Multiple Somatotopic Representations of Heat and Mechanical Pain in the Operculo-Insular Cortex: A High-Resolution fMRI Study

Abstract

Whereas studies of somatotopic representation of touch have been useful to distinguish multiple somatosensory areas within primary (SI) and secondary (SII) somatosensory cortex regions, no such analysis exists for the representation of pain across nociceptive modalities. Here we investigated somatotopy in the operculo-insular cortex with noxious heat and pinprick stimuli in 11 healthy subjects using high-resolution (2 × 2 × 4 mm) 3T functional magnetic resonance imaging (fMRI). Heat stimuli (delivered using a laser) and pinprick stimuli (delivered using a punctate probe) were directed to the dorsum of the right hand and foot in a balanced design. Locations of the peak fMRI responses were compared between stimulation sites (hand vs. foot) and modalities (heat vs. pinprick) within four bilateral regions of interest: anterior and posterior insula and frontal and parietal operculum. Importantly, all analyses were performed on individual, non-normalized fMRI images. For heat stimuli, we found hand-foot somatotopy in the contralateral anterior and posterior insula [hand, 9 ± 10 (SD) mm anterior to foot, P < 0.05] and in the contralateral parietal operculum (SII; hand, 7 ± 10 mm lateral to foot, P < 0.05). For pinprick stimuli, we also found somatotopy in the contralateral posterior insula (hand, 9 ± 10 mm anterior to foot, P < 0.05). Furthermore, the response to heat stimulation of the hand was 11 ± 12 mm anterior to the response to pinprick stimulation of the hand in the contralateral (left) anterior insula (P < 0.05). These results indicate the existence of multiple somatotopic representations for pain within the operculo-insular region in humans, possibly reflecting its importance as a sensory-integration site that directs emotional responses and behavior appropriately depending on the body site being injured.

Extended cortical activations during evaluating successive pain stimuli

“…The 'pain matrix' is also activated by non-painful stimuli (Mouraux and Iannetti, 2009). Using the same type of stimuli, we recently showed that the operculo-insular cortex, especially SII and the posterior insular cortex, are more pain specific (Oertel et al, 2011), which agrees with results using other noxious stimuli or assessments in patients suffering particular central pain syndromes (Peyron et al, 2002;Baumgartner et al, 2010;Garcia-Larrea et al, 2010). The present findings further support observations that pain stimuli are associated with complex and not only pain specific activations in the brain.…”

Differences in cortical coding of heat evoked pain beyond the perceived intensity: An fMRI and EEG study

“…Our analysis of S2 included OP 1-4 as a single region of interest and demonstrated no distinct organization of nociceptive stimuli into hand and trunk areas, with the average most activated voxels independent of stimulation site within OP 4 (ipsilateral and contralateral). However, Baumgärtner et al [2010] provided evidence of somatotopy within OP 1 in response to nociceptive stimuli of the hand and foot. Therefore, we cannot exclude that there may be multiple somatotopic representations within the other single opercula (OP 1, 2, and 3).…”

“…Brain imaging studies have disclosed a network of cortical areas involved in nociceptive processing [Apkarian et al, 2005;Peyron et al, 2000], as well as demonstrated somatotopic organization of nociception in a number of these areas (e.g., primary and secondary somatosensory cortices, S1 and S2, respectively) [Baumgärtner et al, 2010;Bingel et al, 2004;Brooks et al, 2005;DaSilva et al, 2002;Xu et al, 1997].…”

Social rejection shares somatosensory representations with physical pain

“…Prior research has identified two regions in the operculoinsular region that are specifically involved in pain-related somatosensory processing: OP1, the most caudal area of the parietal operculum, and dpINS (19)(20)(21)(22)(23). To identify whether social rejection and physical pain coactivated these areas, we performed a priori ROI analyses on these regions (see Methods for details regarding ROI definition).…”