)1.1 channel, have longer circadian period than WT mice and lack light-induced phase shifts. In contrast, Scn1a(+/-) mice have exaggerated light-induced negative-masking behavior and normal electroretinogram, suggesting an intact retina light response. Scn1a(+/-) mice show normal light induction of c-Fos and mPer1 mRNA in ventral SCN but impaired gene expression responses in dorsal SCN. Electrical stimulation of the optic chiasm elicits reduced calcium transients and impaired ventro-dorsal communication in SCN neurons from Scn1a(+/-) mice, and this communication is barely detectable in the homozygous gene KO (Scn1a(-/-)). Enhancement of GABAergic transmission with tiagabine plus clonazepam partially rescues the effects of deletion of Na(V)1.1 on circadian period and phase shifting. Our report demonstrates that a specific voltage-gated Na(+) channel and its associated impairment of SCN interneuronal communication lead to major deficits in the function of the master circadian pacemaker. Heterozygous loss of Na(V)1.1 channels is the underlying cause for severe myoclonic epilepsy of infancy; the circadian deficits that we report may contribute to sleep disorders in severe myoclonic epilepsy of infancy patients.
Nav1.1 是几种 GABA 能中间神经元的主要电压门控 Na(+)通道,其活性降低会导致兴奋性降低和 GABA 能张力降低。在这里,我们表明 Nav1.1 通道在下丘脑的视交叉上核(SCN)中表达。携带 Scn1a 基因(Scn1a(+/-))杂合功能丧失突变的小鼠,该基因编码 Nav1.1 通道的孔形成α亚基,其昼夜节律周期长于 WT 小鼠,并且缺乏光诱导的相位移动。相比之下,Scn1a(+/-)小鼠具有夸大的光诱导负掩蔽行为和正常的视网膜电图,表明视网膜光反应完整。Scn1a(+/-)小鼠在 SCN 的腹侧显示正常的光诱导 c-Fos 和 mPer1 mRNA,但在 SCN 的背侧显示基因表达反应受损。光刺激视交叉会引起 Scn1a(+/-)小鼠 SCN 神经元中的钙瞬变减少和腹侧-背侧通讯受损,而在纯合基因 KO(Scn1a(-/-))中几乎检测不到这种通讯。用噻加宾加氯硝西泮增强 GABA 能传递可部分挽救 Nav1.1 缺失对昼夜节律周期和相位移动的影响。我们的报告表明,特定的电压门控 Na(+)通道及其相关的 SCN 中间神经元通讯受损导致主生物钟起搏器功能的主要缺陷。Nav1.1 通道的杂合缺失是婴儿严重肌阵挛性癫痫的潜在原因;我们报告的昼夜节律缺陷可能导致严重肌阵挛性癫痫患者的睡眠障碍。