Frequency-dependent response of SI RA-class neurons to vibrotactile stimulation of the receptive field

Three types of experiment were carried out on anesthetized monkeys and cats. In the first, spike discharge activity of rapidly adapting (RA) SI neurons was recorded extracellularly during the application of different frequencies of vibrotactile stimulation to the receptive field (RF). The second used the same stimulus conditions to study the response of RA-I (RA) cutaneous mechanoreceptive afferents. The third used optical intrinsic signal (OIS) imaging and extracellular neurophysiological recording methods together, in the same sessions, to evaluate the relationship between the SI optical and RA neuron spike train responses to low- vs high-frequency stimulation of the same skin site. RA afferent entrainment was high at all frequencies of stimulation. In contrast, SI RA neuron entrainment was much lower on average, and was strongly frequency-dependent, declining in near-linear fashion from 6 to 200 Hz. Even at 200 Hz, however, unambiguous frequencyfollowing responses were present in the spike train activity of some SI RA neurons. These entrainment results support the "periodicity hypothesis" of Mountcastle et al. ( J Neurophysiol 32: 452-484, 1969) that the capacity to discriminate stimulus frequency over the range 5-50 Hz is attributable to the ability of SI RA pyramidal neurons to discharge action potentials in consistent temporal relationship to stimulus motion, and raise the possibility that perceptual frequency discriminative capacity at frequencies between 50 and 200 Hz might be accounted for in the same way. An increase in vibrotactile stimulus frequency within the range 6-200 Hz consistently resulted in an increase in RA afferent mean spike firing rate (M FR). SI RA neuron M FR also increased as frequency increased between 6 and 50 Hz, but declined as stimulus frequency was increased over the range 50-200 Hz. At stimulus frequencies > 100 Hz, and at positions in the RF other than the receptive field center (RF center ), SI RA neuron MFR declined sharply within 0.5-2s of stimulus onset and rebounded transiently upon stimulus termination. In contrast, when the stimulus was applied to the RF center, MFR increased with increasing frequency and tended to remain well maintained throughout the period of high-frequency stimulation. The evidence obtained in "combined" OIS imaging and extracellular microelectrode recording experiments suggests that SI RA neurons with an RF center that corresponds to the stimulated skin site occupy small foci within the much larger SI region activated by same-site cutaneous flutter stimulation, while for the RA neurons located elsewhere in the large SI region activated by a flutter stimulus, the stimulus site and RF center are different.