Responsiveness of the first somatosensory area (SI) of the cerebral cortex was investigated in the marmoset monkey (Callithrix jacchus) in association with cooling-induced, reversible inactivation of the second somatosensory area, SII. The aim was to determine whether SI responsiveness to peripheral tactile stimulation depends on SII and therefore whether SI and SII in the marmoset occupy hierarchically equivalent positions in a parallel organizational scheme for thalamocortical tactile processing as appears to be the case in nonprimate mammals. Inactivation of SII was achieved when the temperature over SII was lowered to < or =12 degrees C, as indicated by abolition of the SII-evoked potentials generated by brief tap stimuli to the hand or foot, and by abolition of tactile responses in single SII neurons located at the margin beneath the block. The effect of SII inactivation on SI-evoked potentials was examined in 16 experiments by simultaneous recording of the SI- and SII-evoked potentials. SI-evoked potentials were never abolished and remained unaffected in 11 cases. In three experiments there was a small reduction in amplitude and inconsistent effects in the remaining two. Responsiveness to controlled tactile stimuli was examined quantitatively in 31 individual SI neurons of different functional classes before, during, and after the inactivation of SII. Tactile responsiveness in individual SI neurons was never abolished by SII inactivation, remaining unchanged in 20 neurons (65%) while undergoing some reduction in the remaining 11 SI neurons (35%). This reduction of tactile responsiveness in one-third of SI neurons is most likely attributable to a removal of a facilitatory influence emanating from SII, based on the observation that background activity of the affected neurons was also reduced. Furthermore, phase locking of SI responses to vibrotactile stimulation was unchanged when SII was inactivated. The retention of responsiveness in SI neurons when SII was inactivated by cooling in the marmoset demonstrates that tactile inputs can reach SI without traversing an indirect, serially organized path through SII. The present results, together with our previous observations that responsiveness in the majority of SII neurons survived SI inactivation, demonstrate that there is a parallel organization of the SI and SII areas for tactile processing in the marmoset monkey and that SI and SII occupy hierarchically equivalent positions in a parallel processing network. There is therefore no longer justification for the view that there are fundamental differences in the organization of thalamocortical tactile processing for SI and SII between simian primates, in general, and other mammals.

Transmission from single, identified hair follicle afferent (HFA) nerve fibers to their target neurons of the cuneate nucleus was examined in anesthetized cats by means of paired recording from individual cuneate neurons and from fine, intact fascicles of the lateral branch of the superficial radial nerve in which it is possible to identify and monitor the activity of each group II fiber. Selective activation of individual HFA fibers was achieved by means of focal vibrotactile skin stimulation. Forearm denervation precluded inputs from sources other than the monitored HFA sensory fiber. Transmission characteristics were analyzed for 21 HFA fiber-cuneate neuron pairs in which activity in the single HFA fiber of each pair reliably evoked spike output from the target neuron at a fixed latency. As the cuneate responses to each HFA impulse often consisted of 2 or 3 spikes, in particular at HFA input rates up to approximately 20 imp/s, the synaptic linkage displayed potent amplification and high-gain transmission, characteristics that were confirmed quantitatively in measures of transmission security and cuneate spike output measures. In response to vibrotactile stimuli, the tight phase locking in the responses of single HFA fibers was well retained in the cuneate responses for vibration frequencies up to approximately 200 Hz. On measures of vector strength, the phase locking declined across the synaptic linkage by no more than approximately 10% at frequencies up to 100 Hz. However, limitations on the impulse rates generated in both the HFA fibers their associated cuneate neurons meant that the impulse patterns could not directly signal information about the vibration frequency above 50-100 Hz. Although single HFA fibers are also known to have secure synaptic linkages with spinocervical tract neurons, it is probable that this linkage lacks the capacity of the HFA-cuneate synapse for conveying precise temporal information, in an impulse pattern code, about the frequency parameter of vibrotactile stimuli.

Organization of somatosensory areas I and II in marsupial cerebral cortex: parallel processing in the possum sensory cortex. Controversy exists over the organization of mammalian thalamocortical somatosensory networks. An issue of particular contention is whether the primary and secondary somatosensory areas of cortex (SI and SII) are organized in a parallel or serial scheme for processing tactile information. The current experiments were conducted in the anesthetized brush-tail possum (Trichosurus vulpecula) to determine which organizational scheme operates in marsupials, which have taken a quite different evolutionary path from the placental species studied in this respect. The effect of rapid reversible inactivation of SI, achieved by localized cortical cooling, was examined on both evoked potential and single neuron responses in SII. SI inactivation was without effect on the amplitude, latency, and time course of SII-evoked potentials, indicating that the transient inputs responsible for the SII-evoked potential reach SII directly from the thalamus rather than traversing an indirect serial route via SI. Tactile responsiveness was examined quantitatively before, during, and after SI inactivation in 16 SII neurons. Fourteen were unchanged in their responsiveness, and two showed some reduction, an effect probably attributable to the loss of a facilitatory influence exerted by SI on a small proportion of SII neurons. The temporal precision and pattern of SII responses to dynamic forms of mechanical stimuli were unaffected, and temporal dispersion in the SII response bursts was unchanged in association with SI inactivation. In conclusion, the results establish that, within this marsupial species, tactile inputs can reach SII directly from the thalamus and are not dependent on a serially organized path through SI. A predominantly parallel organizational scheme for SI and SII operates in this representative of the marsupial order, as it does in a range of placental mammals including the cat and rabbit, the tree shrew and prosimian galago, and at least one primate representative, the marmoset monkey.