Response properties of whisker-related neurons in rat second somatosensory cortex

Abstract

In addition to a primary somatosensory cortex (SI), the cerebral cortex of all mammals contains a second somatosensory area (SII); however, the functions of SII are largely unknown. Our aim was to explore the functions of SII by comparing response properties of whisker-related neurons in this area with their counterparts in the SI. We obtained extracellular unit recordings from narcotized rats, in response to whisker deflections evoked by a piezoelectric device, and compared response properties of SI barrel (layer IV) neurons with those of SII (layers II to VI) neurons. Neurons in both cortical areas have similar response latencies and spontaneous activity levels. However, SI and SII neurons differ in several significant properties. The receptive fields of SII neurons are at least five times as large as those of barrel neurons, and they respond equally strongly to several principal whiskers. The response magnitude of SII neurons is significantly smaller than that of neurons in SI, and SII neurons are more selective for the angle of whisker deflection. Furthermore, whereas in SI fast-spiking (inhibitory) and regular-spiking (excitatory) units have different spontaneous and evoked activity levels and differ in their responses to stimulus onset and offset, SII neurons do not show significant differences in these properties. The response properties of SII neurons suggest that they are driven by thalamic inputs that are part of the paralemniscal system. Thus whisker-related inputs are processed in parallel by a lemniscal system involving SI and a paralemniscal system that processes complimentary aspects of somatosensation.

FIG. 1

A: representative waveforms recorded from a regular spike unit (RSU) and a fast spike unit (FSU). RSUs have longer duration waveforms. B: distribution of response onset latency of second somatosensory cortex (SII) and primary somatosensory cortex (SI) neurons. SI and SII neurons and neurons in different layers of SII have similar onset latencies. P values computed from Kolmogorov-Smirnov (K-S) tests. Depicted are the median and 1st and 3rd quartiles of the data distribution. Whiskers represent data within 1.5 times the range from the 1st to the 3rd quartile. C and D: representative peristimulus time histograms (PSTHs) constructed from responses of an SI barrel (layer IV) neuron (C) and an SII neuron (D) to a 200-ms ramp and hold whisker deflection at time t = 0. In these and subsequent PSTHs, horizontal broken lines depict response magnitude levels exceeding (99% CI) spontaneous activity levels (computed from a 200-ms period preceding stimulus onset; note different ordinate scales).

FIG. 2

Response kinetics of SII neurons. A: PSTH showing the characteristic response pattern recorded from 90.3% of SII neurons. These neurons had a biphasic response, responding to stimulus onset (ON) and stimulus offset (OFF). B: in addition to the ON and OFF responses, in 9.7% of SII neurons, there was a secondary response beginning 146.33 ± 42.07 ms following the ON response and lasting 35.0 ± 27.9 ms. This category of cells included both RSUs and FSUs. C: box-plots of the distribution of response magnitudes of the different classes of neurons. The response magnitude of SII cells was significantly smaller than SI barrel cells, but SII-RSUs and SII-FSUs had similar response magnitudes. D: OFF-ON: response magnitude ratios of SII-FSUs, SII-RSUs, and SI-RSUs were statistically indistinguishable. E: response duration of SI neurons was longer than SII cells due to the fact that a larger proportion of SI barrel neurons were slowly adapting. All statistical comparisons made with K-S tests.

FIG. 3

Receptive field size of SII neurons, determined from 58 cells for which ≥5 whiskers were stimulated. A: PSTHs depicting responses of a layer V SII neuron to stimulation of different whiskers. Indicated above each PSTH are the whisker stimulated, the response onset latency (ms), and the response magnitude (spikes/stimulus). Stimulation of different whiskers results in responses with similar latencies, but different magnitude. B: relative differences in onset latency to stimulation of different whiskers, computed for all 58 neurons. For each neuron, latencies were normalized to responses to the whisker evoking the shortest latency response (W-1; see text for additional details). Error bars depict ±99% CIs. As a population, SII neurons responded with statistically indistinguishable onset latencies to stimulation of 9 different whiskers. C: similar analysis applied to response magnitudes, normalized to responses of the whisker evoking the largest response (W-1). As a population, SII neurons responded to 3 whiskers with similar response magnitudes [defined as the principal whiskers (PWs)] and with significantly smaller magnitude responses to the adjacent whiskers (AWs). D: neurons in all layers of SII had a similar number of PWs. E: onset latencies of responses to PWs were significantly shorter that those to AWs. All statistical comparisons made with K-S test.

FIG. 4

Angular selectivity of SII neurons. PSTHs of responses of a well-tuned (category 6, A) and a poorly tuned (category 0, B) SII neuron to deflection of a single whisker in 8 different directions. Polar plots were constructed by plotting the normalized response magnitude against the direction of whisker deflection. 0° represents deflection in the caudal direction and 90° is deflection in the dorsal direction. C: histogram comparing the distribution of angular tuning of SII neurons with those of SI barrels cells (the latter reproduced, with permission, from Simons and Carvell 1989). Angular tuning was defined as the number of deflection angles evoking responses that are statistically smaller than that to the maximally activating angle. Category 0 represents the least-tuned cells (cells that respond equally to all deflection angles) and category 7 represents the best-tuned neurons. A larger proportion of SII neurons have high angular tuning.