Elsevier

NeuroImage

Volume 53, Issue 1, 15 October 2010, Pages 181-188
NeuroImage

Effects of somatosensory stimulation and attention on human somatosensory cortex: An fMRI study

https://doi.org/10.1016/j.neuroimage.2010.06.023Get rights and content

Abstract

It is well known that primary and non-primary areas of human somatosensory cortex are involved in the processing of adequate deviant/rare stimuli and omission of frequent stimuli. However, the relative weight and interaction of these variables is poorly known. This functional magnetic resonance imaging (fMRI) study tested the hypothesis that somatosensory stimulus processing and attention especially interact in non-primary somatosensory areas including secondary somatosensory cortex (SII) and insula. To test this hypothesis, responses of somatosensory cortex were mapped during four conditions of an oddball paradigm: DELIVERED COUNT and IGNORE (count or ignore deviant/rare electrical stimuli, respectively); OMITTED COUNT and IGNORE (count or ignore the rare omission of frequent electrical stimuli, respectively). The deviant/rare and frequent electrical stimuli were delivered to median and ulnar nerve, respectively. It was observed that contralateral (left) primary somatosensory responses were not markedly modulated by the mentioned deviant/rare events. Furthermore, contralateral SII and insula responded to all but not OMITTED IGNORE (purely attentive) condition, whereas ipsilateral (right) SII responded to all conditions. Finally, ipsilateral insula responded to the COUNT (attentive) conditions, regardless of the physical presence of the deviant/rare stimuli. The results suggest that in somatosensory modality, bilateral SII and left (contralateral) insula reflect complex integrative processes of stimulus elaboration and attention, whereas right (ipsilateral) insula mainly sub-serves active attention to deviance within a sequence of somatosensory stimuli.

Research highlights

►Contralateral SI responses were not modulated by the deviant/rare events. ►Contralateral SII and insula responses were modulated by both deviant/rare somatosensory stimuli and omission of frequent somatosensory stimuli. ►Ipsilateral insula response was modulated by attention to deviant/rare events, regardless of the absence (omission) of the somatosensory stimuli.

Introduction

Electroencephalography (EEG) and its magnetic counterpart (magnetoencephalography, MEG) have been repeatedly used to explore the fine temporal evolution of the responses of cortical somatosensory cortex under attentive conditions. In one typical condition, attention is modulated by either silently counting (active attention) or ignoring (passive attention) somatosensory stimuli. In another typical condition (oddball paradigm), subject feels rare (deviant) and frequent somatosensory stimuli; it is presumed that rare stimuli trigger pre-attentional processes when the subject is asked to ignore these stimuli, whereas they trigger attentional processes when the subject has to respond to the rare stimuli with motor acts or silent counting.

Previous EEG studies have shown that P100 and N140 components of somatosensory evoked potentials (P = positivity, N = negativity, peak latency in milliseconds) increased in amplitude during active attention (typically counting stimuli), thus reflecting selective attention-related enhancement of information processing in somatosensory and associative cortices (Desmedt and Robertson, 1977, Desmedt and Tomberg, 1989, Michie et al., 1987, García-Larrea et al., 1995, Kekoni et al., 1996, Eimer and Driver, 2000, Eimer et al., 2001, Eimer et al., 2002, Eimer and Forster, 2003, Valeriani et al., 2003, Kida et al., 2003, Kida et al., 2004, Tamura et al., 2004). Amplitude of P100 and N140 was also observed to increase for isolated somatosensory stimuli when compared to the same stimuli inserted among frequent stimuli (Kida et al., 2006), thus unveiling attentional effects related to the passive shifts of attention to sensory stimuli presented suddenly against a silent background (i.e. low level of interference).

The use of MEG techniques has contributed to a better spatial localization of the above electrophysiological phenomena. It has been shown that the contralateral primary somatosensory (SI), the bilateral secondary somatosensory (SII), the posterior parietal, and the frontal mesial areas responded to somatosensory stimuli (20–150 ms post-stimulus) in both passive (ignore) and active (count) attentional conditions (Forss et al., 1996). In this framework, frontal mesial response appeared to be especially sensitive to active attention (Forss et al., 1996). It has also been shown that contralateral SI (20–70 ms post-stimulus) and bilateral SII (120–140 ms post-stimulus) responses were greater during both passive (ignore) and active (count) attention to rare stimuli when compared to frequent somatosensory stimuli (Mima et al., 1998). However, SII but not SI responses to rare stimuli were higher in active than passive conditions (Mima et al., 1998). Furthermore, previous MEG evidence has pointed to a strong response (about 80 ms post-stimulus) of SII during active attention (count) for rare somatosensory stimuli, while ignoring frequent electrical stimuli or stimuli of another modality (Fujiwara et al., 2002). Moreover, a modality specific activation of contralateral SI and bilateral SII related to active attention, has been reported, in line with previous findings (Huang et al., 2005, Forss et al., 1996, Mima et al., 1998, Fujiwara et al., 2002).

Fine topographical details of the above responses have been studied by positron emission tomography (PET) and functional magnetic resonance imaging (fMRI). Some studies have reported that attention to somatosensory stimuli modulates SI (Meyer et al., 1991, Arthurs et al., 2004, Drevets et al., 1995, Macaluso et al., 2000, Sterr et al., 2007), whereas other evidence failed to find a significant modulation of SI activation between attended and unattended conditions (Backes et al., 2000). Further PET and fMRI studies have found either similar attention-related activation in both SI and SII (Johansen-Berg et al., 2000, Nelson et al., 2004) or stronger activation changes in SII than SI (Backes et al., 2000, Hämäläinen et al., 2000, Burton et al., 1999).

Keeping in mind the above data, it can be speculated that SI is mainly involved in the passive neural representation of haptic information, whereas SII sub-serves higher order processing of such representation related to attention and learning (Hari and Forss, 1999, Javitt et al., 1994, Näätänen et al., 1978, Näätänen et al., 1993, Winkler et al., 1993). However, the relative weight of adequate stimulus processing and attention in primary and non-primary somatosensory areas is poorly known, especially in the case of unattended stimulus omission. It has been shown that in active time-estimation paradigm, omitted somatosensory stimuli elicited central-parietal late positive event-related potentials similar to those observed in oddball paradigms using deviant somatosensory stimuli (Ito et al., 1997). Furthermore, MEG evidence has unveiled responses of contralateral SI (about 35–80 ms post-stimulus) and bilateral SII (60–100 ms post-stimulus) for the omission of somatosensory stimuli under a condition of passive attention (Karhu and Tesche, 1999). Unfortunately, no PET or fMRI finding enlightened spatial details on the involvement of the somatosensory cortex in the neural representation of omitted somatosensory stimuli.

The present fMRI study tested the hypothesis that stimulus processing and attention especially affect and interact in non-primary somatosensory areas. To test this hypothesis, responses of primary and non-primary somatosensory cortex were mapped in conditions systematically probing the processing of deviant/rare somatosensory stimuli and omission of frequent stimuli during active and passive attentive conditions.

Section snippets

Subjects and stimulation procedure

Thirteen healthy volunteers ranging in age from 19 to 26 years (5 males, 8 females) were enrolled in this study. All subjects were right handed according to the Edinburgh Inventory (Oldfield, 1971) and gave their written informed consent according to the Declaration of Helsinki (World Medical Association Declaration of Helsinki, 1997) and could request an interruption of the investigation at any time. The general procedures were approved by the local Institutional Ethics Committee.

The

Results

Behavioural data showed a consistent task performance across subjects during both COUNT conditions: 39.5 ± 2.2 (Mean ± SD) deviant events were counted during DELIVERED COUNT and 36.7 ± 3.9 deviant events were counted during OMITTED COUNT. Although a slightly superior performance was observed for DELIVERED COUNT with respect to OMITTED COUNT, a t-test did not reveal a statistically significant difference between the two conditions.

The fMRI group analysis showed a statistically significant (p < 0.05,

Discussion

In this fMRI study, responses of primary and non-primary somatosensory cortex were mapped in conditions systematically probing the processing of deviant/rare somatosensory stimuli and omission of frequent stimuli during active and passive attentive conditions. Main results showed that contralateral (left) SI responses were modulated neither in the DELIVERED COUNT and IGNORE conditions (count or ignore deviant/rare electrical stimuli, respectively) nor in the OMITTED COUNT and IGNORE conditions

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    The first two authors contributed equally to the present study.

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