Continuous, multidimensional coding of 3D complex tactile stimuli by primary sensory neurons of the vibrissal system

AbstractTo reveal the full representational capabilities of sensory neurons, it is essential to observe their responses to complex stimuli. In the rodent vibrissal system, mechanical information at the whisker base drives responses of primary sensory neurons in the trigeminal ganglion (Vg). Studies of how Vg neurons encode stimulus properties are typically limited to 2D analyses and restricted stimulus sets. Here we record from Vg neurons during 3D stimulation while quantifying the complete 3D whisker shape and mechanics. Results show that individual Vg neurons simultaneously represent multiple mechanical features of the stimulus, do not preferentially encode principal components of the stimuli, and represent continuous and tiled variations of all available mechanical information. As a population, the neurons span a continuum of rapid and slow adaptation properties; a binary distinction between these adaptation classes is oversimplified. These results contrast with proposed codes in which Vg neurons segregate into functional classes.

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Continuous, multidimensional coding of 3D complex tactile stimuli by primary sensory neurons of the vibrissal system

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2020194118 ◽

2021 ◽

Vol 118 (32) ◽

pp. e2020194118

Author(s):

Nicholas E. Bush ◽

Sara A. Solla ◽

Mitra J. Z. Hartmann

Keyword(s):

Sensory Neurons ◽

Three Dimensional ◽

Primary Sensory Neurons ◽

Tactile Information ◽

Central Neurons ◽

Information Bottleneck ◽

Tactile Stimuli ◽

Functional Classes ◽

Stimulus Features ◽

Multidimensional Representation

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.

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