Spatial gradients and inhibitory summation in the rat whisker barrel system

Abstract

1. Extracellular single-unit recordings and controlled whisker stimuli were used to compare response properties of cells in the barreloids of the ventral posterior medial nucleus of the thalamus and the barrels in the rat primary somatosensory cortex. Whiskers were deflected alone or in combinations involving up to four immediately adjacent whiskers to assess their relative inhibitory and excitatory contributions to individual receptive fields. Quantitative data were obtained from 51 thalamocortical units (TCUs), 79 "regular-spiking" barrel neurons (RSUs), and 5 "fast-spiking" barrel neurons (FSUs) in 28 normal female adult rats. 2. A random-noise generator was used to produce small, continuously varying whisker movements that were applied to one to four adjacent whiskers while the principal (columnar) whisker was displaced with the use of a ramp-and-hold deflection. RSUs displayed adjacent whisker-evoked inhibition that increased as the number of adjacent whiskers stimulated was incremented. Asymptotic levels of inhibition were reached with the application of the noise stimulus to two or three adjacent whiskers depending on which particular combinations were deflected. By contrast, TCUs and FSUs showed weak, or no, surround inhibition. 3. As the number of adjacent whiskers stimulated increased, the background (prestimulus) activity in TCUs and FSUs increased, whereas displayed background activity in RSUs was relatively unaffected. The increase in background activity observed in the FSUs is hypothesized to mediate adjacent whisker-evoked inhibition in the RSUs. 4. A spatial gradient of adjacent whisker inhibition was observed in RSUs. The caudally adjacent whisker evoked more inhibition than the rostrally adjacent whisker, and the ventral more than the dorsal. A cortical origin for the gradient is suggested by the finding that TCUs did not show a spatial inhibitory gradient. 5. As the noise stimulus was applied to an increasing number of adjacent whiskers, RSUs became more sharply tuned for deflection angles. Neither TCUs nor FSUs showed increases in angular tuning. 6. Inhibition worked disproportionately in RSUs to inhibit those responses that were initially the least robust. For example, inhibition was most effective at reducing responses to nonpreferred versus preferred whisker deflection angles. 7. To assess the principal whisker's effect on adjacent whisker excitatory responses, the noise stimulus was applied to the principal whisker. In RSUs, principal whisker-evoked inhibition was more potent than adjacent whisker-evoked inhibition. FSUs were excited to a greater extent by the application of the noise stimulus to the principal whisker than to adjacent whiskers. TCUs did not display principal whisker-evoked inhibition. 8. Inhibition within the barrel serves as a contrast enhancement mechanism to differentiate small versus large magnitude responses. Less vigorous responses, such as those associated with perturbations of noncolumnar whiskers and inputs from nonoptimal deflection angles, are more strongly suppressed. During active touch, when many whiskers simultaneously palpate an object, these inhibitory interactions could effectively increase the "principal whiskerness" of the cortical column.