Local field potentials and the encoding of whisker deflections by population firing synchrony in thalamic barreloids

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.