Hierarchical Equivalence of Somatosensory Areas I and II for Tactile Processing in the Cerebral Cortex of the Marmoset Monkey

Abstract

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.

Functional Connectivity of the Secondary Somatosensory Cortex of the Rat

“…Retrograde degeneration methods also indicated that VP neurons connect directly to both S1 and S2 in cats and squirrel monkeys (Jones, 1975;Stevens et al, 1993). Finally, cooling of S1 does not change S2 responsiveness to peripheral stimulation in rabbits, opossums, rats, and marmoset monkeys (Murray et al, 1992;Coleman et al, 1999;Heppelmann et al, 2001;Zhang et al, 2001b). These results provide an alternative view, that is, S2 received direct thalamic inputs rather than through a serially organized path by means of S1.…”

“…S1 and S2 hierarchies have been studied by inactivation strategies in many species. Functionally, S2 seemed to be equivalent with S1, because it maintained its responsiveness when S1 was reversibly inactivated in rabbits, opossums, prosimian primates, tree shrews, marmoset monkeys, and rats (Woolsey and Wang, 1945;Garraghty et al, 1991;Murray et al, 1992;Coleman et al, 1999;Heppelmann et al, 2001;Zhang et al, 2001b). When the treatment was reversed in cat and marmoset monkey studies, S1 was similarly found to maintain its responsiveness after S2 inactivation (Turman et al, 1995;Zhang et al, 2001b).…”

An fMRI study of somatosensory‐implicated acupuncture points in stable somatosensory stroke patients

“…SII directly connects not only with the ventral posterior nucleus of the thalamus (37,38), but also with SI in nonhuman primates (39). Electrical stimulation of the human median nerve causes synchronized activity in the neurons of SII contralaterally 20 -30 msec after stimulation, which is coincident with the first responses generated in SI (40).…”

Sensorimotor Integration in S2, PV, and Parietal Rostroventral Areas of the Human Sylvian Fissure

“…In humans, connections between S1 and S2 have never been directly examined, but such connectivity has been inferred previously based on the latency difference between the somatosensory-evoked fields (SEFs) from S1 and the S2 region as measured using EEG and MEG recordings (see Lin and Forss 2002 for a review). Although there is increasing evidence for parallel processing in the somatosensory system (Karhu and Tesche 1999;Zhang et al 1996Zhang et al , 2001, support for serial processing between primary and secondary somatosensory fields comes from neuroanatomical studies of connectivity, cortical deactivation studies, and MEG studies in macaque monkeys and humans (Bohlhalter et al 2002;Felleman and Van Essen 1991;Garraghty et al 1990;Inui et al 2004;Pons et al 1992). More recent studies have shown that although both S2 and PV receive afferents from areas 3b and 1, which process cutaneous inputs, and from area 3a, which processes inputs from proprioceptors (Disbrow et al 2003;Qi et al 2002), they also project to posterior parietal areas (Disbrow et al 2003), including cortex representing the hands in the anterior intraparietal sulcus (AIP) (Lewis and Van Essen 2000).…”