Single Neurons in the Insular Cortex of a Macaque Monkey Respond to Skin Brushing: Preliminary Data of the Possible Representation of Pleasant Touch.

Laura Clara Grandi,Marzio Gerbella

doi:10.3389/fnbeh.2016.00090

Abstract

Pleasant touch may serve as a foundation for affiliative behavior, providing a mechanism for the formation and maintenance of social bonds among conspecifics. In humans, this touch is usually referred to as the caress. Dynamic caressing performed on the hairy skin with a velocity of 1–10 cm/s is perceived as being pleasant and determines positive cardio-physiological effects. Furthermore, imaging human studies show that affiliative touch activates the posterior insular cortex (pIC). Recently, it was demonstrated that pleasant touch in monkeys (i.e., sweeping in a grooming-like manner) is performed with velocities similar to those characteristics of human caress (9.31 cm/s), and causes similarly positive autonomic effects, if performed with velocity of 5 cm/s and 10 cm/s, but not lower or higher. Due to similarities between the human caress and non-human primate sweeping, we investigated for the first time whether single neurons of the perisylvian regions (secondary somatosensory cortex [SII] and pIC) of a rhesus monkey can process sweeping touch differently depending on the stimulus speed. We applied stimulation with two speeds: one that optimally induces positive cardio-physiological effects in the monkey who receives it, and includes the real speed of sweep (5–15 cm/s, sweep fast), and a non-optimal speed (1–5 cm/s, sweep slow). The results show that single neurons of insular cortex differently encode the stimulus speed. In particular, even the majority of recorded somatosensory neurons (82.96%) did not discriminate the two speeds, a small set of neurons (16.59%) were modulated just during the sweep fast. These findings represent the first evidence that single neurons of the non-human primates insular cortex can code affiliative touch, highlighting the similarity between human and non-human primates’ social touch systems. This study constitutes an important starting point to carry out deeper investigation on neuronal processing of pleasant sweeping in the central nervous system.

Highlights

The sense of touch is a critical and necessary sense for our experience of the world in daily life, to haptically explore objects and to communicate both negative and positive messages during social interactions (Hertenstein et al, 2006a,b)
Because the posterior insular cortex (pIC) appears to have a key role for coding the affiliative interpersonal touch in humans (Olausson et al, 2002, 2008a,b, 2010), and for triggering social behavior in non-human primates (Kling and Steklis, 1976; Ishida et al, 2014; Jezzini et al, 2015), here we investigated the modulation of single neurons in the pIC and in the adjacent SII region of a macaque monkey during the above cited dynamic tactile stimulation considered pleasant for non-human primates: sweeping
Due to the key role of the pIC in the coding of affiliative interpersonal touch in humans (Olausson et al, 2002, 2008a,b, 2010), and its hypothetical involvement in social behavior in non-human primates (Kling and Steklis, 1976; Ishida et al, 2014; Jezzini et al, 2015), here we investigated for the first time the activity of single neurons of the dysgranular and granular parts of this region of the macaque monkey during a dynamic tactile stimulation, considered pleasant for non-human primates, that is, sweeping

Summary

Introduction

The sense of touch is a critical and necessary sense for our experience of the world in daily life, to haptically explore objects and to communicate both negative and positive messages during social interactions (Hertenstein et al, 2006a,b). Information conveyed by C-fibers are relayed, at higher levels, by the ventromedial posterior thalamic nucleus to the dorsal posterior insular cortex (pIC; Olausson et al, 2002, 2008a,b, 2010; Björnsdotter et al, 2009), to the orbitofrontal cortex (a key area for hedonic processing), to the postero-superior temporal sulcus (STS), the medial prefrontal cortex, the dorso-anterior cingulate cortex, and the pregenual anterior cingulate cortex (Kringelbach and Rolls, 2004; McGlone et al, 2007, 2012; Gordon et al, 2013; Ellingsen et al, 2014) These anatomical data are consistent with the idea that these fibers belong to the interoceptive system, and play a pivotal role in the encoding of the pleasantness and emotional component of interpersonal touch. Noteworthy that to what extent these areas process pleasant touch it remains largely unexplored, the insular cortex, primarily the posterior part, appears to have an especially important role (Olausson et al, 2002, 2010; Björnsdotter et al, 2009)

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Conclusion