Many species of rodents rely on the set of exquisitely sensitive facial vibrissae (whiskers) to guide rich behaviors in which other senses are inadequate. Although whiskers are, like all hairs, inert strands of keratin, they provide the animal with a rich landscape of tactile information which is used to guide complex behaviors. This behavioral importance is complimented by striking anatomical and neural structure to make the rodent whisker system one of the most widely studied model systems across many disciplines of neuroscience. However, the vibrissal research field lacks a detailed understanding of how the set of primary sensory neurons responsible for the initial translation of environmental information into the neural code parses together the complex landscape of tactile interactions with the world. Although much work has been done to dissect the coding properties of these primary sensory neurons (found in the trigeminal ganglion – Vg), individual reductionist experiments offer only a snapshot of the response properties of these neurons. It is still unclear how the coding properties of Vg neurons interpret external information in terms of the fundamental drivers of whisker-object interactions: the mechanical deformations experienced in the follicle. Although the relationship between primary sensory neuron encoding and mechanical deformations has long been expected, the ability to quantify the mechanics governing whisker contact has been impractical. In addition, the whisker system evolved to parse mechanical information from a variety of mechanical contexts in which the features present in the stimuli are complex and covary. Previous work averages over this variability and can only provide glimpses at how the entire range and complexity of natural stimuli are represented. The work described here focuses on how complex and naturalistic mechanical information might be acquired and represented in primary sensory neurons of the vibrissal-trigeminal system. In doing so, we underscore the computational complexity required of the system. We first quantify the mechanical drivers of whisker-object interactions in restricted 2D motions in both anesthetized and awake rats to show that primary sensory neurons do indeed directly represent mechanical stimulus properties. We then describe how a natural stimulus – wind – affects the motion of the whisker, and demonstrate that Vg neuron responses correlate with feature parameters of such complex and natural stimuli. A major short-coming of much work describing the whisker system, not just studies of Vg neurons, is that they neglect motion of the whiskers in 3D space. To address this shortcoming, we first describe formal coordinate systems for describing 3D whisker motions which underscore the complexity of the 3D information available to the system. We culminate the work with recordings from Vg neurons during naturalistic and variable 3D deflections while quantifying 3D mechanical information. This work allows us to describe the broader tuning characteristics of Vg neurons to the large space of possible tactile stimuli, and makes predictions about how the population of Vg neurons may afford flexible and complete representations of the tactile world. Taken together, we hope this work will encourage the whisker field to account for and to appreciate the richness of the sensory, motor, and behavioral capabilities of the rodent whisker system. Supplemental videos are included in this work. Detailed descriptions of these videos can be found in the supplemental figures section. Briefly: supplemental video 2.1 illustrates the qualitative difference between awake and passive whisker contacts; supplemental videos 2.2A-D provide examples of the stimulus space structure explored in a number of active and passive stimulation experiments; supplemental video 2.3 gives a qualitative example of the difference between distal and proximal passive whisker stimulations; supplemental videos 5.1-5.3 give example whisker reconstructions, mechanical consequences of contact, and neural activity for 3 example neurons during the 3D stimulation protocol described in chapter 5.

Creator

• Bush, Nicholas E

DOI

• https://doi.org/10.21985/n2-ej6q-q844

Subject

• Neurosciences

Language

• en

Alternate Identifier

• http://dissertations.umi.com/northwestern:14697
• etdadmin_upload_666783

Keyword

• Mechanics
• Afferent
• Vibrissal
• Trigeminal
• Whisker

Date created

• 2019-01-01

Resource type

• Dissertation

Rights statement

• In Copyright