Seeking pleasant touch: neural correlates of behavioral preferences for skin stroking

Abstract

Affective touch is a dynamic process. In this fMRI study we investigated affective touch by exploring its effects on overt behavior. Arm and palm skin were stroked with a soft brush at five different velocities (0.3, 1, 10, 3, and 30 cm s(-1)), using a novel feedback-based paradigm. Following stimulation in each trial, participants actively chose whether the caress they would receive in the next trial would be the same speed ("repeat") or different ("change"). Since preferred stroking speeds should be sought with greater frequency than non-preferred speeds, this paradigm provided a measure of such preferences in the form of active choices. The stimulation velocities were implemented with respect to the differential subjective pleasantness ratings they elicit in healthy subjects, with intermediate velocities (1, 10, and 3 cm s(-1)) considered more pleasant than very slow or very fast ones. Such pleasantness ratings linearly correlate with changes in mean firing rates of unmyelinated low-threshold C-tactile (CT) afferent nerves in the skin. Here, gentle, dynamic stimulation optimal for activating CT-afferents not only affected behavioral choices, but engaged brain regions involved in reward-related behavior and decision-making. This was the case for both hairy skin of the arm, where CTs are abundant, and glabrous skin of the palm, where CTs are absent. These findings provide insights on central and behavioral mechanisms underlying the perception of affective touch, and indicate that seeking affective touch involves value-based neural processing that is ultimately reflected in behavioral preferences.

Keywords: CT afferents; affective touch; fMRI; interoception; seeking behavior.

Figure 1

Design. Each trial began with a 2 s inter-trial interval during which subjects fixated their gaze on a dot presented centrally on the screen. There followed a 2–16 s stimulation interval, depending on the velocity delivered. Participants received single brush strokes on the arm at different velocities. Stimulation consisted of single brush strokes delivered manually on 5 cm of the arm or the palm. A 1 s interval occurred between stimulation and the onset of the response cue. The response cue consisted of the sentence “Repeat or change?” remaining on the screen for 3 s as the subjects pressed the button indicating their choice.

Figure 2

(A) The two graphs represent the percentage of the ratio of repeats on overall choices for arm (black) and palm (gray). For the arm, ratio values exceeded chance (45%) for 1, 3, and 10 cm s⁻¹ whereas for the palm, the repeat percentages exceeding chance was only for 3 cm s⁻¹. Both curves were significantly best described by a negative quadratic term. (B) Activation maps for GLM3: Preference ratio, reflecting differential weighting across velocities. To represent the behavioral ratio the following contrast was used: [(1 cm s⁻¹ + 3 cm s⁻¹ + 10 cm s⁻¹) > (0.3 cm s⁻¹ + 30 cm s⁻¹)] for the arm trials vs. [(3 cm s⁻¹) > (0.3 cm s⁻¹ + 1 cm s⁻¹ + 10 cm s⁻¹ + 30 cm s⁻¹)] for the palm. This contrast reveals clusters with higher responses for 1, 3, and 10 compared to 0.3 and 30 s⁻¹ in the arm conditions; and 3 compared to 0.3, 1, 10 and 30 s⁻¹ in the palm conditions. Both arm and palm runs were included in the general linear model. Results revealed activation in right dlPFC (35, 39, 6) and right posterior insula (29, −26, 9). All contrasts thresholded at a whole-brain uncorrected level of p < 0.005. Talairach coordinates, radiological convention (left is right).

Figure 3

(A) Activation maps for GLM1: Stimulation. Brush stroking stimulation revealed activations in somatosensory areas. Right primary somatosensory cortex (29, −38, 54) and secondary somatosensory cortex/posterior insula (38, −14, 12) for stimulation on both arm and palm are shown. (B) Activation maps for GLM2: Evaluation Stimulation (Table 2). This interval reflects the 1 s following the stimulation before choice. Bilateral anterior insula (44, 19, −3 and −43, 19, −3) and primary visual cortex (11, −80, 6) are shown. (C) The repeat vs. change contrast, revealed activation in the right caudate (14, 13, 15). Random effect contrasts were performed at a corrected threshold of p < 0.001. Talairach coordinates, radiological convention (left is right).

Figure 4

(A) Activation maps for GLM1: Stimulation Differences between hedonic stroking vs. fixation for arm (red) and palm (green) during stimulation interval. (B) Activation maps for GLM2: Evaluation. Differences between hedonic stroking vs. fixation for arm (red) and palm (green) during the evaluation interval. (C) Activation maps for GLM3: Preference ration. Differences between arm and palm for the GLM3 revealed activation in right dlPFC (35, 40, 3). Random effect contrasts were performed at a corrected threshold of p < 0.001. Talairach coordinates, radiological convention (left is right).