Prediction of Primary Somatosensory Neuron Activity During Active Tactile Exploration

Abstract

12Primary sensory neurons form the interface between world and brain. Their function is well-13 understood during passive stimulation but, under natural behaving conditions, sense organs 14 are under active, motor control. In an attempt to predict primary neuron firing under natural 15 conditions of sensorimotor integration, we recorded from primary mechanosensory neurons 16 of awake, head-fixed mice as they explored a pole with their whiskers, and simultaneously 17 measured both whisker motion and forces with high-speed videography. Using Generalised 18 Linear Models, we found that primary neuron responses were poorly predicted by kinematics 19 but well-predicted by rotational forces acting on the whisker: both during touch and free-air 20 whisker motion. These results are discrepant with previous studies of passive stimulation, but 21 could be reconciled by differences in the kinematics-force relationship between active and 22 passive conditions. Thus, simple statistical models can predict rich neural activity elicited by 23 natural, exploratory behaviour involving active movement of the sense organs. 24 25 26 45 force ('moment') acting on the whisker, but not by whisker angle and its derivativesa 46 finding at odds with passive stimulation studies (Gibson 1983, Lichtenstein et al 1990; Bale 47 et al 2013).48 49 50 4 RESULTS:51 Primary whisker neuron activity during object exploration is predicted by whisker 52 bending moment 53 We recorded the activity of single PWNs from awake mice ( Figure 1A, E`, Figure 1-figure 54 supplement 1) as they actively explored a metal pole with their whiskers (N = 20 units). At 55 the same time, we recorded whisker motion and whisker shape using high-speed videography 56 (1000 frames/s, Figure 1D, Figure 1-figure supplement 2). Since each PWN innervates a 57 single whisker follicle, we tracked the 'principal whisker' of each recorded unit from frame 58 to frame, and extracted both the angle and curvature of the principal whisker in each video 59 frame (total 1,496,033 frames; Figure 1B-E; Bale et al. 2015). Whiskers are intrinsically 60 curved, and the bending moment on a whisker is proportional to how much this curvature 61 changes due to object contact (Birdwell et al. 2007): we therefore used 'curvature change' as 62 a proxy for bending moment (O'Connor et al. 2010a). Whisker-pole contacts caused 63 substantial whisker bending (curvature change), partially correlated with the whisker angle 64 (Figures 1E, 4E) and, consistent with Szwed et al. (2003) and Leiser and Moxon (2007), 65 robust spiking (Figures 1E, 2E). 66To test between candidate encoding variables, our strategy was to determine how accurately 67 it was possible to predict PWN activity from either the angular position (kinematics) or 68 curvature change (mechanics) of each recorded unit's principal whisker. To predict spikes 69 from whisker state, we used Generalised Linear Models (GLMs) (Figure 2A). GLMs, driven 70 by whisker angle, have previously been shown to provide a simple but accurate description 71 of...

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The Sensorimotor Basis of Whisker-Guided Anteroposterior Object Localization in Head-Fixed Mice

“…This leaves the perplexing question of how azimuthal angle at touch can influence choice, because the azimuthal angle of the whisker is not directly encoded by primary sensory afferents [40][41][42][43][44][45]. An influential model has been proposed for how the brain could compute this angle from mentally accessible timevarying features.…”

The Cellular and Mechanical Basis for Response Characteristics of Identified Primary Afferents in the Rat Vibrissal System

“…The rodent vibrissal (whisker) system offers a unique opportunity to probe responses of primary afferents to well-controlled tactile stimulation [3,6,7]. Two features of this system make it a particularly appropriate model for the study of receptor coding properties, complementary to study of mouse hairy skin and the primate hand.…”

“…First, there are no mechanoreceptors along the vibrissa length; instead, all tactile information is transmitted to the follicle at the whisker base [8,9]. Well-established models of vibrissal mechanics [10][11][12] allow tactile input to the follicle to be precisely quantified [6,7,13,14]. Second, the follicle incorporates diverse mechanoreceptor types [8], many of which are analogous to those in the hand.…”