Early integration of bilateral touch in the primary somatosensory cortex

Abstract

Animal, as well as behavioural and neuroimaging studies in humans have documented integration of bilateral tactile information at the level of primary somatosensory cortex (SI). However, it is still debated whether integration in SI occurs early or late during tactile processing, and whether it is somatotopically organized. To address both the spatial and temporal aspects of bilateral tactile processing we used magnetoencephalography in a tactile repetition-suppression paradigm. We examined somatosensory evoked-responses produced by probe stimuli preceded by an adaptor, as a function of the relative position of adaptor and probe (probe always at the left index finger; adaptor at the index or middle finger of the left or right hand) and as a function of the delay between adaptor and probe (0, 25, or 125 ms). Percentage of response-amplitude suppression was computed by comparing paired (adaptor + probe) with single stimulations of adaptor and probe. Results show that response suppression varies differentially in SI and SII as a function of both spatial and temporal features of the stimuli. Remarkably, repetition suppression of SI activity emerged early in time, regardless of whether the adaptor stimulus was presented on the same and the opposite body side with respect to the probe. These novel findings support the notion of an early and somatotopically organized inter-hemispheric integration of tactile information in SI.

Keywords: MEG; SI; bilateral integration; touch at the fingers.

Figure 1

Graphical representation of the possible anatomical pathways mediating the integration processing of tactile information from the two sides of the body. In the example the tactile stimulated finger is the right index. Grey circles represent the passage of information through that particular node. (A) Direct ipsilateral projections, (B) transcallosal projections and (C) SII mediated projections.

Figure 2

Scheme of stimulation sequences. Pairs of short tactile stimuli (12 ms) were presented at different ISIs (A) simultaneously (B) with an ISI of 25 ms or (C) with an ISI of 125 ms. The start of the stimulation phase was indicated by a green fixation cross in the middle of the screen 500 ms before the adaptor stimulus.

Figure 3

Schematic representation of paired (A) and single (B) stimulation conditions. The empty circle represents the test stimulus, while the colored circles represent the adaptor stimuli. (a) Stimulation condition in which the left index was stimulated twice (Li+Li; within hand stimulation); (b) Stimulation condition in which the left index and middle fingers were stimulated (Lm+Li; within hand stimulation); (c) Stimulation condition in which the two index fingers were stimulated (Ri+Li; between hand stimulation); (d) Stimulation condition in which the right middle and left index fingers were stimulated (Rm+Li; between hand stimulation); (e) Stimulation condition in which the left middle finger was stimulated alone; (f) Stimulation condition in which the right middle finger was stimulated alone; (g) Stimulation condition in which the left index finger was stimulated alone; (h) Stimulation condition in which the right index finger was stimulated alone.

Figure 4

Schematic representation of the ECD approach used to define the four ROIs in the contra‐ and ipsi‐lateral S1 and S2. (a) SEFs for the single finger stimulation (150 trials) of the left (left panel) and right (right panel) index and middle fingers respectively. Red and green arrows indicate the latencies at which the ECDs were estimated. (b) The corresponding ECDs located at SI and SII for the left (left panel) and right (right panel) stimulation sides fitted at the peak of the first and second SEF components. MRI slides are in neurological orientation. (c) The correspondence of the two ECDs with the underlying cytoachitectonic maps (Eickoff et al., 2006). Red and green ECDs are overlaid on BA3b and OP1 maps respectively. (d) 3D representation of the four ECDs locations with respect to the participant's anatomical scan.

Figure 5

SEFs for the unilateral (left panels) and bilateral (right panels) stimulation of the single and double short (30 ms) and long (125 ms) fingers stimulation. The corresponding topographic maps of the SEFs in the SI are also shown aside. Green and black arrows indicate the latencies at which the maps were depicted.

Figure 6

Percentage of response suppression of the dipole activity in the cSI when the test stimulus was preceded by an adapting stimulation on the homologous (Li‐Li, red bars) and non‐homologous (Lm‐Li, green bars) finger of the same hand and on the homologous (Ri‐Li, black bars) and non‐homologous (Rm‐Li, yellow bars) finger of the opposite hand simultaneously (Sim), with a short interval of 25 ms (Short) and with a long interval of 125 ms (Long). Error bars represent the standard errors of the mean (±SEM).

Figure 7

Percentage of response suppression of the dipole activity in the cSII and iSII when the test stimulus was preceded by an adapting stimulation on the homologous (Li‐Li, red bars) and non‐homologous (Lm‐Li, green bars) finger of the same hand and on the homologous (Ri‐Li, black bars) and non‐homologous (Rm‐Li, yellow bars) finger of the opposite hand simultaneously (Sim), with a short interval of 25 ms (Short) and with a long interval of 125 ms (Long). Error bars represent the standard errors of the mean (±SEM).