Centre for Developmental Neurobiology and MRC Centre for Neurodevelopmental Disorders, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom.
Queensland Brain Institute and School of Mathematics and Physics, University of Queensland, St Lucia, QLD, Australia.
Front Neural Circuits. 2017 Nov 21;11:88. doi: 10.3389/fncir.2017.00088. eCollection 2017.
The circuit mechanisms that give rise to direction selectivity in the retina have been studied extensively but how direction selectivity is established in retinorecipient areas of the brain is less well understood. Using functional imaging in larval zebrafish we examine how the direction of motion is encoded by populations of neurons at three layers of the optic tectum; retinal ganglion cell axons (RGCs), a layer of superficial inhibitory interneurons (SINs), and periventricular neurons (PVNs), which constitute the majority of neurons in the tectum. We show that the representation of motion direction is transformed at each layer. At the level of RGCs and SINs the direction of motion is encoded by three direction-selective (DS) subtypes tuned to upward, downward, and caudal-to-rostral motion. However, the tuning of SINs is significantly narrower and this leads to a conspicuous gap in the representation of motion in the rostral-to-caudal direction at the level of SINs. Consistent with previous findings we demonstrate that, at the level of PVNs the direction of motion is encoded by four DS cell types which include an additional DS PVN cell type tuned to rostral-to-caudal motion. Strikingly, the tuning profile of this emergent cell type overlaps with the gap in the representation of rostral-to-caudal motion at the level of SINs. Using our functional imaging data we constructed a simple computational model that demonstrates how the emergent population of PVNs is generated by the interactions of cells at each layer of the tectal network. The model predicts that PVNs tuned to rostral-to-caudal motion can be generated via convergence of DS RGCs tuned to upward and downward motion and feedforward tuned inhibition via SINs which suppresses responses to non-preferred directions. Thus, by reshaping directional tuning that is inherited from the retina inhibitory inputs from SINs can generate a novel subtype of DS PVN and in so doing enhance the encoding of directional stimuli.
视网膜中产生方向选择性的电路机制已经得到了广泛的研究，但在大脑的视网膜接收区中，方向选择性是如何建立的还不太清楚。我们使用幼虫斑马鱼的功能成像来研究在三个视顶盖层中神经元群体如何对运动方向进行编码; 视网膜神经节细胞轴突 (RGCs)、浅层抑制性中间神经元 (SINs) 层和脑室周围神经元 (PVNs)，它们构成了视顶盖中的大多数神经元。我们表明，运动方向的表示在每个层中都发生了转换。在 RGCs 和 SINs 层面，运动方向由三种方向选择性 (DS) 亚型编码，这些亚型分别对向上、向下和向后到向前的运动敏感。然而，SINs 的调谐明显更窄，这导致在 SINs 层面上运动方向的表示出现明显的缺口。与先前的发现一致，我们证明，在 PVNs 层面，运动方向由四种 DS 细胞类型编码，其中包括一种对向后到向前运动敏感的额外 DS PVN 细胞类型。引人注目的是，这种新兴细胞类型的调谐曲线与 SINs 层面上向后到向前运动的表示缺口重叠。使用我们的功能成像数据，我们构建了一个简单的计算模型，该模型演示了新兴的 PVNs 群体如何通过视顶盖网络各层细胞的相互作用产生。该模型预测，对向后到向前运动敏感的 PVNs 可以通过向上和向下运动的 DS RGCs 的会聚以及通过 SINs 的前馈调谐抑制产生，该抑制抑制对非首选方向的反应。因此，通过重塑从视网膜继承的方向调谐，来自 SINs 的抑制性输入可以产生新型的 DS PVN 亚型，并以此增强对方向刺激的编码。
