Primary somatosensory cortical neuronal activity during monkey's detection of perceived change in tooth-pulp stimulus intensity.

Abstract

To elucidate the functional properties of primary somatosensory cortical neurons for the perception of tooth-pulp sensation, neuronal activity was recorded from the primary somatosensory cortex (SI) in awake behaving monkeys. Monkeys were trained to detect changes in tooth-pulp stimulus intensity applied to the upper canine or incisor tooth pulp. Stimulus intensities applied to the tooth pulp were multiples of the threshold intensity for the jaw opening reflex (1.0 T) elicited by tooth-pulp stimulation. When monkeys pressed a button, baseline electrical pulses (V1: 0.5 T, 1.0 T, 2.0 T, or 3.0 T) were applied to the tooth pulp. After 4-8 s, a V2 stimulus (0.3 T, 0.5 T, 1.0 T, or 2.0 T) was added to V1. Percent escapes at V1 stimulus intensity of 0.5 T and 1.0 T were approximately 10%, 22% at 2.0 T, and 40% at 3.0 T (total of 1,997 trials). A total of 862 single units were recorded from the SI. Thirty-seven SI neurons responded to electrical stimulation of the tooth pulp (tooth-pulp-driven neurons; TPNs), 139 SI neurons responded to tactile stimulation of the lateral face area, 90 to upper lip and 99 to lower lip, 44 to tongue and 102 to periodontal membrane, whereas 351 SI neurons were not responsive to tactile stimulation of the orofacial regions. Thirty of 37 TPNs were recorded long enough to test with V1 stimuli ranging from 0.5 T to 3.0 T. Eleven of 30 TPNs linearly increased their firing frequency following increases in stimulus intensity (encoding TPNs), whereas 19 did not (nonencoding TPNs). Mean first spike latency of encoding TPNs was 24.8 +/- 1.7 ms (n = 11), that of nonencoding TPNs was 23.6 +/- 1.5 ms (n = 19), and that of unclassified TPNs was 24.7 +/- 3.7 ms (n = 7). TPNs were distributed in the areas 1-2, 3a, and 3b within the oral projection area and the transition zone between the face and oral projection areas of the SI. All of them received inputs from the intraoral structures, facial skin, or both. The firing frequency of eight encoding and nonencoding TPNs was correlated with detection latency at stimulus intensities of 0.5 and 1.0 T. On the other hand, when the baseline stimulus was increased to 2.0 T and 3.0 T, the discharge of most TPNs did not increase in firing frequency with the reduction in detection latency. These results indicate that the discharge rates of some SI TPNs are correlated with detection latency at near-noxious threshold and noxious stimulus intensities. These findings suggest that some TPNs are involved in the sensory-discriminative aspect of tooth-pulp sensation in the near-pain threshold and pain ranges.