Physiological and Behavioral Responses Reveal 9-Month-Old Infants’ Sensitivity to Pleasant Touch

Method

Procedure

The infants were allowed to play for about 10 min before the test session so they could familiarize themselves with the experimental room. Infants were then seated in a baby seat (Bumbo Babysitter, Toronto, Ontario, Canada) held on the lap of the attending parent. The parent and child were placed in a walled-off section of the lab facing a monitor and video-recording device (LifeCam Studio Q2F-00013, Microsoft, Redmond, WA) at an approximate distance of 70 cm. A pulse oximeter (Contec Medical, CMS 60C, Qinhuangdao, Hebei Province, China) was attached to the large toe of the infants’ right foot using a specialized infant clip and medical tape. While the pulse oximeter was attached, the child started watching the silent distractor film (one of two films from the Czech cartoon series, “Krtecˇek,” or “The Little Mole,” by Zdeneˇk Miler). Because photoplethysmography (PPG) can be affected by movement, the baby seat ensured that infants’ legs were restrained to some degree; if necessary, the attending parent held the infant’s leg (Fig. 1a). After it was established that the pulse-oximeter signal was consistently recording, data collection was started, with tactile stroking stimuli beginning after 1 min of baseline heart rate data were obtained.

OPEN IN VIEWER

Fig. 1.

Experimental paradigm (a) and sample timeline (b). The illustration shows the experimental setup. The infant was seated in a Bumbo baby seat placed on the lap of the parent. Parent and infant faced a monitor, which played a distractor film. The experimenter was seated beside the infant so she could easily stroke the infant’s nondominant dorsal forearm with an artist’s paintbrush at one of three velocities (slow: 0.3 cm/s, medium: 3 cm/s, fast: 30 cm/s). A response in arousal was measured by a special infant pulse-oximeter probe placed on the large toe of the right foot. The graph shows an individual infant’s heart rate (HR) during the 10 s before stimulation and the 10 s during stimulation as a function of stroking velocity. As the sample timeline (b) shows, baseline HR was recorded before the start of trials, and then stroking stimuli (in pseudorandomized order) alternated with short rest periods throughout the trials.

Using a procedure described by Löken and colleagues (2011), the nondominant dorsal forearm was stroked by the experimenter using a Chinese hake paintbrush (5-cm width) at one of three defined velocities (0.3, 3, or 30 cm/s). The three speeds of stroking were administered with four repeats each, the order of which was pseudorandomized across infants such that there were no immediate repetitions of one velocity, and one particular velocity did not always precede another. Seated next to the parent, a female experimenter administered brush strokes over a marked-out 10-cm area on the dorsal side of the infant’s left lower forearm (i.e., on hairy skin). The experimenter stroked from epicondyle to wrist (i.e., in the proximo-distal direction), with each stimulation lasting 10 s (Fig. 1a). The experimenter had practiced the three speeds of brush strokes. The handheld manipulation has been used with success previously (Löken et al., 2011; Morrison et al., 2010) and has recently been validated in direct comparison with robotic stimulation (Triscoli, Olausson, Sailer, Ignell, & Croy, 2013).

We were able to control for the amount of force the experimenter applied to the brushstrokes because of the von Frey effect. This effect assumes that the force required to bend the nylon hairs of the brush when pressed against the skin is constant and, therefore, can be used to apply a very accurate force on specific areas of the skin. Furthermore, the brush did not induce changes in temperature (as a hand could have), and contact area was controlled across participants. The protocol was similar to one in which neural recordings were obtained, which allowed us to make more direct links to previously published results (Löken et al., 2009; Löken et al., 2011). Additionally, with our parametric manipulation, we attempted to control for context with minimal social contact; the experimenter was instructed to make minimal eye contact with the infant, and stroking was performed indirectly through a paintbrush rather than by hand or with a socially relevant object. The experimenter was prompted by a hidden screen as to the velocity of the stroking and was blind to the order of conditions.

Between each 10-s stroking stimulus, there was a 40-s rest period to prevent receptor fatigue as well as to allow for a 10-s prestimulus baseline heart rate measurement (Fig. 1b). Parents were instructed to have as little physical contact as possible with the child during testing. Moreover, parents were in no way cued to the order or content of the conditions. At the end of testing, the primary caregiver completed a German translation of the STQ. The STQ is a self-report measure that examines the individual’s approach and response to situations involving social touch. Responses to items such as “I generally seek physical contact with others” or “I feel embarrassed if I have to touch someone in order to get their attention” provided a measure of the caregiver’s sensitivity to social touch. Lower scores on this measure indicate a greater preference for social touch, whereas higher scores index a greater aversion to giving, receiving, and observing social touch. In this sample, internal consistency (Cronbach’s α) of the 20 questions was .60.

Results

On the basis of adult behavioral studies of touch (Drescher et al., 1980; Drescher et al., 1985), we hypothesized that the specificity of the response of the C-tactile fibers to medium-velocity stroking would be evident from both the physiological heart rate data and from the behavioral responses. Specifically, we expected a significant decrease in heart rate and a significant increase in behavioral engagement, as measured by longer individual gazes toward the stroking stimulus during medium-velocity stroking than during slow- or fast-velocity stroking.

As predicted, our cardiac data revealed a U-shaped relationship between brushing velocity and heart rate, as measured by percentage signal change (slow: M = 1.02, SE = 1.51; medium: M = −1.21, SE = 1.40; fast: M = 1.19, SE = 1.46; see Fig. 2a). Specifically, heart rate decelerations were observed in the medium-velocity condition, whereas slight accelerations were observed in the slow- and fast-velocity conditions. Post hoc t tests showed significant differences between the slow- and medium-velocity conditions, t(15) = 1.97, one-tailed p = .03, two-tailed p = .065, and between the medium- and fast-velocity conditions, t(15) = 2.9, p = 0.01. No significant difference was seen between the slow- and fast-velocity conditions (p = .89).

OPEN IN VIEWER

Fig. 2.

Results. Mean percentage heart rate (HR) change (a) is shown as a function of stroking velocity. Attentional engagement (b) is shown as a function of stroking velocity, separately for engagement with the paintbrush (left) and with the experimenter (right). Engagement was calculated as the duration of gazes divided by the number of gaze shifts. In (a) and (b), error bars represent standard errors, and an asterisk indicates a significant difference relative to the other two conditions (p < .05). The scatter plot (c; with best-fitting regression line) shows the correlation between mean percentage HR change for each infant in the medium-velocity condition and his or her parent’s score on the Social Touch Questionnaire (Wilhelm, Kochar, Roth, & Gross, 2001). Lower scores indicate greater preference for social touch.

We next examined the number of gaze shifts between the distractor film and the stimulation and the duration of looks made to either the paintbrush or the experimenter during the 10 s of brushing. Separately, these factors showed little or no effect of the manipulation. The number of gaze shifts toward the experimenter (slow: M = 1.16, SE = 0.13; medium: M = 1.42, SE = 0.25; fast: M = 1.52, SE = 0.21) and toward the paintbrush (slow: M = 1.35, SE = 0.12; medium: M = 1.61, SE = 0.15; fast: M = 1.78, SE = 0.24) were similar across velocity conditions, as were the duration of looks toward the experimenter (slow: M = 1.73 s, SE = 0.23; medium: M = 2.33 s, SE = 0.39; fast: M = 2.58 s, SE = 0.40) and toward the paintbrush (slow: M = 3.03 s, SE = 0.30; medium: M = 3.69 s, SE = 0.45; fast: M = 3.51 s, SE = 0.54).

Durations and frequencies for each velocity condition were then used to create a single “engagement” parameter assessing both the attentional switch and sustained attention, separately toward the paintbrush and toward the experimenter. Across conditions, a one-way repeated measures ANOVA showed a significant effect of brushing velocity, F(2, 48) = 3.28, p = .04, with significantly longer attention (engagement) toward the paintbrush during the medium- relative to the fast-velocity, t(15) = 3.66, p = .0021, and slow-velocity condition, t(15) = 3.84, p = .0014 (slow: M = 2.40, SE = 0.30; medium: M = 3.09, SE = 0.31; fast: M = 2.01, SE = 0.29; see Fig. 2b). Despite a similar trend, no significant main effect was seen in the measure of engagement with the experimenter (slow: M = 1.70, SE = 0.15; medium: M = 2.39, SE = 0.37; fast: M = 1.93, SE = 0.22).

Next, we compared infants’ physiological responses with their parent’s responses on the STQ. As shown in Figure 2c, our analysis revealed a significant positive correlation between the infant’s response in heart rate (deceleration) and the parent’s STQ score (r = .56, p = .02), but only in the medium-velocity condition. This correlation was not significant in the slow- (r = .20, p = .42) and fast-velocity (r = .14, p = .58) conditions. This finding indicates that the greater the caregiver’s sensitivity to social touch, the greater the infant’s heart rate deceleration in response to medium-velocity touch.

Discussion

In the current study, we investigated whether human infants are sensitive to pleasant touch by assessing their levels of physiological arousal and behavioral engagement while being stroked at varying velocities (slow, medium, and fast). In line with our predictions, the current results revealed that only when stroked at medium velocity, (a) infants’ heart rate decelerated, which reflects increased parasympathetic activity and is indicative of a decrease in arousal, and (b) infants’ behavioral engagement with the stroking object (brush) increased, which is indicative of an increased interest in the stroking object. These findings support the notion that pleasant touch plays a vital role in human social interactions by demonstrating that the sensitivity to pleasant touch emerges early in human development.

Critically, infants’ selective physiological (decrease in heart rate) and behavioral (increased engagement) responses to medium-velocity brushing are in line with the response profile of a special class of nerve fibers in human adults—the CLTM afferents (which show preferential activity in response to medium-velocity brushing; see Löken et al., 2009). This suggests that the physiological and behavioral effects observed in infants might be related to CLTM afferent function. Note that a direct test of CLTM afferent function is unlikely to be carried out because of ethical and technical concerns. Therefore, the current approach can be seen as an indirect but effective way of illuminating CLTM afferent function in human infants. Furthermore, our results show that infants’ physiological and behavioral responses are unlikely to be related to the discriminative touch system mediated by myelinated Aβ fibers. If our measures had been influenced by the discriminative touch system, we should have observed a linear relationship between the velocity of touch and our physiological and behavioral measures, but this was not the case. Our findings therefore provide evidence for a selective responsiveness to medium-velocity touch in 9-month-old infants. This physiological and behavioral sensitivity might serve important adaptive functions, because caregiving touch has been shown to be essential for promoting healthy social and cognitive development (Feldman et al., 2009; Field, 2010).

It is important to note that the observed decrease in heart rate in response to pleasant-touch stimuli agrees with the existing view that touch and its positive influence on mood, growth, and development rely on parasympathetic activity (Field, 2010). Generally, heart rate deceleration is thought to reflect parasympathetic activity facilitating an orienting reflex (Graham & Jackson, 1970) and has been observed in response to sedative music treatments in premature infants (Lorch, Lorch, Diefendorf, & Earl, 1994; Shenfield, Trehub, & Nakata, 2003). The observed heart rate deceleration in response to pleasant-touch stimuli may be related to findings showing that touch attenuates heart rate increases in anticipation of electrical shock (Anderson & Gantt, 1966). Clearly, more work, including a wider range of measures, is needed to elucidate the exact physiological nature of pleasant touch and its effects in infancy.

Our analysis further revealed that decreases in each infant’s heart rate during the medium (but not during the slow or fast) condition were correlated with his or her parents’ score on the STQ. This finding, as well as the fact that in the heart rate data, standard errors were greater than the mean changes across conditions, suggests that there is variation in the infants’ responsiveness to pleasant touch. Individual differences might be attributed to differences in the primary caregiver’s sensitivity to social touch. From the current data, it remains unclear whether this association exists because (a) infants experience differing levels of social touch as a function of their caregiver’s sensitivity to social touch or (b) sensitivity to social touch is heritable and therefore correlated between caregivers and infants (Morrison et al., 2011).

In addition to the physiological responses, we assessed the behavioral engagement of infants during the experiment and observed greater attentional engagement with the stimulating brush during the medium-velocity condition than during the slow- and fast-velocity conditions. This shows that infants preferentially orient toward the object that produces the medium-velocity touch, and it provides behavioral evidence for infants’ sensitivity to pleasant-touch stimuli. Infants show this increased engagement even though they have to look away from an attention-grabbing (distractor) video stimulus in order to engage with the brush. Given the required disengagement from the video screen, this might be seen as even stronger evidence for a behavioral preference for the pleasant-touch stimulus. The observed behavioral preference in infants may be related to adults’ preference for medium-velocity stimuli, as indexed by their pleasantness ratings (Löken et al., 2009). However, it is also possible that medium-velocity stroking simply induces increased attention in the infant rather than a specific hedonic state.

It is interesting that despite the presence of the female experimenter performing the tactile stimulation, the behavioral effect was limited to the brush, as no significant effect was observed for engagement with the experimenter. This may be due to the fact that the experimenter’s attention was focused on the brush and therefore cued the infants’ attention toward that object (Grossmann & Farroni, 2009). Alternatively, this might be due to a heightened salience of the object causing this touch sensation. Regardless of the exact nature of this behavioral response, the current behavioral findings critically add to the heart rate results by demonstrating that infants at 9 months of age not only show a selective physiological response but also preferentially orient their attention to pleasant-touch stimuli.

In summary, through the direct assessment of physiological and behavioral responses to touch, the present study is the first to demonstrate that human infants are sensitive to medium-velocity pleasant touch. This supports the notion that the ability to perceive and sensitively respond to pleasant touch is vital from early in ontogeny because of its significance for affiliation, bonding, and biobehavioral synchrony, especially between caregivers and infants (Feldman, 2012; Feldman et al., 2009; Field, 2010). This study, by providing evidence for the existence of a functioning pleasant-touch system in human infants, lays the foundation for future work that should systematically examine this ability and its underlying physiological mechanisms, as well as its typical and atypical effects on social and cognitive development.