Somatotopic Organization of Gentle Touch Processing in the Posterior Insular Cortex

Abstract

A network of thin (C and A␦) afferents relays various signals related to the physiological condition of the body, including sensations of gentle touch, pain, and temperature changes. Such afferents project to the insular cortex, where a somatotopic organization of responses to noxious and cooling stimuli was recently observed. To explore the possibility of a corresponding body-map topography in relation to gentle touch mediated through C tactile (CT) fibers, we applied soft brush stimuli to the right forearm and thigh of a patient (GL) lacking A␤ afferents, and six healthy subjects during functional magnetic resonance imaging (fMRI). For improved fMRI analysis, we used a highly sensitive multivariate voxel clustering approach. A somatotopic organization of the left (contralateral) posterior insular cortex was consistently demonstrated in all subjects, including GL, with forearm projecting anterior to thigh stimulation. Also, despite denying any sense of touch in daily life, GL correctly localized 97% of the stimuli to the forearm or thigh in a forced-choice paradigm. The consistency in activation patterns across GL and the healthy subjects suggests that the identified organization reflects the central projection of CT fibers. Moreover, substantial similarities of the presently observed insular activation with that described for noxious and cooling stimuli solidify the hypothesized sensory-affective role of the CT system in the maintenance of physical well-being as part of a thin-afferent homeostatic network.

Vicarious Responses to Social Touch in Posterior Insular Cortex Are Tuned to Pleasant Caressing Speeds

“…Since this pathway is similar to that of visceral afferents, CT afferents have more in common with interoceptive systems conveying information about body state regulation than with classical exteroceptive systems conveying discriminative aspects of touch (Björnsdotter et al, 2010). The CT afferent pathway projection to insular cortex in humans is supported by neuroimaging studies of both patients and healthy controls, demonstrating that brushing stimulation likely to elicit CT discharge results in activation of contralateral mid-and posterior insular cortex (Olausson et al, 2002(Olausson et al, , 2008aBjörnsdotter et al, 2009Björnsdotter et al, , 2010. In the present study, the felt and seen velocity-specific activations in experiments 1 and 2 fell in granular insular cortex (Ig2 of Kurth et al, 2010b) on or near the long gyri and within the insular central sulcus, sometimes extending onto the posterior short gyrus.…”

“…CT units showed a unique preference for speeds of 1-10 cm/s, with the biggest difference between 3 and 30 cm/s, the velocities used in the present study. The CT pathway associated with dynamic, affective touch differs anatomically and functionally from that of myelinated A␤ afferents associated with rapid sensory-discriminative tactile processing (Essick et al, 1999(Essick et al, , 2010Olausson et al, 2002Olausson et al, , 2008aOlausson et al, ,b, 2010McGlone et al, 2007;Guest et al, 2009;Löken et al, 2009;Björnsdotter et al, 2009; McGlone and Spence, 2010; Morrison et al, 2010Morrison et al, , 2011. CT receptors are found in hairy but not in glabrous (smooth, e.g., palm) skin (Johansson and Vallbo, 1979;Nordin, 1990;Vallbo et al, 1999; Figure 2.…”

“…This region is activated by a broad range of visceral and somatosensory stimulation in humans (Kurth et al, 2010a), including human touch (Lovero et al, 2009), and is highly functionally connected with sensorimotor cortices (Deen et al, 2010;Cauda et al, 2011). It also exhibits distinct somatotopic responses for stroking on the arm and thigh within the range of CT afferents' preferred speed (Björnsdotter et al, 2009(Björnsdotter et al, , 2010. Functional and spatial specialization between visceral (interoceptive) and somatic stimulation is low in the insula (Eickhoff et al, 2006), the weak separation implying that this region plays an integrative role among somatosensory and interoceptive inputs.…”

“…This velocity-sensitive CT response is tightly correlated with subjective ratings of how pleasant the touch feels . Human CT pathways ultimately target the insular cortex (Olausson et al, 2002(Olausson et al, , 2008aBjörnsdotter et al, 2009Björnsdotter et al, , 2010, a region associated with emotion and homeostatic balance (Craig, 2002(Craig, , 2008(Craig, , 2009Paulus, 2007).…”

Differential Involvement of Somatosensory and Interoceptive Cortices during the Observation of Affective Touch

“…Importantly, two distinct neural systems can be identified regarding the processing of cutaneous information. An exteroceptive modality in the somatosensory cortices is mainly involved in the discrimination of the physical characteristics of tactile stimuli, whereas an interoceptive modality in posterior insular cortex is believed to process the internal affective feeling states evoked by experienced touch (Björnsdotter, Löken, Olausson, Vallbo, & Wessberg, 2009;Craig, 2002;Olausson et al, 2002;Servos, Lederman, Wilson, & Gati, 2001;Schnitzler & Ploner, 2000). A modulation of the activation of somatosensory cortices by the observation of othersʼ affective tactile experiences is found, in particular, by studies that required explicit processing of the sensory-discriminative aspects of the visual stimuli, mostly depicting intense or painful tactile stimulation, or measured sensory-evoked potentials (e.g., Bufalari, Aprili, Avenanti, Di Russo, & Aglioti, 2007;Cheng et al, 2007;Lamm, Nusbaum, Meltzoff, & Decety, 2007), whereas no studies reported evidence for involvement of posterior insular cortices.…”