Hierarchical equivalence of somatosensory areas I and II for tactile processing in the cerebral cortex of the marmoset monkey

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 organiza tional scheme for thalamocortical tactile processing as appears to be the c ase in nonprimate mammals. Inactivation of SII was achieved when the temper ature over SII was lowered to less than or equal to 12 degreesC, as indicat ed 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 n eurons located at the margin beneath the block. The effect of SII inactivat ion 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 t here was a small reduction in amplitude and inconsistent effects in the rem aining two. Responsiveness to controlled tactile stimuli was examined quant itatively in 31 individual SI neurons of different functional classes befor e, during, and after the inactivation of SII. Tactile responsiveness in ind ividual SI neurons was never abolished by SII inactivation, remaining uncha nged in 20 neurons (65%) while undergoing some reduction in the remaining 1 1 SI neurons (35%). This reduction of tactile responsiveness in one-third o f SI neurons is most likely attributable to a removal of a facilitatory inf luence emanating from SII, based on the observation that background activit y of the affected neurons was also reduced. Furthermore, phase locking of S I responses to vibrotactile stimulation was unchanged when SII was inactiva ted. The retention of responsiveness in SI neurons when SII was inactivated by cooling in the marmoset demonstrates that tactile inputs can reach SI w ithout traversing an indirect, serially organized path through SII. The pre sent results, together with our previous observations that responsiveness i n the majority of SII neurons survived SI inactivation, demonstrate that th ere is a parallel organization of the SI and SII areas for tactile processi ng in the marmoset monkey and that SI and SII occupy hierarchically equival ent positions in a parallel processing network. There is therefore no longe r justification for the view that there are fundamental differences in the organization of thalamocortical tactile processing for SI and SII between s imian primates, in general, and other mammals.