Parallel processing in cerebral cortex of the marmoset monkey: effect of reversible SI inactivation on tactile responses in SII

Abstract

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 disappearan...

Parallel Processing of Nociceptive and Non-nociceptive Somatosensory Information in the Human Primary and Secondary Somatosensory Cortices: Evidence from Dynamic Causal Modeling of Functional Magnetic Resonance Imaging Data

“…Strong intrinsic connections between S1 and S2 are also compatible with the observation that transcranial magnetic stimulation over S1 can disrupt tactile discrimination in humans not only through a direct effect on the processing of tactile input in S1 but also through an indirect effect on the processing of tactile input in S2 (Cohen et al, 1991;Knecht et al, 2003;Hannula et al, 2008). Finally, it is important to mention that the observations suggesting that the responses elicited in S2 are relayed in S1 (Pons et al, 1992) are in contradiction with the findings of Zhang et al (1996), showing that in higher primates the responses to non-nociceptive somatosensory stimuli in S2 are mostly unaffected by the reversible inactivation of S1 by cooling, thus indicating that the bulk of the inputs triggering the responses in S2 are, in fact, not relayed through S1. Allison et al (1989a,b) used direct intracranial recordings performed in patients to observe that non-nociceptive somatosensory stimuli elicit responses of earlier latency in S1 compared with S2.…”

“…This difference in hierarchical organization has been interpreted as the result of an evolutionary shift from a phylogenetically older parallel organization to a more recent serial organization of somatosensory processing in S1 and S2 (Mountcastle, 2005). However, a small number of studies have suggested the opposite: that, even in higher primates, non-nociceptive somatosensory input is processed in parallel in S1 and S2 Zhang et al, 1996Zhang et al, , 2001Karhu and Tesche, 1999).…”

The physiology and psychology of selective attention to touch

“…This assumption has been tested in a number of different species by anatomical and inactivation studies (58)(59)(60)(61)(62)(63)(64)(65)(66)(67)(68)(69)(70).…”

Response Properties of Whisker-Related Neurons in Rat Second Somatosensory Cortex

“…However, there is also evidence that visual information is processed in parallel by multiple cortical areas (Herkenham 1980;Weyand and Swadlow 1986). A similar ambiguity characterizes somatosensory cortical regions, with evidence existing for both serial and parallel processing by different cortical areas (Burton 1991;Coleman et al 1999; Dykes 1983;Pons et al 1992;Turman et al 1995;Zhang et al 1996).…”

“…However, there is also evidence that visual information is processed in parallel by multiple cortical areas (Herkenham 1980;Weyand and Swadlow 1986). A similar ambiguity characterizes somatosensory cortical regions, with evidence existing for both serial and parallel processing by different cortical areas (Burton 1991;Coleman et al 1999; Dykes 1983;Pons et al 1992;Turman et al 1995;Zhang et al 1996).In rodents, stimulation of the mystacial vibrissae (whiskers) evokes responses both in the first somatosensory ("barrel") cortex (SI) and in the second somatosensory cortex (SII; so named because it was discovered later than SI; White 1987). However, apart from the fact that whisker-related neurons in SII have large receptive fields (Carvell and Simons 1986;Fabri and Burton 1991;Remple et al 2003), relatively little is known about the functional organization of this cortical area.…”