Local Field Potentials and the Encoding of Whisker Deflections by Population Firing Synchrony in Thalamic Barreloids

Abstract

In layer IV of rat somatosensory cortex, barrel circuitry is highly sensitive to thalamic population firing rates during the first few milliseconds of the whisker-evoked response. This sensitivity of barrel neurons to thalamic firing synchrony was inferred previously from analysis of simulated barrel circuitry and from single-unit recordings performed one at a time. In this study, we investigate stimulus-dependent synchronous activity in the thalamic ventral posteromedial nucleus (VPm) using the more direct approach of local field potential (LFP) recording. We report that thalamic barreloid neurons generate larger magnitude LFP responses to principal versus adjacent whiskers, to preferred versus nonpreferred movement directions, and to high- versus low-velocity/acceleration deflections. Responses were better predicted by acceleration than velocity, and they were insensitive to the final amplitude of whisker deflection. Importantly, reliable and robust stimulus/response relationships were found only for the initial 1.2-7.5 ms of the thalamic LFP response, reflecting arrival of afferent information from the brain stem. Later components of the thalamic response, which are likely to coincide with arrival of inhibitory inputs from the thalamic reticular nucleus and excitatory inputs from the barrel cortex itself, are variable and poorly predicted by stimulus parameters. Together with previous results, these findings underscore a critical role for thalamic firing synchrony in the encoding of small but rapidly changing perturbations of specific whiskers in particular directions.

Synaptic Responses to Whisker Deflections in Rat Barrel Cortex as a Function of Cortical Layer and Stimulus Intensity

“…These results are consistent with the multiunit recordings by Pinto et al (2000) and are comparable with the synaptic responses of barrel cortex neurons shown here [compare Fig. 6 A in Temereanca and Simons (2003) with our Fig. 6].…”

“…Here, we chose to plot our measurements against velocity only and not acceleration, because this was the parameter that could be more accurately quantified (see Materials and Methods). We acknowledge that acceleration is also increasing and could in fact be the more important parameter (Temereanca and Simons, 2003) of the deflection determining the synaptic response. However, the main thrust of this work is not to characterize the cortical responses to either velocity or acceleration specifically but to understand the effect of increasing stimulus intensity (represented by the velocity-acceleration of the deflection) on the composition of synaptic responses in the different layers of the barrel cortex.…”

“…In a related study, recordings of local field potentials (LFPs) from VB (Temereanca and Simons, 2003) demonstrated that increasing the velocity-acceleration of whisker deflection reduces the latency to onset, reduces the latency to peak, and increases the amplitude of the LFP response. These results are consistent with the multiunit recordings by Pinto et al (2000) and are comparable with the synaptic responses of barrel cortex neurons shown here [compare Fig.…”

“…In the rodent barrel system, neurons are exquisitely sensitive to velocity (Gibson and Welker, 1983;Ito, 1985;Shoykhet et al, 2000;Deschenes et al, 2003;Temereanca and Simons, 2003;Lee and Simons, 2004) and acceleration (Temereanca and Simons, 2003) at which the corresponding principal whisker in the mystacial pad is deflected. As rodents explore, their whiskers repetitively move back and forth at 5-15 Hz (Welker et al, 1964;Carvell and Simons, 1995;Berg and Kleinfeld, 2003) contacting surfaces and objects, causing small angular deflections at the base of the whiskers.…”

“…As rodents explore, their whiskers repetitively move back and forth at 5-15 Hz (Welker et al, 1964;Carvell and Simons, 1995;Berg and Kleinfeld, 2003) contacting surfaces and objects, causing small angular deflections at the base of the whiskers. Encoding deflection velocity-acceleration is probably critical for discriminating between surfaces of different textures (Dykes, 1975;Temereanca and Simons, 2003), a task that rats are capable of performing (Guic-Robles et al, 1989;Carvell and Simons, 1990). It may also be critical for determining the distance to objects (Cowan et al, 2004), because striking a whisker at different distances from the face generates deflections with different angular velocities.…”