PAPER Touch attenuates infants��� physiological reactivity to stress Ruth Feldman, Magi Singer and Orna Zagoory Department of Psychology and the Gonda Brain Sciences Center, Bar-Ilan University, Israel Abstract Animal studies demonstrate that maternal touch and contact regulate infant stress, and handling during periods of maternal deprivation attenuates the stress response. To measure the effects of touch on infant stress reactivity during simulated maternal deprivation, 53 dyads were tested in two paradigms: still-face (SF) and still-face with maternal touch (SF+T). Maternal and infant cortisol levels were sampled at baseline, reactivity, and recovery and mother���s and infant���s cardiac vagal tone were measured during the free play, still-face, and reunion episodes of the procedure. Cortisol reactivity was higher among infants in the SF condition and while cortisol decreased at recovery for infants in the SF+T, it further increased for those in the SF. Vagal tone showed a greater suppression when SF was not accompanied by maternal touch. Touch synchrony during free play was associated with higher infant vagal tone, whereas touch myssynchrony ��� maternal tactile stimulation while the infant gaze averts ��� correlated with higher maternal and infant cortisol. In humans, as in mammals, the provision of touch during moments of maternal unavailability reduces infants��� physiological reactivity to stress. Introduction Animal studies indicate that maternal touch and contact carry a life-long organizing effect on the infant���s stress management systems and function to regulate the stress response (Champagne, 2008 Hofer, 1995 Meaney, 2001). Early maternal separation has been linked with long-term disruptions to the HPA-axis stress regulating system, resulting in increased baseline cortisol, altered patterns of cortisol reactivity, and disrupted recovery of the system following stress (Levine, 2005). On the other hand, touch and handling during periods of maternal deprivation were shown to buffer the negative effects of stress on the pup���s physiological reactivity (Weller & Feldman, 2003). Much less research has examined whether touch during moments of maternal deprivation has a similar regulating effect on the stress response of the human infant. The notion that touch during periods of maternal deprivation attenuates the effects of separation on the human infant���s physiology is supported by research in premature infants. Prematurity provides a human model for the study of maternal deprivation, as mother and infant are separated immediately after birth, infants are placed in incubators, and full bodily contact is precluded during the post-birth period. Studies assessing the effects of skin-to-skin contact on the development of premature infants demonstrated that both stress hormones (Weller, Rozin, Goldstein, Charpak, Ruiz-Pelaez, Figueroa de Calume, Charpak & Sack, 2002) and autonomic reactivity (Feldman & Eidelman, 2003a Gray, Watt & Blass, 2000) were more optimal in the treated infants as compared to matched controls. Similarly, a daily regime of massage therapy improved cortisol reactivity and heart rate in premature infants (Field, 1995 Field & Diego, 2008). Similar to the long-lasting effects of early contact during periods of maternal deprivation on the stress response of young mammals, the positive effects of skin-to-skin contact on children���s cortisol response and autonomic reactivity were found to persist across the first 10 years of life (Feldman, 2009). Maternal still-face (SF) ��� an experimental paradigm in which mother interacts freely with the infant, then refrains from social communication and maintains a ���still-face���, and finally resumes play ��� has been extensively used to simulate the experience of ���maternal deprivation��� and examine its effects on the child (for review: Adamson & Frick, 2003). The negative effects of the mother���s momentary unavailability on the infant���s affect and behavior have been well documented, including high negative arousal, social withdrawal, increased self-soothing behavior, and re-engagement attempts. It has also been shown that during re-engagement much of the infant���s stress-related repertoire is still observed and this episode contains significantly more stress indicators than the initial free play (Weinberg & Tronick, 1996). In terms of its impact on infant physiology, the SF procedure has been shown Address for correspondence: Ruth Feldman, Department of Psychology and the Gonda Brain Sciences Center, Bar-Ilan University, Ramat-Gan, Israel 52900 e-mail: feldman@mail.biu.ac.il �� 2009 The Authors. Journal compilation �� 2010 Blackwell Publishing Ltd, 9600 Garsington Road, Oxford OX4 2DQ, UK and 350 Main Street, Malden, MA 02148, USA. Developmental Science 13:2 (2010), pp 271���278 DOI: 10.1111/j.1467-7687.2009.00890.x

to increase both cortisol levels and heart rate in infants (Haley & Stansbury, 2003 Lewis & Ramsay, 2005), indicating that the procedure creates sufficient stress to elicit a multi-dimensional physiological stress response. Several studies used a modification of the SF paradigm that includes maternal touch during the SF episode (SF+T) and examined the differential effects of touch versus no-touch conditions on infant behavior. Touch during maternal SF reduced the infant���s distress and elicited less crying, negative arousal, self-soothing behavior, and gaze aversion as compared to the standard SF (Stack & Muir, 1992). It has been suggested that during moments of maternal unavailability, touch functions to uphold the affective communication when other communicative channels are blocked (Jean & Stack, 2008). Whether or not this tactile continuity also attenuates the infant���s physiological reactivity has not been examined. Such findings may suggest that the breech in social communication leading to physiological and emotional distress may be somewhat ameliorated by the continuation of tactile contact. In addition to the momentary effects of touch on the stress response, maternal touch is a central determinant of the mother���infant communication system and carries a long-term impact on infant growth and development. Maternal affectionate touch in the postpartum, a behavior akin to the licking-and-grooming of mam- mals, has been associated with higher oxytocin whereas more intrusive types of stimulatory or functional touch have been correlated with higher maternal cortisol (Feldman, Weller, Zagoory-Sharon & Levine, 2007 Fleming, O���Day & Kraemer, 1999). Frequent maternal affectionate touch in the postpartum is related to higher infant baseline vagal tone (Feldman & Eidelman, 2007) and contributes to neurobehavioral, cognitive and social- emotional growth (Feldman & Eidelman, 2003b, 2004). Touch synchrony ��� the matching of maternal affectionate touch with mother and child���s mutual gaze ��� has been shown to predict more optimal attachment behaviors, better regulation of negative arousal, and lower behavior problems (Feldman & Eidelman, 2004 Feldman, Granat & Gilboa-Schechtman, 2005). It is thus possible that more attuned and synchronous interactions that incorporate touch into the mutually regulating social system may facilitate more optimal autonomic and hormonal stress reactivity, whereas aversive touch that is not suited to the infant���s communicative signals may be less conducive in downregulating physiological distress. In light of the above, the present study examined the effects of maternal touch during moments of maternal unavailability on the infant���s stress response. We expected that the SF+T condition would elicit significantly less physiological stress as expressed in lower cortisol reactivity and quicker cortisol recovery. We similarly expected that the SF+T condition would be associated with milder withdrawal of the vagal brake. According to Porges��� (2003) polyvagal theory, vagal tone (Vna) ��� the respiratory cycle in heart rate variability that is controlled by the regulatory parasympathetic system ��� reflects the mammalian capacity to mobilize sufficient energy to react to environmental challenges. Change in Vna from baseline to a stressful condition, the vagal brake, measures the organism���s adaptive response to stress, and the degree of Vna suppression indexes the level of experienced stress (Porges, 1995). Studies have shown that infants��� vagal tone withdraws in response to situational stress, including change from free play to the SF episode (Bazhenova, Plonskaia & Porges, 2001 Moore & Calkins, 2004), from free play to maternal separation during the ���strange situation��� paradigm (Hill-Soderlund, Mills-Koonce, Propper, Calkins, Granger, Moore, Gariepy & Cox, 2008), and in response to physical pain such as circumcision or heel- prick (Arditi, Feldman & Eidelman, 2006 Porter, Porges & Marshall, 1988), confirming that a decrease in Vna serves as an index for the magnitude of the stress response. In terms of the tactile component in the mother���s general interactive style, based on research showing links between more positive and synchronous interactions during the free play episode with lower cortisol (Haley & Stansbury, 2003) and more optimal vagal regulation (Moore & Calkins, 2004), we expected that touch synchrony would be related to more adaptive physiological reactivity, whereas myssynchrony ��� the mother���s stimulatory touch while the infant gaze averts ��� would correlate with more intense expressions of the stress response. Method Participants Fifty-three mothers and their 6-month-old infants (25 boys, M = 25.65 weeks, SD = 1.30) participated. The original sample included 66 dyads but in 13 cases one or more cortisol assessment points were missing. Mothers were recruited on the 2nd post-birth day and were screened for symptoms of anxiety and depression in the postpartum and again at 6 months. Inclusion criteria were: singleton healthy infant, mother married or cohabitating with the infant���s father, mother with at least high-school education, and mother over 21 years. Mothers were on average 28.9 years (SD = 4.0) and completed 14.6 (SD = 2.3) years of education. Procedure Mothers and infants arrived at the laboratory during the morning hours. Upon arrival, dyads were introduced to the lab and baseline salivary cortisol was assayed from mother and child. Mothers placed a roll of cotton in their own and the infant���s mouth and both chewed on it for 1 minute until it became saturated and was placed in 272 Ruth Feldman et al. �� 2009 The Authors. Journal compilation �� 2010 Blackwell Publishing Ltd.