Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis.

Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis.
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DOI:
10.1038/nature06927
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发表时间:
2008-07-03
期刊:
影响因子:
64.8
通讯作者:
Schafer, William R.
Schafer, William R.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Suzuki, Hiroshi;Thiele, Tod R.;Faumont, Serge;Ezcurra, Marina;Lockery, Shawn R.;Schafer, William R.

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秀丽隐杆线虫的趋化性,就像细菌的趋化性一样,涉及一个随机游走,受到引诱剂浓度的时间导数的影响,但导数是如何计算的尚不清楚。激光消融显示,当ASE神经元(ASEL和ASER)被杀死时,对盐的趋化性出现最强的缺陷,表明这对神经元起主导作用。尽管这些神经元在解剖学上是左右同源的,但它们在基因表达和离子偏好方面表现出明显的不对称性。在这里,利用完整动物ASE神经元钙瞬态的光学记录,我们证明了额外的不对称性:ASEL是一个on细胞,受到NaCl浓度增加的刺激,而ASER是一个off细胞,受到NaCl浓度降低的刺激。这两种反应都是可靠的,但都是短暂的,表明ASE神经元报告的是浓度变化,而不是绝对水平。突触和感觉转导突变体的记录表明,开关不对称是ASE神经元之间内在差异的结果。单侧激活实验表明,这种不对称性延伸到了行为输出的层面:ASEL延长了向前运动的回合(奔跑),而ASEL促进了方向变化(转弯)。引人注目的是,ASE神经元的输入和输出不对称恰恰是计算化学感觉信息时间导数的一个简单而新颖的神经元基序的输入和输出不对称,这是秀丽隐杆线虫趋化性的基本计算。其他化学感觉网络中ON和OFF细胞的证据表明,这种基序可能在通过味觉和嗅觉导航的动物中很常见。
Chemotaxis in C. elegans, like chemotaxis in bacteria, involves a random walk biased by the time derivative of attractant concentration, but how the derivative is computed is unknown. Laser ablations have shown that the strongest deficits in chemotaxis to salts are obtained when the ASE neurons (ASEL and ASER) are killed, indicating that this pair plays a dominant role. Although these neurons are left-right homologs anatomically, they exhibit marked asymmetries in gene expression and ion preference. Here, using optical recordings of calcium transients in ASE neurons in intact animals, we demonstrate an additional asymmetry: ASEL is an ON-cell, stimulated by increases in NaCl concentration, whereas ASER is an OFF-cell, stimulated by decreases in NaCl concentration. Both responses are reliable yet transient, indicating that ASE neurons report changes in concentration rather than absolute levels. Recordings from synaptic and sensory transduction mutants show that the ON-OFF asymmetry is the result of intrinsic differences between ASE neurons. Unilateral activation experiments indicate that the asymmetry extends to the level of behavioral output: ASEL lengthens bouts of forward locomotion (runs) whereas ASER promotes direction changes (turns). Strikingly, the input and output asymmetries of ASE neurons are precisely those of a simple yet novel neuronal motif for computing the time derivative of chemosensory information, which is the fundamental computation of C. elegans chemotaxis. Evidence for ON and OFF cells in other chemosensory networks suggests that this motif may be common in animals that navigate by taste and smell.
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影响因子: 5.3
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