Ernst Strüngmann Institute for Neuroscience in Cooperation with Max Planck Society, Frankfurt/Main D-60528, Germany;
Frankfurt Institute for Advanced Studies, Frankfurt/Main D-60438, Germany.
Proc Natl Acad Sci U S A. 2017 May 16;114(20):E4057-E4064. doi: 10.1073/pnas.1616163114. Epub 2017 May 3.
Neurons sharing similar features are often selectively connected with a higher probability and should be located in close vicinity to save wiring. Selective connectivity has, therefore, been proposed to be the cause for spatial organization in cortical maps. Interestingly, orientation preference (OP) maps in the visual cortex are found in carnivores, ungulates, and primates but are not found in rodents, indicating fundamental differences in selective connectivity that seem unexpected for closely related species. Here, we investigate this finding by using multidimensional scaling to predict the locations of neurons based on minimizing wiring costs for any given connectivity. Our model shows a transition from an unstructured salt-and-pepper organization to a pinwheel arrangement when increasing the number of neurons, even without changing the selectivity of the connections. Increasing neuronal numbers also leads to the emergence of layers, retinotopy, or ocular dominance columns for the selective connectivity corresponding to each arrangement. We further show that neuron numbers impact overall interconnectivity as the primary reason for the appearance of neural maps, which we link to a known phase transition in an Ising-like model from statistical mechanics. Finally, we curated biological data from the literature to show that neural maps appear as the number of neurons in visual cortex increases over a wide range of mammalian species. Our results provide a simple explanation for the existence of salt-and-pepper arrangements in rodents and pinwheel arrangements in the visual cortex of primates, carnivores, and ungulates without assuming differences in the general visual cortex architecture and connectivity.
具有相似特征的神经元通常以更高的概率被选择性连接,并且应该位于接近的位置以节省布线。因此,选择性连接被认为是皮质图中空间组织的原因。有趣的是,在食肉动物、有蹄类动物和灵长类动物中发现了视觉皮层中的方位偏好 (OP) 图,但在啮齿动物中没有发现,这表明选择性连接存在根本差异,这似乎与密切相关的物种不符。在这里,我们通过使用多维尺度分析来预测神经元的位置,根据最小化任何给定连接的布线成本来预测神经元的位置,从而研究了这一发现。我们的模型表明,当神经元数量增加时,即使不改变连接的选择性,也会从无结构的椒盐组织过渡到风车排列。增加神经元数量还会导致选择性连接的层、视网膜拓扑或眼优势柱的出现,对应于每种排列。我们进一步表明,神经元数量是出现神经图的主要原因,这是整体互连性的影响,我们将其与统计力学中类似伊辛模型的已知相变联系起来。最后,我们从文献中整理了生物学数据,以显示在广泛的哺乳动物物种中,随着视觉皮层中神经元数量的增加,出现了神经图。我们的结果为在啮齿动物中存在椒盐排列和在灵长类动物、食肉动物和有蹄类动物的视觉皮层中存在风车排列提供了一个简单的解释,而无需假设一般视觉皮层结构和连接存在差异。