Ipsilateral Input Modifies the Primary Somatosensory Cortex Response to Contralateral Skin Flutter

Abstract

We recorded the optical intrinsic signal response of squirrel monkey primary somatosensory cortex (SI) to 25 Hz vibrotactile ("flutter") stimulation applied independently to the thenar eminence on each hand and also to bilateral (simultaneous) stimulation of both thenars. The following observations were obtained in every subject (n ϭ 5). (1) Ipsilateral stimulation was accompanied by an increase in absorbance within the SI hand region substantially smaller than the absorbance increase evoked by contralateral stimulation. (2) The absorbance increase evoked by simultaneous bilateral stimulation was smaller (by ϳ30%) than that evoked by contralateral stimulation. (3) The spatiointensive pattern of the SI response to bilateral flutter was distinctly different than the pattern that accompanied contralateral flutter stimulation: with contralateral flutter, the center of the responding region of SI underwent a large increase in absorbance, whereas absorbance decreased in the surrounding region; in contrast, during bilateral flutter, absorbance decreased (relative to that evoked by contralateral flutter) in the central region of SI but increased in the surround. The results raise the possibility that somatosensory perceptual experiences specific to bimanual tactile object exploration derive, at least in part, from the unique spatiointensive activity pattern evoked in SI when the stimulus makes contact with both hands. It is suggested that modulatory influences evoked by ipsilateral thenar flutter stimulation reach SI via a two-stage pathway involving interhemispheric (callosal) connections between information processing levels higher than SI and subsequently via intrahemispheric (corticocortical) projections to the SI hand region.

Congruency of body-related information induces somatosensory reorganization

“…the secondary somatosensory cortex (Frot and Mauguière, 1999;Hari et al, 1984) -has been suggested to receive and integrate information from both sides of the body (Desmedt and Robertson, 1977;Eickhoff et al, 2010) via transcallosal connections between homologous SII regions that allow inputs from a stimulated body part to reach the ipsilateral SII area (Schnitzler et al, 1995;Tamè et al, 2015b;Tommerdahl et al, 2006). Additionally, the P100 component has been shown to be the first SEP component integrating contralateral and ipsilateral tactile processing .…”

“…The two suggested alternative explanations are not mutually exclusive and we could speculate that reorganization of somatosensory areas can result by a combination of bottom-up and top-down projections. However, it is worth noticing that, despite bilateral integration of tactile information being generally accepted for structures beyond SI -in particular SII (Eickhoff et al, 2010) -growing evidence has demonstrated contribution of SI in the integration of somatosensory inputs from the 25 two sides of the body (Tamè et al, 2012(Tamè et al, , 2011Tommerdahl et al, 2006).…”

The Hand and the Ipsilateral Primary Somatosensory Cortex: Figure 1.

“…However, the hypothesis that SI cortex also receives input from the ipsilateral hand dates back several decades (Tamura, 1972). The responsiveness of ipsilateral SI to distal upper-limb stimulation is supported by converging evidence from multiple lines of research, including the following: (1) cortical ablation studies in rats; (2) single-neuron electrophysiology and functional magnetic resonance imaging (fMRI) with nonhuman primates; and (3) intracranial recording, magnetoencephalographic (MEG), transcranial magnetic stimulation, and fMRI studies with humans, as well as behavioral results from bimanual tasks (for most recent discussion, see Tommerdahl et al, 2006). Despite this evidence, general acceptance has not been achieved, potentially because of the incomplete characterization of ipsilateral input within SI cortex.…”

“…Three possibilities have been considered: (1) transcallosal input from contralateral SI (Allison et al, 1989); (2) direct uncrossed afferent projections to ipsilateral SI (Kanno et al, 2003); and (3) top-down input from higher-level processing areas such as SII (Tommerdahl et al, 2006). Hlushchuk and Hari (2006) suggest that the observed ipsilateral responses result from transcallosal input.…”

“…Primates' high capacity for sophisticated bimanual tasks indicates that fusion of information from the hands occurs within the CNS and possibly underlies essential behaviors (Tommerdahl et al, 2006). Psychophysical studies have demonstrated that finger stimulation to one hand can alter perception at the opposite hand (Harris et al, 2001;Braun et al, 2005).…”