The thalamo-cortical pathway is the crucial sensory gateway into the cerebral cortex. We aimed to determine the nature of the tactile information encoded by neurons in the whisker somatosensory relay nucleus (VPm). We wanted to distinguish whether VPm neurons encode similar stimulus features, acting as a single information channel, or encode diverse features. We recorded responses to whisker deflections that thoroughly explored the space of temporal stimulus variables and identified features to which neurons were selective by reverse correlation. The timescale of the features was typically 1-2 ms, at the limit imposed by our experimental conditions, indicating highly acute feature selectivity. Sensitivity to stimulus kinetics was strikingly diverse. Some neurons (25%) only encoded velocity; others were sensitive to position, acceleration, or more complex features. A minority (19%) encoded two or more features. These results indicate that VPm contains a distributed representation of whisker motion, based on high-resolution kinetic features.

Primary sensory neurons form the interface between world and brain. Their function is well-understood during passive stimulation but, under natural behaving conditions, sense organs are under active, motor control. In an attempt to predict primary neuron firing under natural conditions of sensorimotor integration, we recorded from primary mechanosensory neurons of awake, head-fixed mice as they explored a pole with their whiskers, and simultaneously measured both whisker motion and forces with high-speed videography. Using Generalised Linear Models, we found that primary neuron responses were poorly predicted by whisker angle, but well-predicted by rotational forces acting on the whisker: both during touch and free-air whisker motion. These results are in apparent contrast to previous studies of passive stimulation, but could be reconciled by differences in the kinematics-force relationship between active and passive conditions. Thus, simple statistical models can predict rich neural activity elicited by natural, exploratory behaviour involving active movement of sense organs.DOI: http://dx.doi.org/10.7554/eLife.10696.001

Rats discriminate texture by whisking their vibrissae across the surfaces of objects. This process induces corresponding vibrissa vibrations, which must be accurately represented by neurons in the somatosensory pathway. In this study, we investigated the neural code for vibrissa motion in the ventroposterior medial (VPm) nucleus of the thalamus by single-unit recording. We found that neurons conveyed a great deal of information (up to 77.9 bits/s) about vibrissa dynamics. The key was precise spike timing, which typically varied by less than a millisecond from trial to trial. The neural code was sparse, the average spike being remarkably informative (5.8 bits/spike). This implies that as few as four VPm spikes, coding independent information, might reliably differentiate between 10(6) textures. To probe the mechanism of information transmission, we compared the role of time-varying firing rate to that of temporally correlated spike patterns in two ways: 93.9% of the information encoded by a neuron could be accounted for by a hypothetical neuron with the same time-dependent firing rate but no correlations between spikes; moreover, > or =93.4% of the information in the spike trains could be decoded even if temporal correlations were ignored. Taken together, these results suggest that the essence of the VPm code for vibrissa motion is firing rate modulation on a submillisecond timescale. The significance of such a code may be that it enables a small number of neurons, firing only few spikes, to convey distinctions between very many different textures to the barrel cortex.

A prominent characteristic of neurons in the whisker system is their selectivity to the direction in which a whisker is deflected. The aim of this study was to determine how information about whisker direction is encoded at successive levels of the lemniscal pathway. We made extracellular recordings under identical conditions from the trigeminal ganglion, ventro-posterior medial thalamus (VPM), and barrel cortex while varying the direction of whisker deflection. We found a marked increase in the variability of single unit responses along the pathway. To study the consequences of this for information processing, we quantified the responses using mutual information. VPM units conveyed 48% of the mutual information conveyed by ganglion units, and cortical units conveyed 12%. The fraction of neuronal bandwidth used for transmitting direction information decreased from 40% in the ganglion to 24% in VPM and 5% in barrel cortex. To test whether, in cortex, population coding might compensate for this information loss, we made simultaneous recordings. We found that cortical neuron pairs conveyed 2.1 times the mutual information conveyed by single neurons. Overall, these findings indicate a marked transformation from a subcortical neural code based on small numbers of reliable neurons to a cortical code based on populations of unreliable neurons. However, the basic form of the neural code in ganglion, thalamus, and cortex was similar-at each stage, the first poststimulus spike carried the majority of the information.

Communication in the nervous system occurs by spikes: the timing precision with which spikes are fired is a fundamental limit on neural information processing. In sensory systems, spike-timing precision is constrained by first-order neurons. We found that spike-timing precision of trigeminal primary afferents in rats and mice is limited both by stimulus speed and by electrophysiological sampling rate. High-speed video of behaving mice revealed whisker velocities of at least 17,000°/s, so we delivered an ultrafast "ping" (Ͼ50,000°/s) to single whiskers and sampled primary afferent activity at 500 kHz. Median spike jitter was 17.4 s; 29% of neurons had spike jitter Ͻ 10 s. These results indicate that the input stage of the trigeminal pathway has extraordinary spike-timing precision and very high potential information capacity. This timing precision ranks among the highest in biology.

In any sensory system, the primary afferents constitute the first level of sensory representation and fundamentally constrain all subsequent information processing. Here, we show that the spike timing, reliability, and stimulus selectivity of primary afferents in the whisker system can be accurately described by a simple model consisting of linear stimulus filtering combined with spike feedback. We fitted the parameters of the model by recording the responses of primary afferents to filtered, white noise whisker motion in anesthetized rats. The model accurately predicted not only the response of primary afferents to white noise whisker motion (median correlation coefficient 0.92) but also to naturalistic, texture-induced whisker motion. The model accounted both for submillisecond spike-timing precision and for non-Poisson spike train structure.Wefoundsubstantialdiversityintheresponsesoftheafferentpopulation,butthisdiversitywasaccuratelycapturedbythemodel:a2Dfilter subspace, corresponding to different mixtures of position and velocity sensitivity, captured 94% of the variance in the stimulus selectivity. Our results suggest that the first stage of the whisker system can be well approximated as a bank of linear filters, forming an overcomplete representation of a low-dimensional feature space.

During active somatosensation, neural signals expected from movement of the sensors are suppressed in the cortex, whereas information related to touch is enhanced. This tactile suppression underlies low-noise encoding of relevant tactile features and the brain’s ability to make fine tactile discriminations. Layer (L) 4 excitatory neurons in the barrel cortex, the major target of the somatosensory thalamus (VPM), respond to touch, but have low spike rates and low sensitivity to the movement of whiskers. Most neurons in VPM respond to touch and also show an increase in spike rate with whisker movement. Therefore, signals related to self-movement are suppressed in L4. Fast-spiking (FS) interneurons in L4 show similar dynamics to VPM neurons. Stimulation of halorhodopsin in FS interneurons causes a reduction in FS neuron activity and an increase in L4 excitatory neuron activity. This decrease of activity of L4 FS neurons contradicts the "paradoxical effect" predicted in networks stabilized by inhibition and in strongly-coupled networks. To explain these observations, we constructed a model of the L4 circuit, with connectivity constrained by in vitro measurements. The model explores the various synaptic conductance strengths for which L4 FS neurons actively suppress baseline and movement-related activity in layer 4 excitatory neurons. Feedforward inhibition, in concert with recurrent intracortical circuitry, produces tactile suppression. Synaptic delays in feedforward inhibition allow transmission of temporally brief volleys of activity associated with touch. Our model provides a mechanistic explanation of a behavior-related computation implemented by the thalamocortical circuit.

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...