Edited by: Bernadette M. Fitzgibbon, Monash University, Australia
Reviewed by: Marinus Van IJzendoorn, Leiden University, Netherlands; Vittorio Gallese, University of Parma, Italy; Lisa Roque, Catolica-Lisbon School of Business and Economics, Portugal
*Correspondence: Barbara Manini and Daniela Cardone, Department of Neuroscience and Imaging, G. d'Annunzio University, Via dei Vestini 33, 66013 Chieti, Italy e-mail:
†These authors have contributed equally to this work.
This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.
Maternal attunement with an infant's emotional states is thought to represent a distinctive feature of the human primary bond. It implies the mother's ability of empathizing with her child in order to fulfil the child's needs in an immediate and appropriate manner. Thus, it is particularly involved in stressful situations. By assuming that maternal attunement embodies a direct sharing of physiological responses with the child, we compared the autonomic response of mothers observing their own distressed child with those of other women observing an unknown child involved in an ecological distressful condition (mishap paradigm). The hypothesis was that the adult's response was more attuned with the child's response in the former group than in the latter group. The autonomic response was non-invasively evaluated through the recording of the thermal facial imprints by means of thermal infrared (IR) imaging. Nine mother-child dyads and 9 woman-unknown child dyads were studied. We found marked similarities between the facial temperature dynamics of women and children along the experimental procedure, thus providing evidence for a direct emotional sharing within the adult-child dyad. The evidence for common dynamics in the time course of the temperatures was assessed through correlation analysis and, nevertheless, resulted stronger in the mother-child dyads than in the other women-child dyads. In addition, temporal analysis showed a faster response in mothers than in other women, thus confirming our study hypothesis. Besides confirming the extraordinary capability of IR imaging to preserve ecological context in the study of social or non-verbal interactions, these results suggest that maternity appears to potentiate the emotional attunement with the child. Although based on preliminary results, this study opens new perspectives in the study of the factors modulating vicarious socio-emotional processes.
Maternal attunement with a child is a key element of secure attachment relationships (Bowlby,
Maternal attunement with offspring is especially involved when mothers are facing infants' distress. As shown by a large amount of empirical evidence, mother's alertness and arousal increase because of the baby's distress signals (Swain et al.,
Beyond the ability to provide the right intervention in distressing situations, synchronization of the mother's responses to the infant's signals in typical dyadic interactions can be considered a key aspect of sensitive parenting, as it implies the promptness of the mother response (Bell and Ainsworth,
The autonomic nervous system seems to represent an elementary mechanism supporting emotional synchrony between mother and infant. According to Porges (
The physiological side of the mother-infant bond has been typically observed in stressful situations. Mother's and infant's cortisol reactivity were found to be strictly associated in the still-face paradigm, an interactive situation eliciting some degree of stress in infants (Haley and Stansbury,
The present study aimed to deepen the results found by our previous one (Ebisch et al.,
Fourteen children (seven male, age 39–45 months) participated in the study. All of the children were born at term and had a typical psychological and physical development. The adult sample was composed of eighteen women divided in two groups: the first one included nine mothers (age 25–43) who watched their own child during the experiment (“mothers,” M); the second sample was composed of 9 women (age 23–38) (“other woman,” OW). Four of these had preschool children not participating to the study, while the other five were not mother. The data about six out of nine mother-child dyads were included in our previous study (Ebisch et al.,
Prior to testing, each subject was left to acclimatize for 10–20 min to the experimental room and to allow the neutral condition skin temperature to stabilize. The recording rooms were set at standardized temperature (23°C), humidity (50–60%) without direct ventilation. The subjects sat comfortably on a chair during both the acclimatization and the measurement periods, without any restriction of body movements. Before the start of the experiment, the children underwent an adequate familiarization period to ease the psychological habituation to the setting and the experimenter, first in presence of their mothers, then followed by neutral interaction with the experimenter alone. During neutral interaction between the experimenter and the child, some toys were presented to allow the child to feel at ease and to get used to play with the experimenter.
After the neutral interaction with the experimenter, the children were exposed to a potential stressful experience, elicited by the “Mishap Paradigm” (Cole et al.,
In order to perform the analyses, the above mentioned phases were grouped in conditions. The neutral interaction defined the “neutral condition”; the presentation and playing phases together formed the “intermediate condition”; the mishap, re-entry and soothing phases together formed the “experimental condition.”
The “mothers” and the “other women,” naive about the specific content of the experiment, were invited to silently observe the children-experimenter interaction through a one-way mirror from a separated room. It was possible that two women (one for each group of dyads) watched at the same child together, though they could not see each other or interact as a screen was placed between them.
Facial thermal images for all of the subjects were recorded along the whole experimental procedure (acclimatization, neutral, intermediate, and experimental conditions).
Thermal IR imaging was performed by means of three digital thermal cameras FLIR SC660 (640 × 480 bolometer FPA, sensitivity: <30 mK @ 30°C). The acquisition frame rate was set to 15 Hz for each thermal camera.
Two remote-controlled video-cameras (Canon Vc-C50iR) were used to film the child for the behavioral analysis. Video-signals were sent to two video-recorders (BR-JVC) and mixed by a Pinnacle system (Liquid 6). Subsequently, the movies were processed through a specialized software (Interact Plus, Mangold) that allows to code behavior in synchrony with the ongoing movies of the children during the experiment. The toy presented to the children in the “Mishap Paradigm” was a black and white robot with a height of approximately 20 cm. When turning on the robot with a switch on its back, it started to walk and play music. Both hands of the robot could be opened and closed by means of pressing/relieving a button. One of the hands of the robot were prepared to break when manipulated by the child. The robot could be repaired only by the experimenter. The toys presented during neutral interaction between the experimenter and the child were a puzzle, a magic wand and 3-D book.
Following from the notion that different combinations of relevant signs in a mishap situation may be indicative of guilt (Barrett et al.,
Gaze and face |
Gaze aversion | The child stares into space, or toward the oblique low, or toward another insignificant object (excluding the broken toy and the experimenter). |
Lip rolled-in | Lower lip rolled-in; corners of mouth drawn. | |
Bodily tension |
Bodily avoidance | The child backs up while looking at the experimenter; or moves away from her, toward insignificant object, after focusing on her. |
Hunched shoulders | Relaxed or hunched shoulders. | |
Head lowered | Head hanging or tilted forward. | |
Arms |
Arms across body | Arms across the midline, held close to the body (e.g., hugging the body). |
Covering, touching face | The child covers or touches all or part of the face. | |
Fingers in mouth | Putting a finger or fingers in mouth. | |
Repair |
Trying to repair the object | The child tries to repair, to fix the toy or he/she manipulates it. It is not coded as repair if the action is meant to play. |
Verbalizations |
Confession | The child admits to have broken the toy e.g., saying “I broke it” or “I pulled this piece off.” |
Negative self-evaluation | The child judges him/herself negatively, e.g., saying “I am not able to play” or “I can't do it.” |
Comparisons were made between the playing, mishap and re-entry phases, because in these phases the children were engaged with the same object and that made more reliable the coding of their behaviors.
Two observers coded all the children for each phase and Kappa's ranged from 0.72 to 0.80 (all
A visual inspection of the changes in facial thermal imprints in all subjects was performed to qualitatively investigate the autonomic responses of the women and the children throughout the experiment. This analysis was followed by a quantitative estimation of temperature variations of the nasal tip. Referring to the literature about thermal signature of emotions (Shastri et al.,
Thermal signals have been extracted through the use of tracking software, developed with homemade Matlab algorithms (The Mathworks Inc., Natick, MA). The tracking algorithm is based on the 2-D cross-correlation between a template region, chosen by the user on the initial frame, and a similar ROI in a wider searching region, expected to contain the desired template in each of the following frames (Tangherlini et al.,
A comparison was made between the neutral, the intermediate, and the experimental conditions. Because the mishap paradigm is an ecological situation the duration of the conditions depended on the children spontaneous behaviors. Therefore, the timing of the experiment presented some variations within subject. The mean duration of neutral condition was 134.62 (
The thermal signals of the nasal tip for all the subjects were transformed in
A cross-correlation like analysis on each dyad's temperature signals during the experimental condition was also performed to test which delay between the signals corresponded their highest correlation value. For this purpose, Pearson correlation coefficients were computed by delaying the woman's signal with respect to the child's signal with 10, 20, 30, 40 s. For each group, the mean values of the delays corresponding to the highest dyad correlation were computed. A Mann–Whitney
As the “other women” group included four mothers, explorative descriptive analyses on the “other women” subgroups were performed to preliminarily investigate possible differences between other mothers and non-mothers. Pearson correlation coefficients were calculated on the individual dyads level for the other mothers and non-mothers subgroups. Furthermore, the temporal modulation of the signal was explored for the two subgroups.
Since the experiment duration depended on the child's behavior, signal resampling was performed to compare the three conditions and the three groups (children, mother, other women). Each temperature signal was resampled in order to obtain 300 data points for each condition, equally spared across the time duration of the condition (for the experimental condition, 120 samples were included for the mishap phase, 60 for the re-entry phase and 120 for the soothing phase). The resampled
Behavioral analyses showed that all children experienced an increase of distress in response to the mishap. Specifically, the repeated-measures ANOVA indicated that the children reacted in a different way in the playing, mishap and re-entry of experimenter phase [
Gaze and face | 14 | 0.57 | 0.51 | 0.86 | 0.36 | 0.71 | 0.47 |
Bodily tension | 14 | 0.14 | 0.36 | 0.36 | 0.50 | 0.50 | 0.52 |
Arms | 14 | 0.21 | 0.42 | 0.29 | 0.47 | 0.29 | 0.47 |
Repair | 14 | 0 | 0 | 0.64 | 0.50 | 0.43 | 0.51 |
Verbalizations | 14 | 0 | 0 | 0.21 | 0.43 | 0.21 | 0.43 |
Total scores | 14 | 1.71 | 0.47 | 2.42 | 0.51 | 2.28 | 0.61 |
A visual inspection of the facial thermal imprints was performed to investigate the presence of appreciable signs of autonomic responses in the mothers, the other women and the children throughout the experiment. The qualitative results resembled those already found in our previous work (Ebisch et al.,
A representative example of the facial thermal imprints of one mother-other woman-child triad is shown in Figure
Concerning the mother, no appreciable modulation of skin temperature distribution was detected during the intermediate condition. After the mishap as well as after the re-entry of the experimenter, the same thermal variations observed in the child could be appreciated in the mother. During the soothing phase, the mother showed a gradual and generalized increase of facial temperature, re-establishing the neutral condition state. Moreover, like the child, she showed an over response of the nasal tip temperature, compared to the start of the experiment.
Finally, the other woman did not show any signal modulation between neutral condition, intermediate condition, and mishap. During the experimenter re-entry, there was a cooling of the nasal tip, however, milder (using the same temperature scale and image contrast) than that showed by the child and the mother. In the soothing phase the other woman showed a recovery of the nasal tip temperature to the initial neutral condition value.
An ANOVA (3 × 3) was performed on the re-sampled
Table
1 | M-C | 0.53 |
0.67 |
2 | M-C | 0.51 |
0.76 |
3 | M-C | −0.51 |
0.71 |
4 | M-C | 0.49 |
0.84 |
5 | M-C | 0.86 |
0.91 |
6 | M-C | −0.64 |
0.94 |
7 | M-C | −0.61 |
0.28 |
8 | M-C | 0.86 |
0.97 |
9 | M-C | 0.06 |
0.23 |
10 | OW-C | −0.12 |
0.24 |
11 | OW-C | 0.26 |
0.58 |
12 | OW-C | −0.77 |
−0.03 |
13 | OW-C | −0.85 |
0.82 |
14 | OW-C | 0.35 |
−0.38 |
15 | OW-C | −0.24 |
0.75 |
16 | OW-C | 0.29 |
0.40 |
17 | OW-C | 0.93 |
0.71 |
18 | OW-C | −0.32 |
0.54 |
With respect to the other woman child-dyads, in 5 out of 9 cases there was an increase of correlation in the experimental condition, compared with the neutral condition. The mean value of the neutral condition correlation was
The comparison between the two groups suggested that there was no significant difference regarding correlation coefficients in the neutral condition (
Finally, an explorative descriptive analysis was performed in order to assess the differences in correlation coefficient between other mothers-child dyads and non-mother-child dyads belonging to the other women group. The mean correlation in the other mother-child dyads was
Table
1 | M-C | 0.24 |
0.94 |
0.92 |
0.90 |
|
2 | M-C | 0.24 |
0.21 |
0.19 |
0.16 |
|
3 | M-C | 0.34 |
0.41 |
0.5 |
0.58 |
|
4 | M-C | –0.34 |
–0.35 |
–0.39 |
–0.29 |
|
5 | M-C | 0.76 |
0.72 |
0.47 |
0.92 |
|
6 | M-C | 0.67 |
0.76 |
0.78 |
0.83 |
|
7 | M-C | 0.63 |
0.44 |
0.19 |
–0.03 |
|
8 | M-C | 0.74 |
0.50 |
0.13 |
–0.20 |
|
9 | M-C | 0.89 |
0.69 |
0.64 |
0.69 |
|
10 | OW-C | 0.75 |
0.79 |
0.84 |
0.88 |
|
11 | OW-C | 0.30 |
0.28 |
0.14 |
–0.17 |
|
12 | OW-C | 0.67 | 0.68 |
0.62 |
0.35 |
|
13 | OW-C | 0.51 |
0.28 |
0.35 |
0.45 |
|
14 | OW-C | 0.24 |
0.60 |
0.68 |
0.71 |
|
15 | OW-C | 0.51 |
0.49 |
0.49 |
0.47 |
|
16 | OW-C | 0.28 |
0.48 |
0.60 |
0.68 |
|
17 | OW-C | 0.55 |
–0.52 |
–0.53 |
–0.52 |
– |
18 | OW-C | 0.82 |
0.79 |
0.86 |
0.88 |
The average value of the maximum correlation coefficients for the mothers-child dyad group was
One mother-child dyad (dyad #6) reached its maximum correlation value at a 40-s delay, even though its correlation coefficient was already larger than 0.67 and significant at 0 time delay. By excluding this dyad from the group, the average value of the highest correlation coefficients did not change, but there was a significant decrease of the mean delay in which
The average value of the maximum correlation coefficients for the other woman-child dyad group was
Although aware of the small size of the sample, an explorative analysis was performed on the other women group, by dividing it in two subgroups: other mothers (i.e., mothers watching not their own child) and non-mothers. The mean of the maximum correlation coefficients in other mother-child dyads was
Figure
The present study focused on the physiological expression of the emotional attunement of mothers to their own children. We compared the autonomic response, measured through the nose tip temperature, of a group of mothers while watching their own child engaged in a stressful situation with that of another group of women observing unknown children in the same situation. According to the exiting literature, reporting increased behavioral responses and higher neural activation in mothers watching their own distressed child, we expected that the two groups would have presented differences with respect to either the intensity and/or the timing of their physiological reactions. Our results indicate that, for both groups of women, the considered autonomic response significantly changed during the experimental condition with respect to the neutral one. The emotional attunement resulted slightly stronger and much faster in the mother-child group than in the other women-child group.
Specifically, according to the hypothesis that the emotional attunement with another person embodies a direct sharing of visceral-autonomic responses (Konvalinka et al.,
Moreover, the highest cross-correlation coefficient values between the time courses of the adult-child dyad signals during the experimental condition were found at a very short or null delay for the mother-child group, whereas a much longer delay characterized the other women-child group.
Group average correlation coefficient values did not significantly differ between the two groups. This result may rise an apparent discrepancy between the results found at a group level and at a single dyad level results. Such a mismatch likely depends on the procedure used to perform the group analysis, which emphasized the shared signals modulations within the dyads. As the experiment was designed to maximally preserve the natural and ecological context, there were no a priori limits or timing for the time duration of the phases' time duration. Therefore, it was not possible to adopt a unique common time frame the whole at the group level.
The last finding suggests that the emotional promptness to one's own child's distress is a distinct feature of maternal attitude, thus confirming at a physiological level the largely confirmed results found at a behavioral level (Stern,
The explorative, qualitative analysis within the other women group suggested interesting preliminary information about possible differences between mothers and not mothers looking unknown children. The small size of the sample does not allow drawing any conclusion, but our results suggest to investigate further whether the other mothers may have a stronger autonomic attunement with child and a faster response than non-mothers. Such a result would be in accordance with previous fMRI data showing different responses in brain regions involved in the attachment and in the integration of autonomic states with social behavior to infant negative emotions between the mothers and non-mothers (e.g., hypothalamic–midbrain–limbic–paralimbic–cortical circuits) (Seifritz et al.,
The present study crucially extends the results obtained by our previous work (Ebisch et al.,
Our study present some limitations that should be addressed. Firstly, the sample size is somewhat small. Therefore, our results should be considered preliminary, but suggestive of new insights in the study of the body communication between adults and children. Larger sample would be desirable, even though it has to be recognized that is it difficult, and somehow complex, to involve young children with their parents in a physiological study on children's distress. However, we plan to enlarge the sample size. The choice of preserving the ecological context determined the needs for the rejection of a not irrelevant number of dyads because of the excessive movements of the child that caused a artifacts that our tracking software could not fix. In addition, it determined the impossibility for a obtaining a group average signal.
To conclude, the findings show that the child's distress evocates in the observing women a spontaneous autonomic response, which could reflect an emotional sharing ability, stronger and faster in the mothers. Therefore, our study supports the hypothesis that the maternal bond can modulate the promptness of the adult's response to the child's needs.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.