Liu Shaolin, Shao Zuoyi, Puche Adam, Wachowiak Matt, Rothermel Markus, Shipley Michael T
Department of Anatomy & Neurobiology and Program in Neuroscience, University of Maryland School of Medicine, Baltimore, Maryland 21201, and
Department of Anatomy & Neurobiology and Program in Neuroscience, University of Maryland School of Medicine, Baltimore, Maryland 21201, and.
J Neurosci. 2015 Apr 8;35(14):5680-92. doi: 10.1523/JNEUROSCI.4953-14.2015.
Cholinergic [acetylcholine (ACh)] axons from the basal forebrain innervate olfactory bulb glomeruli, the initial site of synaptic integration in the olfactory system. Both nicotinic acetylcholine receptors (nAChRs) and muscarinic acetylcholine receptors (mAChRs) are expressed in glomeruli. The activation of nAChRs directly excites both mitral/tufted cells (MTCs) and external tufted cells (ETCs), the two major excitatory neurons that transmit glomerular output. The functional roles of mAChRs in glomerular circuits are unknown. We show that the restricted glomerular application of ACh causes rapid, brief nAChR-mediated excitation of both MTCs and ETCs in the mouse olfactory bulb. This excitation is followed by mAChR-mediated inhibition, which is blocked by GABAA receptor antagonists, indicating the engagement of periglomerular cells (PGCs) and/or short axon cells (SACs), the two major glomerular inhibitory neurons. Indeed, selective activation of glomerular mAChRs, with ionotropic GluRs and nAChRs blocked, increased IPSCs in MTCs and ETCs, indicating that mAChRs recruit glomerular inhibitory circuits. Selective activation of glomerular mAChRs in the presence of tetrodotoxin increased IPSCs in all glomerular neurons, indicating action potential-independent enhancement of GABA release from PGC and/or SAC dendrodendritic synapses. mAChR-mediated enhancement of GABA release also presynaptically suppressed the first synapse of the olfactory system via GABAB receptors on sensory terminals. Together, these results indicate that cholinergic modulation of glomerular circuits is biphasic, involving an initial excitation of MTC/ETCs mediated by nAChRs followed by inhibition mediated directly by mAChRs on PGCs/SACs. This may phasically enhance the sensitivity of glomerular outputs to odorants, an action that is consistent with recent in vivo findings.
来自基底前脑的胆碱能[乙酰胆碱(ACh)]轴突支配嗅球小球,这是嗅觉系统中突触整合的起始部位。烟碱型乙酰胆碱受体(nAChRs)和毒蕈碱型乙酰胆碱受体(mAChRs)在小球中均有表达。nAChRs的激活直接兴奋了传递小球输出的两种主要兴奋性神经元——二尖瓣/簇状细胞(MTCs)和外侧簇状细胞(ETCs)。mAChRs在小球回路中的功能作用尚不清楚。我们发现,在小鼠嗅球中,向小球局部施加ACh会导致由nAChRs介导的MTCs和ETCs快速、短暂的兴奋。这种兴奋之后是由mAChRs介导的抑制,该抑制被GABAA受体拮抗剂阻断,表明球周细胞(PGCs)和/或短轴突细胞(SACs)这两种主要的小球抑制性神经元参与其中。实际上,在离子型谷氨酸受体(GluRs)和nAChRs被阻断的情况下,选择性激活小球mAChRs会增加MTCs和ETCs中的抑制性突触后电流(IPSCs),这表明mAChRs激活了小球抑制性回路。在存在河豚毒素的情况下选择性激活小球mAChRs会增加所有小球神经元中的IPSCs,这表明PGCs和/或SAC树-树突触释放GABA的过程与动作电位无关,且mAChRs可增强这一过程。mAChR介导的GABA释放增强还通过感觉末梢上的GABAB受体对嗅觉系统的第一个突触进行突触前抑制。总之,这些结果表明胆碱能对小球回路的调节是双相的,包括由nAChRs介导的MTCs/ETCs的初始兴奋,随后是由PGCs/SACs上的mAChRs直接介导的抑制。这可能会阶段性地增强小球输出对气味剂的敏感性,这一作用与最近的体内研究结果一致。