A dendrite-autonomous mechanism for direction selectivity in retinal starburst amacrine cells.

A dendrite-autonomous mechanism for direction selectivity in retinal starburst amacrine cells.
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DOI:
10.1371/journal.pbio.0050185
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发表时间:
2007-07
期刊:
影响因子:
9.8
通讯作者:
Denk W
Denk W
中科院分区:
生物学1区
文献类型:
--
作者:
Hausselt SE;Euler T;Detwiler PB;Denk W

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图像运动方向的检测始于视网膜,其中星爆无长突细胞 (SAC) 发挥着主要作用。当 SAC 从体体向树突尖端运动时,与相反方向运动相比,SAC 会产生更大的树突 Ca2+ 信号。为了研究 SAC 树突方向选择性 (DS) 计算的机制,通过体细胞全细胞记录测量对扩张和收缩圆波视觉刺激的电反应,并使用傅立叶分析进行量化。对于扩展刺激,基波频率分量(尤其是谐波频率分量)更大。这种 DS 在 GABA 和甘氨酸受体拮抗剂存在的情况下持续存在,表明抑制网络相互作用并不是必需的。谐波的存在表明非线性,正如谐波幅度和保持电位之间的关系所示,这可能是由于电压门控通道的激活所致。由电压阶跃引起并通过双光子显微镜监测的 SAC 树突中的 [Ca2+] 变化表明,远端树突相对于体体是强直去极化的,部分原因是强直性谷氨酸突触输入介导的静息电流,并且高电压激活的 Ca2+ 通道在静息时是活跃的。在区室模型的支持下,我们得出结论,SAC 中的树突 DS 可以由树突本身计算,依赖于电压门控通道和树突电压梯度,这提供了方向辨别所需的空间不对称性。视觉系统投入大量资源来检测运动及其方向。 40 多年来,研究人员一直试图破译视网膜神经元计算定向运动的基本计算机制。参与方向辨别的一种视网膜中间神经元是“星爆”无长突细胞。星爆细胞树突会被从体体向树突尖端的视觉运动强烈激活,但不会被相反方向的运动激活。例如,有人提出,方向选择性是由横向抑制相互作用产生的,其中激活的细胞抑制其邻居。然而,尽管进行了广泛的建模,但潜在的生理机制仍然难以捉摸。在这里,通过结合全细胞记录、双光子显微镜和建模,我们表明星爆细胞树突运动方向的辨别不需要视网膜中的横向抑制相互作用,而是可以通过依赖于内在电机制的“树突自主”计算来生成。阻断抑制相互作用并不能消除方向响​​应,而电压门控膜电导和树突电压梯度的差异激活可以提供必要的空间不对称性以产生方向信号。树突自主方向选择性的计算可能代表迄今为止树突信息处理最复杂的示例之一。视网膜星爆无长突细胞的方向选择性可以由电压门控通道和在没有侧向抑制的情况下的树突电压梯度产生。
Detection of image motion direction begins in the retina, with starburst amacrine cells (SACs) playing a major role. SACs generate larger dendritic Ca2+ signals when motion is from their somata towards their dendritic tips than for motion in the opposite direction. To study the mechanisms underlying the computation of direction selectivity (DS) in SAC dendrites, electrical responses to expanding and contracting circular wave visual stimuli were measured via somatic whole-cell recordings and quantified using Fourier analysis. Fundamental and, especially, harmonic frequency components were larger for expanding stimuli. This DS persists in the presence of GABA and glycine receptor antagonists, suggesting that inhibitory network interactions are not essential. The presence of harmonics indicates nonlinearity, which, as the relationship between harmonic amplitudes and holding potential indicates, is likely due to the activation of voltage-gated channels. [Ca2+] changes in SAC dendrites evoked by voltage steps and monitored by two-photon microscopy suggest that the distal dendrite is tonically depolarized relative to the soma, due in part to resting currents mediated by tonic glutamatergic synaptic input, and that high-voltage–activated Ca2+ channels are active at rest. Supported by compartmental modeling, we conclude that dendritic DS in SACs can be computed by the dendrites themselves, relying on voltage-gated channels and a dendritic voltage gradient, which provides the spatial asymmetry necessary for direction discrimination. The visual system dedicates substantial resources to detecting motion and its direction. For more than 40 years, researchers have tried to decipher the underlying computational mechanisms by which retinal neurons compute directed motion. One type of retinal interneuron involved in direction discrimination is the “starburst” amacrine cell. Starburst-cell dendrites are strongly activated by visual motion from their somata towards the dendritic tips, but not by motion in the opposite direction. It has been proposed, for example, that directional selectivity arises from lateral inhibitory interactions in which activated cells inhibit their neighbors. However, despite extensive modeling, the underlying physiological mechanism has remained elusive. Here, by combining whole-cell recordings, two-photon microscopy, and modeling, we show that discrimination of motion direction in starburst-cell dendrites does not require lateral inhibitory interactions in the retina, but can be generated by a “dendrite-autonomous” computation, which relies on intrinsic electrical mechanisms. Blocking inhibitory interactions does not eliminate directional responses, whereas differential activation of voltage-gated membrane conductances and a dendritic voltage gradient can provide the necessary spatial asymmetry to produce directional signals. The computation underlying dendrite-autonomous direction selectivity may represent one of the most intricate examples to date of dendritic information processing. Direction selectivity in starburst amacrine cells in the retina can arise from voltage-gated channels and a dendritic voltage gradient in the absence of lateral inhibition.
DOI: 10.1038/nature00931
发表时间: 2002-08-22
期刊: NATURE
影响因子: 64.8
作者:
Euler, T;Detwiler, PB;Denk, W
通讯作者: Denk, W
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影响因子: 2.5
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影响因子: 5.5
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发表时间: 2002-11-28
期刊: NATURE
影响因子: 64.8
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