Parallel processing in cerebral cortex of the marmoset monkey: effect of reversible SI inactivation on tactile responses in SII.
1. Responsiveness within the hand region of the second somatosensory area of cortex (SII) was investigated in the marmoset monkey (Callithrix jacchus) in association with cooling-induced, reversible inactivation of the primary somatosensory area, SI. The aims were to determine whether thalamocortical systems in this primate species are organized according to a serial scheme in which tactile information is conveyed from the thalamus to SI and thence to SII as the next hierarchical level of processing and to establish whether primates are fundamentally different, in this respect, from mammals in which tactile information is conveyed in parallel from the thalamus to both SI and SII. 2. Inactivation of the SI had area was achieved when the temperature at the face of the silver cooling block over this SI region was lowered to < or = 13 degrees C. Inactivation was confirmed by abolition of the SI surface potential evoked by a brief tap stimulus to the hand and by the abolition of responsiveness in single SI neurons located beneath and around the edge of the block. 3. The effect of SI inactivation on SII-evoked potentials was investigated in 20 experiments by simultaneous recording of the SI- and SII-evoked potentials. The SII response was never abolished and was unchanged in the majority (12/20) of experiments. In the remainder, the SII-evoked potentials underwent a reduction in amplitude that was usually < 30% but never > 50%. 4. Tactile responsiveness was examined quantitatively in 47 individual SII neurons of different functional classes before, during, and after the inactivation of SI. Controlled tactile stimuli consisted of trains of sinusoidal vibration or rectangular pulses delivered to the glabrous or hairy skin of the hand. 5. Thirteen of the 47 SII neurons (28%) were unaffected in their response levels in association with SI inactivation. The remaining 34 SII neurons underwent some reduction in responsiveness, but in only 6% (3/47) was responsiveness abolished by SI inactivation. As the same range of functional classes of tactile neurons were represented among the affected and unaffected SII neurons, there was no evidence for a differential susceptibility among SII tactile neurons to the effect of SI inactivation. 6. Where reductions in amplitude of the SII-evoked potential or in response levels of SII neurons were observed, the effects were not attributable to direct spread of cooling from SI to the SII hand area as there was no cooling-induced prolongation of either the evoked potential or spike waveform in SII, an effect that is known to precede cooling-induced reductions in responsiveness. 7. These lines of evidence indicate that reductions in SII responsiveness in association with SI inactivation may be attributable to a loss of a background facilitatory influence rather than to a blockage of a component of peripheral input that comes over a putative serial path to SII via SI. First, as SI was cooled, there was a progressive increase in latency and time course of the SI responses before their disappearance, but no comparable delay in the SII responses as might be expected if SI were placed earlier than SII in a strict hierarchical scheme of thalamocortical processing. Second, SI inactivation failed to bring about a tightening in the phase-locking of SII responses to vibrotactile stimuli as might have been expected if the inputs to the SII neurons come via both a direct path from the thalamus and an indirect intracortical path via SI. Blockage of the indirect intracortical pathway through SI might be expected to reduce temporal dispersion in the input to SII neurons and result in an improvement in phase-locking in the SII responses to skin vibration. Third, the background activity of some SII neurons was reduced during SI inactivation along with the reduction in their responses to tactile stimulation.