The Neurobiology Shaping Affective Touch: Expectation, Motivation, and Meaning in the Multisensory Context

Abstract

Inter-individual touch can be a desirable reward that can both relieve negative affect and evoke strong feelings of pleasure. However, if other sensory cues indicate it is undesirable to interact with the toucher, the affective experience of the same touch may be flipped to disgust. While a broad literature has addressed, on one hand the neurophysiological basis of ascending touch pathways, and on the other hand the central neurochemistry involved in touch behaviors, investigations of how external context and internal state shapes the hedonic value of touch have only recently emerged. Here, we review the psychological and neurobiological mechanisms responsible for the integration of tactile "bottom-up" stimuli and "top-down" information into affective touch experiences. We highlight the reciprocal influences between gentle touch and contextual information, and consider how, and at which levels of neural processing, top-down influences may modulate ascending touch signals. Finally, we discuss the central neurochemistry, specifically the μ-opioids and oxytocin systems, involved in affective touch processing, and how the functions of these neurotransmitters largely depend on the context and motivational state of the individual.

Keywords: hedonics; opioids; oxytocin; placebo effect; social processing; top–down modulation; touch.

FIGURE 1

Contextual modulation of touch pleasantness during identical tactile stimuli. (A) Touch pleasantness of both gentle stroking (human) touch and equally intense vibratory (machine) touch is highest during concomitant presentation of smiling faces and lowest during presentation of frowning faces (Ellingsen et al., 2014). (B) In a similar fashion, touch pleasantness is highest during concomitant presentation of pleasant (rose) odors and lowest during presentation of disgusting (civette) odors (Croy et al., 2014). (C) People find the gently rubbing of a skin cream more pleasant when being told it is a “rich moisturizing cream” (rubrich) relative to a “basic cream” (rubthin) (McCabe et al., 2008). (D) While one study found no effect of intranasal oxytocin on touch pleasantness (Ellingsen et al., 2014), another study (E) found that oxytocin increased touch pleasantness in heterosexual men when they believed they were being sensually caressed by a woman, but not when they believed the caresser was a man (Scheele et al., 2014). (E–F) Caresses are more pleasant when the caresser is believed to be a woman relative to a man (Gazzola et al., 2012; Scheele et al., 2014). Figure adapted from (McCabe et al., 2008; Gazzola et al., 2012; Ellingsen et al., 2014; Croy et al., 2014; Scheele et al., 2014). ^∗∗p < 0.01.

FIGURE 2

Contextual modulation of brain to affective touch. (A) After self-administrating a (placebo) nasal spray believed to have beneficial effects on gentle touch and pain perception, placebo-induced increases in touch pleasantness and reductions in pain unpleasantness were underpinned by respective increases and decreases in somatosensory processing of pleasant touch and pain (top). The individual magnitude of this somatosensory modulation was associated with the degree to which placebo treatment increased the functional connectivity between the medial OFC (mOFC) and PAG (bottom, left), an important pathway for pain modulation – those with the strongest increase in mOFC-PAG connectivity had the strongest somatosensory increases to pleasant touch (bottom, middle) and the strongest somatosensory decreases to pain stimuli (bottom, right) (Ellingsen et al., 2013). (B) In heterosexual men, SI activity during gentle caresses was larger when they believed a woman, relative to a man, performed the caress. The same pattern was seen across different sub-regions of SI, as well as (non-significantly) in the ACC and insula (bottom) (Gazzola et al., 2012). Figure adapted from (Gazzola et al., 2012; Ellingsen et al., 2013). ^∗p < 0.05, ^∗∗p < 0.01.