Additive contributions of melanopsin and both cone types provide broadband sensitivity to mouse pupil control.

Additive contributions of melanopsin and both cone types provide broadband sensitivity to mouse pupil control.
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DOI:
10.1186/s12915-018-0552-1
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发表时间:
2018-07-31
期刊:
影响因子:
5.4
通讯作者:
Brown TM
Brown TM
中科院分区:
生物学2区
文献类型:
--
作者:
Hayter EA;Brown TM

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视网膜内光敏神经节细胞(ipRGC)驱动一系列非成像(NIF)视觉反应,包括昼夜光诱导和瞳孔光反射。ipRGC整合了外在(视杆/视锥)和内在(黑视蛋白)光感受信号,但视锥对ipRGC依赖性反应的贡献仍不完全清楚。鉴于最近的数据显示,锥衍生的颜色信号影响小鼠的昼夜节律和瞳孔反应在人类中,在这里,我们着手调查颜色信息在小鼠瞳孔控制中的作用。我们首先记录了具有红移视锥细胞群(Opn 1 mwR)的麻醉小鼠和缺乏功能性视锥细胞(Cnga 3 −/−)或黑视蛋白(Opn 1 mwR; Opn 4 −/−)的小鼠的顶盖前橄榄核(PON)的电生理活动。使用多光谱刺激,选择性地调制个别视蛋白类的活动,我们表明,PON细胞接收ipRGC输入也表现出强大的S-和/或L-视锥视蛋白驱动的活动。该群体包括许多细胞,其中两种视锥视蛋白驱动对手反应(最常见的是对S-视蛋白刺激的兴奋性/ON反应和对L-视蛋白刺激的抑制性/OFF反应)。这些视锥输入可靠地跟踪在明视条件下照度/颜色的甚至缓慢(0.025 Hz)变化,其中黑视蛋白贡献对于较高对比度/较低时间频率刺激变得越来越占主导地位。我们还评估了清醒动物的一致性瞳孔反应,并表明,令人惊讶的是,这方面的生理是不敏感的彩色信号起源于锥。相反,与人类的情况相反,来自黑视蛋白和两种视锥蛋白的信号以纯粹的加性方式结合联合收割机来驱动小鼠的瞳孔收缩。我们的数据揭示了小鼠瞳孔的感觉控制相对于ipRGC的另一个主要目标-昼夜节律钟的关键差异。后者使用颜色信息来帮助估计一天中的时间,而小鼠瞳孔则将视锥视蛋白类的信号相加,以提供对照明变化的宽带光谱灵敏度。因此,虽然色反应和黑视蛋白输入PON中的广泛共存支持颜色辨别机制和NIF视觉处理之间的密切关联,但我们的数据表明,小鼠中的颜色对手PON细胞有助于瞳孔控制以外的功能。本文的在线版本(10.1186/s12915-018-0552-1)包含补充材料,可供授权用户使用。
Intrinsically photosensitive retinal ganglion cells (ipRGCs) drive an array of non-image-forming (NIF) visual responses including circadian photoentrainment and the pupil light reflex. ipRGCs integrate extrinsic (rod/cone) and intrinsic (melanopsin) photoreceptive signals, but the contribution of cones to ipRGC-dependent responses remains incompletely understood. Given recent data revealing that cone-derived colour signals influence mouse circadian timing and pupil responses in humans, here we set out to investigate the role of colour information in pupil control in mice. We first recorded electrophysiological activity from the pretectal olivary nucleus (PON) of anaesthetised mice with a red-shifted cone population (Opn1mwR) and mice lacking functional cones (Cnga3−/−) or melanopsin (Opn1mwR; Opn4−/−). Using multispectral stimuli to selectively modulate the activity of individual opsin classes, we show that PON cells which receive ipRGC input also exhibit robust S- and/or L-cone opsin-driven activity. This population includes many cells where the two cone opsins drive opponent responses (most commonly excitatory/ON responses to S-opsin stimulation and inhibitory/OFF responses to L-opsin stimulation). These cone inputs reliably tracked even slow (0.025 Hz) changes in illuminance/colour under photopic conditions with melanopsin contributions becoming increasingly dominant for higher-contrast/lower temporal frequency stimuli. We also evaluated consensual pupil responses in awake animals and show that, surprisingly, this aspect of physiology is insensitive to chromatic signals originating with cones. Instead, by contrast with the situation in humans, signals from melanopsin and both cone opsins combine in a purely additive manner to drive pupil constriction in mice. Our data reveal a key difference in the sensory control of the mouse pupil relative to another major target of ipRGCs—the circadian clock. Whereas the latter uses colour information to help estimate time of day, the mouse pupil instead sums signals across cone opsin classes to provide broadband spectral sensitivity to changes in illumination. As such, while the widespread co-occurrence of chromatic responses and melanopsin input in the PON supports a close association between colour discrimination mechanisms and NIF visual processing, our data suggest that colour opponent PON cells in the mouse contribute to functions other than pupil control. The online version of this article (10.1186/s12915-018-0552-1) contains supplementary material, which is available to authorized users.
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