Max F. Perutz Laboratories, University of Vienna, Vienna, Austria.
PLoS Biol. 2013;11(6):e1001585. doi: 10.1371/journal.pbio.1001585. Epub 2013 Jun 11.
The functional principle of the vertebrate brain is often paralleled to a computer: information collected by dedicated devices is processed and integrated by interneuron circuits and leads to output. However, inter- and motorneurons present in today's vertebrate brains are thought to derive from neurons that combined sensory, integration, and motor function. Consistently, sensory inter-motorneurons have been found in the simple nerve nets of cnidarians, animals at the base of the evolutionary lineage. We show that light-sensory motorneurons and light-sensory interneurons are also present in the brains of vertebrates, challenging the paradigm that information processing and output circuitry in the central brain is shielded from direct environmental influences. We investigated two groups of nonvisual photopigments, VAL- and TMT-Opsins, in zebrafish and medaka fish; two teleost species from distinct habitats separated by over 300 million years of evolution. TMT-Opsin subclasses are specifically expressed not only in hypothalamic and thalamic deep brain photoreceptors, but also in interneurons and motorneurons with no known photoreceptive function, such as the typeXIV interneurons of the fish optic tectum. We further show that TMT-Opsins and Encephalopsin render neuronal cells light-sensitive. TMT-Opsins preferentially respond to blue light relative to rhodopsin, with subclass-specific response kinetics. We discovered that tmt-opsins co-express with val-opsins, known green light receptors, in distinct inter- and motorneurons. Finally, we show by electrophysiological recordings on isolated adult tectal slices that interneurons in the position of typeXIV neurons respond to light. Our work supports "sensory-inter-motorneurons" as ancient units for brain evolution. It also reveals that vertebrate inter- and motorneurons are endowed with an evolutionarily ancient, complex light-sensory ability that could be used to detect changes in ambient light spectra, possibly providing the endogenous equivalent to an optogenetic machinery.
专门设备收集的信息由中间神经元电路进行处理和整合，并导致输出。然而，目前在脊椎动物大脑中存在的中间神经元和运动神经元被认为源自于具有感觉、整合和运动功能的神经元。一致地，在简单的神经网中发现了感觉中间运动神经元，这些动物处于进化谱系的基础。我们表明，光感觉运动神经元和光感觉中间神经元也存在于脊椎动物的大脑中，这挑战了中枢大脑中的信息处理和输出电路免受直接环境影响的范式。我们研究了两组非视觉视蛋白，VAL 和 TMT 视蛋白，在斑马鱼和青鳉鱼中；这两个硬骨鱼物种来自于 3 亿多年进化历史的不同栖息地。TMT 视蛋白亚类不仅特异性表达在下丘脑和丘脑深部脑光感受器中，而且还表达在没有已知光感受功能的中间神经元和运动神经元中，例如鱼类视顶盖的类型 XIV 中间神经元。我们进一步表明，TMT 视蛋白和脑视蛋白使神经元细胞对光敏感。TMT 视蛋白相对于视紫红质对蓝光具有优先响应，具有亚类特异性的响应动力学。我们发现，tmt-opsins 与已知的绿光受体 val-opsins 共同表达在不同的中间神经元和运动神经元中。最后，我们通过对分离的成年顶盖切片进行电生理记录表明，类型 XIV 神经元位置的中间神经元对光有反应。我们的工作支持“感觉中间运动神经元”作为大脑进化的古老单元。它还表明，脊椎动物中间神经元和运动神经元具有古老的、复杂的光感觉能力，可用于检测环境光光谱的变化，可能为内源提供光遗传学机制的等效物。
