Interdepartmental Neuroscience Program, Northwestern University, Evanston, IL 60208.
Department of Physics and Astronomy, Northwestern University, Evanston, IL 60208.
Proc Natl Acad Sci U S A. 2021 Aug 10;118(32). doi: 10.1073/pnas.2020194118.
Across all sensory modalities, first-stage sensory neurons are an information bottleneck: they must convey all information available for an animal to perceive and act in its environment. Our understanding of coding properties of primary sensory neurons in the auditory and visual systems has been aided by the use of increasingly complex, naturalistic stimulus sets. By comparison, encoding properties of primary somatosensory afferents are poorly understood. Here, we use the rodent whisker system to examine how tactile information is represented in primary sensory neurons of the trigeminal ganglion (Vg). Vg neurons have long been thought to segregate into functional classes associated with separate streams of information processing. However, this view is based on Vg responses to restricted stimulus sets which potentially underreport the coding capabilities of these neurons. In contrast, the current study records Vg responses to complex three-dimensional (3D) stimulation while quantifying the complete 3D whisker shape and mechanics, thereby beginning to reveal their full representational capabilities. The results show that individual Vg neurons simultaneously represent multiple mechanical features of a stimulus, do not preferentially encode principal components of the stimuli, and represent continuous and tiled variations of all available mechanical information. These results directly contrast with proposed codes in which subpopulations of Vg neurons encode select stimulus features. Instead, individual Vg neurons likely overcome the information bottleneck by encoding large regions of a complex sensory space. This proposed tiled and multidimensional representation at the Vg directly constrains the computations performed by more central neurons of the vibrissotrigeminal pathway.
在所有感觉模态中，第一级感觉神经元是信息瓶颈：它们必须传达动物感知和在其环境中行动所需的所有信息。我们对听觉和视觉系统中初级感觉神经元编码特性的理解得益于越来越复杂的、自然主义刺激集的使用。相比之下，初级躯体感觉传入的编码特性理解得很差。在这里，我们使用啮齿动物胡须系统来研究触觉信息在三叉神经节（Vg）的初级感觉神经元中的表示方式。Vg 神经元长期以来一直被认为分为与信息处理的不同流相关的功能类。然而，这种观点是基于 Vg 对受限刺激集的反应，这些反应可能会低估这些神经元的编码能力。相比之下，目前的研究记录了 Vg 对复杂三维（3D）刺激的反应，同时量化了完整的 3D 胡须形状和力学，从而开始揭示它们的全部表示能力。结果表明，单个 Vg 神经元同时表示刺激的多个机械特征，不优先编码刺激的主要成分，并且表示所有可用机械信息的连续和平铺变化。这些结果与 Vg 神经元亚群编码选择刺激特征的拟议代码直接形成对比。相反，单个 Vg 神经元可能通过编码复杂感觉空间的大区域来克服信息瓶颈。这种在 Vg 提出的平铺和多维表示直接限制了触须振动三叉神经通路中更中心神经元的计算。
