Flight motor networks modulate primary olfactory processing in the moth Manduca sexta.

Flight motor networks modulate primary olfactory processing in the moth Manduca sexta.
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DOI:
10.1073/pnas.1722379115
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发表时间:
2018-05-22
影响因子:
11.1
通讯作者:
Daly KC
Daly KC
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Chapman PD;Burkland R;Bradley SP;Houot B;Bullman V;Dacks AM;Daly KC

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在脊椎动物和无脊椎动物中,必然放电回路(CDC)投射并告知感觉网络有关动物的运动,这直接影响感觉处理。CDC的失败可能是精神分裂症、帕金森病和呼吸困难的感觉幻觉的基础,突出了CDC对于成功解释感觉线索以适应性地与外部世界互动的根本重要性。最终,了解CDCs在整合感觉运动功能中的作用对于了解这些疾病至关重要,但对CDCs的功能机制知之甚少。CDCs已经在除嗅觉以外的大多数感觉领域中被鉴定。我们的研究结果表明,组胺能CDC增强嗅觉系统的能力,更精确地编码刺激的时间结构,从而提高嗅觉敏锐度。神经系统必须区分来自动物自身运动的感觉信号(reafference)和来自环境的感觉信号(exafference)。为了实现这一点,运动神经网络产生的reafference传输运动信息,通过一个必然的放电电路(CDC),受影响的感觉网络,在行为过程中调节感觉功能。虽然CDCs已被描述在大多数感觉方式,没有被观察到投射到嗅觉通路。在蛾,两个mesothoracic中脑组胺能神经元(MDHns)项目从飞行感觉运动中心mesothoracic neuromere的触角叶(AL),在那里他们提供的唯一来源的组胺(HA),但他们是否代表CDC是未知的。我们表明,MDHn尖峰活动与翅膀电机输出呈正相关,并增加了运动活动的回合之前,这表明MDHns沟通全球运动状态,而不是提供一个精确的定时电机副本。在AL,HA应用程序加剧夹带的投射神经元的气味刺激嵌入在模拟翅拍诱导的流量,而MDHN轴突切断术或AL HA受体(HA-R)的封锁减少夹带。这一发现与高阶CDC一致,因为MDHns增强而不是过滤了AL投射神经元的夹带。最后,HA-r阻断增加了行为测定中的气味检测和辨别阈值。这些结果确立了MDHns作为调节AL时间分辨率的CDC,增强了气味引导行为。因此,MDHN似乎代表了昆虫嗅觉通路的高阶CDC;这种CDC的独特性质突出了运动到感觉信号传导作为微调感觉功能的上下文特异性机制的重要性。
Across vertebrates and invertebrates, corollary discharge circuits (CDCs) project to and inform sensory networks about an animal’s movements, which directly impact sensory processing. Failure of CDCs likely underlie sensory hallucinations in schizophrenia, Parkinson’s disease, and dyspnea, highlighting the fundamental importance of CDCs for successfully interpreting sensory cues to adaptively interact with the external world. Ultimately, understanding the role of CDCs in integrating sensory motor function will be vital to understand these diseases, but mechanistically little is known about how CDCs function. CDCs have been identified in most sensory domains except olfaction. Our findings indicate that a histaminergic CDC enhances the ability of the olfactory system to more precisely encode stimulus temporal structure, resulting in enhanced olfactory acuity. Nervous systems must distinguish sensory signals derived from an animal’s own movements (reafference) from environmentally derived sources (exafference). To accomplish this, motor networks producing reafference transmit motor information, via a corollary discharge circuit (CDC), to affected sensory networks, modulating sensory function during behavior. While CDCs have been described in most sensory modalities, none have been observed projecting to an olfactory pathway. In moths, two mesothoracic to deutocerebral histaminergic neurons (MDHns) project from flight sensorimotor centers in the mesothoracic neuromere to the antennal lobe (AL), where they provide the sole source of histamine (HA), but whether they represent a CDC is unknown. We demonstrate that MDHn spiking activity is positively correlated with wing-motor output and increased before bouts of motor activity, suggesting that MDHns communicate global locomotor state, rather than providing a precisely timed motor copy. Within the AL, HA application sharpened entrainment of projection neuron responses to odor stimuli embedded within simulated wing-beat–induced flows, whereas MDHn axotomy or AL HA receptor (HA-r) blockade reduced entrainment. This finding is consistent with higher-order CDCs, as the MDHns enhanced rather than filtered entrainment of AL projection neurons. Finally, HA-r blockade increased odor detection and discrimination thresholds in behavior assays. These results establish MDHns as a CDC that modulates AL temporal resolution, enhancing odor-guided behavior. MDHns thus appear to represent a higher-order CDC to an insect olfactory pathway; this CDC’s unique nature highlights the importance of motor-to-sensory signaling as a context-specific mechanism that fine-tunes sensory function.
DOI: 10.1371/journal.pone.0023382
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影响因子: 6.6
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发表时间: 2004-07-13
影响因子: 11.1
作者:
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通讯作者: Hildebrand, JG
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发表时间: 2011-11-01
影响因子: 2.2
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