We see because retinal ganglion cells respond to light. We hear because spiral ganglion cells respond to sound. We feel because primary somatosensory neurons respond to touch. But what is touch? Whereas light and sound can be characterized by physical parameters (amplitude, frequency, phase, and polarization), the mechanics of touch, and the manner in which primary sensory neurons encode the parameters of touch, are largely unquantified. This is a glaring gap within the entire field of somatosensation, and it occurs because mechanics are difficult to quantify. To close this gap we will use the rat vibrissal (whisker) system as a model to directly relate the responses of primary sensory neurons to the quantified mechanics of touch. Paralleling the increased use of rodents in genetic and optogenetic research, the rodent vibrissal array has become an increasingly important model for the study of touch and sensorimotor integration. In the past few years, our laboratory has made rapid progress in characterizing vibrissal mechanics, and we are now uniquely positioned to determine how 3D whisker deflections and vibrations are represented in the firing patterns of primary sensory neurons of the trigeminal ganglion (Vg) during natural whisking behavior. The central goal of our investigation is to predict the responses of Vg neurons during both contact and non-contact whisking by appropriately combining 3D dynamic and quasistatic models of mechanical signals. Our three aims move from the outside of the rat inwards, from whisker, to follicle, to Vg neurons.
In Aim 1, we will develop models of mechanical coding by the whisker, quantifying the 3D mechanical signals at the vibrissal base during both contact and non-contact whisking.
In Aim 2, these models will be used to predict responses of mechanoreceptors within the follicle and thus to identify classes of Vg neurons based on the mechanical transformation they perform. Finally, in Aim 3 we will quantify the responses of Vg neurons during natural whisking behavior in awake animals. Exploiting the cell classes identified in Aim 2, and consistent with the modeling of Aim1, we will test the hypothesis that Vg responses are more linearly correlated with mechanical signals during whisking than they are with the geometry and kinematics of whisking behavior. The proposed work will be the first to record from Vg neurons in awake behaving animals while fully characterizing the mechanical input during both contact and non-contact whisking.
We aim to solve a large portion of the coding problem for the vibrissal-trigeminal system. Solving this problem will provide a better understanding of what a Vg spike means for more central stages of the trigeminal system, including sensory thalamus and barrel cortex.

Public Health Relevance

Our sense of touch is an essential part of our everyday experience - we use our sense of touch in activities that range from grasping a coffee mug to giving a hug to a loved one. Our ability to combine movement with the sense of touch is impaired in disorders such as stroke, but the ability to help patients overcome these deficits is hindered by the fact that neuroscientists still do not understand how 'touch' is represented in the electrical activity of neurons. The proposed work makes use of the rat whisker system as a model to study how the mechanics of movement and touch are encoded by neurons in the earliest stages of brain processing; it is these neurons that establish the features of the code to be used by subsequent brain areas to represent the sensory experience of touch.

Agency
National Institute of Health (NIH)
Institute
National Institute of Neurological Disorders and Stroke (NINDS)
Type
Research Project (R01)
Project #
5R01NS093585-03
Application #
9317557
Study Section
Special Emphasis Panel (ZRG1)
Program Officer
Gnadt, James W
Project Start
2015-07-01
Project End
2020-06-30
Budget Start
2017-07-01
Budget End
2018-06-30
Support Year
3
Fiscal Year
2017
Total Cost
Indirect Cost
Name
Northwestern University at Chicago
Department
Biomedical Engineering
Type
Biomed Engr/Col Engr/Engr Sta
DUNS #
160079455
City
Evanston
State
IL
Country
United States
Zip Code
60201
Abraham, Ian; Prabhakar, Ahalya; Hartmann, Mitra J Z et al. (2017) Ergodic Exploration Using Binary Sensing for Nonparametric Shape Estimation. IEEE Robot Autom Lett 2:827-834
Huet, Lucie A; Rudnicki, John W; Hartmann, Mitra J Z (2017) Tactile Sensing with Whiskers of Various Shapes: Determining the Three-Dimensional Location of Object Contact Based on Mechanical Signals at the Whisker Base. Soft Robot 4:88-102
Belli, Hayley M; Yang, Anne E T; Bresee, Chris S et al. (2017) Variations in vibrissal geometry across the rat mystacial pad: base diameter, medulla, and taper. J Neurophysiol 117:1807-1820
Bush, Nicholas E; Solla, Sara A; Hartmann, Mitra Jz (2016) Whisking mechanics and active sensing. Curr Opin Neurobiol 40:178-188
Yu, Yan S W; Graff, Matthew M; Hartmann, Mitra J Z (2016) Mechanical responses of rat vibrissae to airflow. J Exp Biol 219:937-48
Hobbs, Jennifer A; Towal, R Blythe; Hartmann, Mitra J Z (2016) Evidence for Functional Groupings of Vibrissae across the Rodent Mystacial Pad. PLoS Comput Biol 12:e1004109
Yu, Yan S W; Graff, Matthew M; Bresee, Chris S et al. (2016) Whiskers aid anemotaxis in rats. Sci Adv 2:e1600716
Yang, Anne E T; Hartmann, Mitra J Z (2016) Whisking Kinematics Enables Object Localization in Head-Centered Coordinates Based on Tactile Information from a Single Vibrissa. Front Behav Neurosci 10:145
Bush, Nicholas E; Schroeder, Christopher L; Hobbs, Jennifer A et al. (2016) Decoupling kinematics and mechanics reveals coding properties of trigeminal ganglion neurons in the rat vibrissal system. Elife 5:
Huet, Lucie A; Hartmann, Mitra J Z (2016) Simulations of a Vibrissa Slipping along a Straight Edge and an Analysis of Frictional Effects during Whisking. IEEE Trans Haptics 9:158-69

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