Therapeutic touch and therapeutic alliance in pediatric care and neonatology: An active inference framework

Abstract

Therapeutic affective touch has been recognized as essential for survival, nurturing supportive interpersonal interactions, accelerating recovery-including reducing hospitalisations, and promoting overall health and building robust therapeutic alliances. Through the lens of active inference, we present an integrative model, combining therapeutic touch and communication, to achieve biobehavioural synchrony. This model speaks to how the brain develops a generative model required for recovery, developing successful therapeutic alliances, and regulating allostasis within paediatric manual therapy. We apply active inference to explain the neurophysiological and behavioural mechanisms that underwrite the development and maintenance of synchronous relationships through touch. This paper foregrounds the crucial role of therapeutic touch in developing a solid therapeutic alliance, the clinical effectiveness of paediatric care, and triadic synchrony between health care practitioner, caregiver, and infant in a variety of clinical situations. We start by providing a brief overview of the significance and clinical role of touch in the development of social interactions in infants; facilitating a positive therapeutic alliance and restoring homeostasis through touch to allow a more efficient process of allostatic regulation. Moreover, we explain the role of CT tactile afferents in achieving positive clinical outcomes and updating prior beliefs. We then discuss how touch is implemented in treatment sessions to promote cooperative interactions in the clinic and facilitate theory of mind. This underwrites biobehavioural synchrony, epistemic trust, empathy, and the resolution of uncertainty. The ensuing framework is underpinned by a critical application of the active inference framework to the fields of pediatrics and neonatology.

Full text

EDITED BY
Darren J. Edwards,
Swansea University, United Kingdom
REVIEWED BY
Patrice Duquette,
Independent researcher, Birmingham, MI,
United States
Sean Hagberg,
Affect Neuro, Inc, United States
*CORRESPONDENCE
Jorge E. Esteves
osteojorge@gmail.com
SPECIALTY SECTION
This article was submitted to Children and
Health, a section of the journal Frontiers in
Pediatrics
RECEIVED 03 June 2022
ACCEPTED 07 February 2023
PUBLISHED 27 February 2023
CITATION
McParlin Z, Cerritelli F, Manzotti A, Friston KJ
and Esteves JE (2023) Therapeutic touch and
therapeutic alliance in pediatric care and
neonatology: An active inference framework.
Front. Pediatr. 11:961075.
doi: 10.3389/fped.2023.961075
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© 2023 Mcparlin, Cerritelli, Manzotti, Friston
and Esteves. This is an open-access article
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Therapeutic touch and
therapeutic alliance in pediatric
care and neonatology: An active
inference framework
Zoe McParlin1, Francesco Cerritelli2*, Andrea Manzotti1,2,3,
Karl J Friston4and Jorge E Esteves1,5,6*
1
Foundation COME Collaboration, Clinical-Based Human Research Department, Pescara, Italy,
2
Division
of Neonatology, “V. Buzzi”Children’s Hospital, ASST-FBF-Sacco, Milan, Italy,
3
Research Department,
SOMA, Istituto Osteopatia Milano, Milan, Italy,
4
Wellcome Centre for Human Neuroimaging, Institute of
Neurology, Queen Square, London, United Kingdom,
5
Malta ICOM Educational, Malta, Finland,
6
Research
Department, University College of Osteopathy, Research Department, London, United Kingdom
Therapeutic affective touch has been recognized as essential for survival, nurturing
supportive interpersonal interactions, accelerating recovery—including reducing
hospitalisations, and promoting overall health and building robust therapeutic
alliances. Through the lens of active inference, we present an integrative model,
combining therapeutic touch and communication, to achieve biobehavioural
synchrony. This model speaks to how the brain develops a generative model
required for recovery, developing successful therapeutic alliances, and regulating
allostasis within paediatric manual therapy. We apply active inference to explain
the neurophysiological and behavioural mechanisms that underwrite the
development and maintenance of synchronous relationships through touch. This
paper foregrounds the crucial role of therapeutic touch in developing a solid
therapeutic alliance, the clinical effectiveness of paediatric care, and triadic
synchrony between health care practitioner, caregiver, and infant in a variety of
clinical situations. We start by providing a brief overview of the significance and
clinical role of touch in the development of social interactions in infants;
facilitating a positive therapeutic alliance and restoring homeostasis through
touch to allow a more efficient process of allostatic regulation. Moreover, we
explain the role of CT tactile afferents in achieving positive clinical outcomes
and updating prior beliefs. We then discuss how touch is implemented in
treatment sessions to promote cooperative interactions in the clinic and
facilitate theory of mind. This underwrites biobehavioural synchrony, epistemic
trust, empathy, and the resolution of uncertainty. The ensuing framework is
underpinned by a critical application of the active inference framework to the
fields of pediatrics and neonatology.
KEYWORDS
therapeutic alliance, active inference, affective touch, perinatal care, synchrony
Introduction
Therapeutic touch has been shown to have positive physiological and psychological
benefits for the pediatric population. This practice can be traced back to ancient China,
where therapeutic massage was used on infants (1). Touch is considered to be a powerful
sense in prenatal development, as it is the first sense to develop (2). Somatosensory
receptors begin to develop at 4–7 weeks of gestation and fetuses show movement in
response to touch on their lips at 7 weeks post-conception (3,4). Brain responses to
TYPE Hypothesis and Theory
PUBLISHED 27 February 2023
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DOI 10.3389/fped.2023.961075
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therapeutic touch begin between 11 and 36 days after birth, with
the same activation patterns in the somatosensory and insular
cortices observed in response to therapeutic touch in older
individuals (5,6).
Affective touch refers to the involvement of CT fibers in the
tactile processing of sensory information within an emotional
context (7). Low-velocity touch, often referred as affiliative,
affective, pleasant or therapeutic, is characterized by slow, gentle
stroking at skin temperature, typically 1 cm–10 cm/sec, which
activates the unmyelinated C-Tactile afferent nerve fibers in the
hairy skin. This type of touch is associated with the instinctual
caress of a parent towards their infant and has been found to
positively impact socio-emotional and cognitive development, as
well as physiological and stress markers (1,8–15). One well-
known example of this is Kangaroo Care, where an infant’s bare
skin is placed on the bare chest of a caregiver, which has been
shown to be beneficial in regulating an infant’s physiology for
over 40 years (16). In this paper, we will use the term
therapeutic touch to link our arguments more effectively to
paediatric care. Therapeutic touch has been shown to have a
significant impact on the physiological and psychological well-
being of neonatal and paediatric patients. Studies have found that
therapeutic touch can positively regulate physiological markers
such as epigenetics, neuroendocrine and stress markers (11,12).
These findings suggest that therapeutic touch plays a crucial role
in the development of infants’socio-emotional and cognitive
abilities, as well as their biobehavioural synchrony (1,10,13,14).
The positive effects of therapeutic touch on physiological and
psychological markers further highlight the importance of
incorporating this practice in healthcare settings, particularly for
vulnerable populations such as infants.
The Social Baseline Theory posits that humans have evolved to
be social creatures and that social interactions are essential for the
efficient regulation of physiological and psychological processes
(17,18). Biobehavioral synchrony refers to the coordination of
physiological and psychological processes during social
interactions, such as the coordination of nonverbal behaviour,
autonomic regulation, heart rhythms, brain-to-brain synchrony,
and the release of neurotransmitters like oxytocin (19,20).
Research has shown that when these systems are sufficiently
coupled, they exhibit similar dynamic neuronal structures,
including matching activations in the parietal and frontal
cortices, particularly during therapeutic touch (21,22). It is
suggested that caring therapeutic touch, which is both social and
affective, may contribute to biobehavioural synchrony, affective
physiological embodied predictions, and modulation of predictive
homeostasis and nervous, immune, and neuroendocrine
homeostatic regulation, which infants seem to outsource to
caring adults (23,24).
The therapeutic alliance, in the field of paediatrics and
neonatology, often refers to a collaborative relationship between
the child, parent, and practitioner. This alliance is essential for
understanding family-centred care, ensuring child and parent
satisfaction, and achieving positive clinical outcomes both in and
out of the clinic. In this paper, the term “practitioner”refers to
anyone providing manual or touch-based therapy, such as but
not limited to physiotherapists, osteopaths, chiropractors, and
massage therapists. A successful therapeutic alliance in
paediatrics and neonatology encompasses the three core
characteristics as described by Bordin (25); agreement on goals,
tasks, and the development of a harmonious relationship between
the therapist, patient, and their family. A strong therapeutic
alliance is crucial for ensuring mutual trust, collaboration, and
safety in all aspects of care (26). This is particularly important
when dealing with a paediatric population, where the practitioner
frequently encounters complex triadic relationships that depend
on the interactions between the practitioner, caregiver, and patient.
Active inference is a theoretical framework that aims to
understand sentient behavior by proposing that the brain actively
creates generative predictive models of the external world based
on the likelihood of incoming sensory inputs from both the
individual’s inner (interoceptive or proprioceptive) and outer
(exteroceptive) environment. This creates the individual’s own
multisensory perception of the world, which may differ from
reality (27,28). It is important to note that the brain and
nervous system prioritize balance and regulation in order to
achieve a state of allostasis, or the expected physiological needs
for survival (29–31). In the pediatric population, managing
allostasis is closely connected to collaborative rapport and
biobehavioral synchrony with others, as infants are unable to
regulate their essential physiology, such as body temperature,
without external help. Therapeutic touch has been proposed as
an effective method for achieving allostatic regulation,
physiological co-regulation, and embodied predictions related to
social attachments, especially in infants with limited
communication abilities (24,32–34). The potential benefits of
therapeutic touch may be partly attributed to its involvement of
the insular cortex, which plays a fundamental role in attachment,
alliance, and allostatic regulation, promoting rewarding
synchronization, balance, and reducing pain (34,35).
We propose that the use of therapeutic affective touch in
paediatric manual therapy can facilitate the development of an
ecological (therapeutic) niche and enhance the formation of a
positive triadic collaborative relationship between the patient,
caregiver, and therapist. Based on our recently published framework
on the role of therapeutic touch in promoting biobehavioral
synchrony within the clinical encounter (34), we suggest that touch
is a crucial tool in facilitating homeostatic and allostatic regulation,
ultimately enhancing the effectiveness of paediatric care.
Application of active inference to
touch and therapeutic alliance
Predictive coding postulates that the brain retains a sensitive
balance of its internal generative model of how unobservable
causes in the external and inner worlds generate sensations such
as top-down predictions and bottom-up sensory inputs (28,36).
When there is a discrepancy between the expected or predicated
sensory stimulation and the actual sensory input being
experienced, the difference is referred to as a prediction error (37).
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These prediction errors are used to guide and update prior or
existing beliefs if deemed more precise, which are necessary to
minimize this discrepancy that challenges and threatens their
current generative model (36,38–43). Precision reflects
expectations of predictability, with increased precision weighting
being elicited within a predictable and reliable setting (44).
Significantly the temporoparietal and medial temporal lobes
which are involved in both adapting, verifying, and reinforcing
prior beliefs in specific contexts are also activated in affective
touch (7,45). Additionally minimizing prediction errors ensures
self-regulation efficiency while also minimizing something called
variational free energy, especially in ambiguous situations (46,
47). In this setting, free energy is the statistical measure of
surprise or discrepancy associated with an unpredicted sensory
stimulus in their current generative model (48). It has also been
suggested that using additional sensory stimulation through
therapeutic touch could minimize free energy. Research shows
that comforting massage therapy for five days in preterm
neonates significantly decreased energy expenditure to 1.8 Kcal/
Kg/24 h (49). Similarly, individuals often collaborate to find the
most efficient action through therapeutic touch. Intuitively, this
amounts to minimizing the effort required to maintain
homeostasis and accomplish the crucial task of growth and
recovery, which is especially critical for infants who cannot
usually achieve this on their own (18,50,51).
Significantly, the precision bestowed on a prediction error can
be irrational and maladaptive, especially in chronic pain patients,
physiologically and psychologically. Physiologically, the brain can
alter the sensory states by increasing the precision to the selected
sensory state allowing the belief to be updated at the higher
levels of neural processing and correspondingly increasing the
synaptic gain of secondary sensory and association cortices
representing the associated prediction errors (52–54).
Psychologically, this manifests as sensory attenuation (of sensory
prediction errors) or selective attention (by increasing the
precision of sensory prediction errors). This kind of precision
weighting is mediated by modulating the gain of neural
populations encoding prediction errors (55–59). The attenuation
of sensory prediction errors can also be crucially applied to
healthcare because it could determine whether an individual will
actively ignore or pay attention to specific sensory data,
especially in chronic pain (46). When someone is in chronic
pain, it is not necessarily movement that causes the pain; instead,
it is the inability to attenuate sensory evidence such as touch (31,
60). In other words, in an attempt to explain away
somatosensory prediction errors that cannot be attenuated, the
hypothesis of “I am in pain”is invoked, with all the
accompanying pain-related behavior.
Similarly, this failure to attenuate sensory prediction errors
could account for the self-stimulation and misalignment in
dyadic interactions observed in severe autism; a syndrome
thought to be characterized by a failure to attenuate sensory
precision (61–65). It has been suggested that autism’s lack of
coherence between the brain’s neural processing and touch
awareness may contribute to these individuals’inability to
recognize or explain therapeutic touch (66).
Moreover, it has been argued that, by using fMRI, it is possible
to identify and minimize atypical responses and the processing of
affective touch in children, allowing Therapist to observe and
monitor the condition’s development through therapeutic touch
(67,68). Notwithstanding this, certain forms of therapeutic
massage appear to be effective in addressing and rehabilitating
these touch-averse preferences in autistic children by reducing
anxiety, increasing social communication and encouraging
bonding (69). Therapeutic touch can be used to assist in focusing
attention (i.e., optimizing precision gain) for specific prediction
errors by modulating and deregulating top-down predictions
initiated by touch-specific neurotransmitters in the
hypothalamus-pituitary adrenocortical system (24,70–75).
Subsequently, generating a positive influence and makes sense of
the physical world, helping the child become skilled in or
mentalize the deployment of attention to current interoceptive
signals; that they may struggle to do in conditions like autism.
This may make it easier to nuance the precision afforded to
higher-level prior beliefs to facilitate belief updating via
attunement and synchrony rather than relying on previous
expectations or priors (10,41,42,76,77). In a pediatric clinic
setting, where there is often a triadic hierarchy, the practitioner is
often perceived to have more authority and knowledge. This
hierarchical model can influence the caregiver and child to rely
on the practitioner’s guidance in order to reduce their prediction
errors and uncertainty, ultimately promoting homeostasis. In
short, therapeutic touch enables individuals to recognize their
maladaptive and overly precise beliefs and attempt to update or
normalize them through a shared narrative of mutually predicted
sensations; for example, learning that a fall does not necessarily
mean they have broken something within a predictable and
reliable setting (31,44).
The impact of touch on biobehavioural
synchrony and infant physiology
Intentional social touch, particularly at speeds that activate CT
fibers during social interactions, has been proposed to play a crucial
role in attachment, communication, and regulation of physiology
of individuals (78). Therapeutic touch interventions, such as
massage, have been linked to various physiological benefits.
Studies have found that these interventions can increase vagal
tone, oxygen saturation, and dopamine levels, while decreasing
cortisol, oxytocin, and stress levels (79–83). Additionally, it has
been suggested that affective social touch can also contribute to
establishing biobehavioral synchrony, which is known to assist in
regulating an infant’s physiology.
Affective CT-mediated touch is commonly used as an efficient
medium for communication through social exchanges in various
forms, such as a simple one-way exchange like a hand on a
shoulder or dynamic reciprocal exchanges like a hug (84). This
type of touch is considered an invaluable mode of
communication, as it is used across cultures in various
combinations to convey emotions through nonverbal exchanges
(84). Social touch can effectively convey a wide range of
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emotions, including sadness, happiness, alertness, and calmness,
and can contribute to the processing of facial emotions even if
the touch is not directly targeted at the receiver (85,86).
Additionally, it is important to note that affective social touch is
believed to have the same significance as direct gaze in four-
month-old infants (87).
Social touch is often used in a reciprocal manner to communicate
with others and build relationships. This is reflected in the way that
dopaminergic reward systems respond to individuals touching each
other. In fact, research has found that even one-month-old infants
can potentially perceive pleasant touch and express motivation for
future interactions, as demonstrated by somatosensory and insular
activation reported by Tuulari et al. (5). Additionally, affective touch
has been widely reported to reciprocally increase oxytocin levels in
both individuals (88). However, in cases of post-natal depression
where mothers engage in less touch, including affective, affectionate
and breastfeeding, and in negative ways (e.g., rough pulling), infants
may subsequently touch themselves more, potentially to compensate
forthislackoftouch(89,90). This can lead to delays and negative
consequences in socio-emotional and cognitive development,
including higher risk of insecure attachment and bonding, as well as
reduced cortisol levels (10,14,91). Furthermore, adults who
experienced reduced touch early in life may not find affective touch
more pleasant than other forms, suggesting that we may need to
learn to enjoy and engage in touch (78,92).
Affective touch plays a crucial role in facilitating mutual
understanding, regulating physiology, and forming a robust
therapeutic alliance between the practitioner, patient, and caregiver
(82,84,87,93,94). Through the frequent use of affective touch as
a mode of communication, it can help to develop behavioral
synchrony, coupling, and a shared dynamic neural code between
the practitioner, patient and their family (95). This can lead to an
increase in rapport, trust, and mutual respect in the therapeutic
relationship, allowing the caregiver to provide more supportive
and autonomous care to the child’s clinical needs (96,97).
Furthermore, incorporating family-centered care, which takes into
consideration the values, attitudes, and context of the child’s
family in conjunction with the biomedical aspects of treatment, is
regarded as best practice in pediatrics. The use of therapeutic
affective touch in conjunction with family-centered care can help
to attain patient satisfaction, biobehavioral synchrony, therapeutic
alliance, and cooperative communication and improve both
physical and psychological well-being for conditions such as
juvenile idiopathic arthritis (96–100).
The application of biobehavioral synchrony in parent-infant
interactions has been shown to result in a high level of
synchronization, particularly with mother-infant heart rates,
following therapeutic affective touch (80,101). Research has also
demonstrated that the oxytocin levels of mothers and fathers,
following 15 min of play including affectionate and affective
touch with their child, can predict the exact increase in oxytocin
levels that the child will experience, due to the synchronization
of the parents’hormones and behavior within the triadic family
unit (102). At three months of age, infants are able to initiate
synchronization of coordinated affectionate affective touch and
body movements with their parents to achieve parasympathetic
co-regulation, owing to the increased vagal tone acquired during
social engagement (103,104). Furthermore, therapeutic touch has
been shown to assist in the physiological adaptation and
regulation of the autonomic system following birth trauma or
daily life stresses, through skin-to-skin and affective touch
immediately following birth, and when being carried while the
parent walks, increasing cardio-respiratory coupling parameters
such as heart rate variability and body temperature, while
decreasing crying and body movements (105–107). The available
evidence suggests that biobehavioral synchrony, established
through affectionate affective touch, can assist young infants in
developing a blueprint for achieving and creating generative
models for their physiological needs (103,104).
The significance of parental touch in the development and
well-being of infants has been well-documented in various
studies. As proposed by Meaney et al. (108), parental touch can
signal to the infant that their environment is safe and supportive,
allowing them to adapt and thrive in that environment. This
theory is supported by research that has shown how caregiving
touch evokes physiological and epigenetic changes that decrease
stress responses and enable increased infant learning and
exploration (78,109). Furthermore, a study by Feldman (110)
found that premature infants who received skin-to-skin contact
exhibited better exploratory behaviours at 6 months of age,
highlighting the positive impact of parental touch on infant
development. Overall, it is clear that parental touch plays a
crucial role in the formation of a secure attachment, the
regulation of physiology, and the development of cognitive and
socio-emotional skills in infants.
Consequently, long-term infant-caregiver biobehavioral
synchrony can be observed, with preterm infants receiving
Kangaroo care showing greater synchrony than preterm infants
receiving incubator care. However, this synchrony is less
pronounced compared to that observed in full-term infants (33).
But, by adulthood, adult child-parent synchrony is equal between
preterm infants who received kangaroo care and full-term
infants, highlighting the lasting impact of therapeutic touch on
the long-term synchrony between mother and infant (33).
Touch and allostatic regulation in
paediatrics and neonatology
The concept of allostasis, which refers to the continuous
adjustment of an individual’s internal physiological or behavioural
state through a complex neuro-humoral system, is central to
understanding how therapeutic touch can aid in the regulation of
an individual’sphysiology(33,111). Social affiliation, whether
intentional or not, can assist in co-regulating another individual
and strengthen their relationship, as they subconsciously recognize
that the other individual plays a crucial role in regulating their
allostasis and fulfilling their interoceptive predictions more
efficiently (23,112). Affective parental touch, such as stroking, can
aid in aspects of cognitive, metacognitive, and embodiment
processing, particularly in infants whose brains are still too
immature to efficiently regulate themselves (24,110,113). This
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type of touch is considered an embodiment ostensive cue, serving the
evolutionary need to assist, change or delay another individual’s
interoceptive needs by creating opportunities or epistemic gains,
such as facial recognition (86,104). Overall, therapeutic touch can
contribute to allostatic regulation by providing a sensory stimulus
to create, modify, or update existing beliefs.
Feldman’s 2020 study on “kangaroo care”investigated the
long-term effects of 2 weeks of skin-to-skin contact in premature,
low birthweight infants compared to maternal separation (110).
The study found improved autonomic function, orientation, and
information processing in the neonatal period, consistent with
other research suggesting that parental touch contributes to co-
regulation and synchronization between an infant and a
caregiver, potentially reducing cortisol and respiratory rate,
regulating peripheral and core temperatures in premature or
newborn infants, and addressing a variety of critical physiological
vulnerabilities in neonates (114–117). The study also found
continued improvements in physiological and cognitive
regulation, arousal, and social interactions up to 2 years old and
at 10 years old, the infants showed more adaptive autonomic
nervous systems in terms of cardiac and stress regulation,
cognitive flexibility, and sleep patterns compared to the separated
infants. This may be partly due to synchronization with a
caregiver, helping to minimize prediction errors and regulate
allostasis, especially during times of distress or uncertainty in the
external environment, which could put additional strain on their
allostatic regulation (23,118,119). Additionally, socio-affective
regulation elicited by touch can result in beneficial changes in
inflammation, immunity, stress, and allostatic load, as well as the
effort required to maintain homeostasis in critically ill,
premature, or multifactorial medical conditions (18,51,120,121).
Feldman (2022) also found that individuals who received
“kangaroo care”(skin-to-skin contact) in their infancy exhibited
more adaptable empathic responses in young adulthood (18–20
years). The increased synchrony from early attachment
experiences is believed to have provided a pathway between the
amygdala, insular and temporal pole, allowing for better
recognition and understanding of others’affective states, thereby
preparing them for adult social life (110). Furthermore, the
combination of insular projections and specific temporo-social
computations exhibited in social touch interactions allows for the
creation of joint predictive models, which can aid in
understanding and predicting the behaviour of others (33,59).
Therapeutic touch, such as massage, has been shown to have a
positive impact on individuals experiencing allostatic overload by
promoting relaxation and reducing stress levels. Studies have
found that therapeutic touch can increase vagal tone, oxygen
saturation, and dopamine levels, while decreasing cortisol,
oxytocin, and stress levels (79–83). Additionally, therapeutic
touch is believed to symbolize the physical unity of the
therapeutic alliance, indicating that the practitioner is willing to
share their resources and work together with the patient to
resolve clinical symptoms (18). Furthermore, research suggests
that receiving therapeutic touch is more effective than self-care at
mitigating and regulating the effects of physical and emotional
stress (110,122).
This theory, paired with the social concept of “mommy”
suggested by Atzil and colleagues (2018), can be applied in a
clinical setting (23). “Mommy”represents a computational
predictive model that uses previous experiences of exteroceptive
information about a caregiver associated with interoceptive
information about allostasis, with the brain subsequently making
predictions for allostatic regulation based on social information
or vice versa. Patients experiencing symptomatic distress will
have gathered interoceptive information, such as pain from
inflammatory mediators, to infer that they are facing allostatic
overload. It has been suggested that patients may have developed
exteroceptive beliefs that practitioners generally have expertise
and success in promoting recovery, or from previous experiences
with practitioners, to help them infer that treatment, including
manual therapeutic touch, will contribute to their recovery.
Additionally, it has been suggested that patients can remember a
particular practitioner’s distinctive touch or feel they understand
their specific pathology from previous painful episodes. By
examining, treating, reassuring, and assisting the patient in
reconnecting and learning about their injury through tactile
feedback, practitioners can help reduce allostatic overload, while
also assisting in developing a successful therapeutic alliance and
interpersonal relationship (118,123).
Despite some promising clinical results for therapeutic affective
touch, its effectiveness remains uncertain. Practitioners recognize
that their outcomes are influenced by various sensory modalities,
including non-verbal and verbal communication, which can
impact a patient’s recovery (31,124). It is possible that
expectation-associated placebo effects contribute to reduced pain
reported in sham treatments, particularly in chronic pain,
through non-conscious Bayesian biases (31). During a
therapeutic intervention, whether sham or standard, the body’s
regulatory system makes inferences about internal and external
states to minimize prediction errors and regulate allostasis (125).
Therapeutic affective touch provides the individual with evidence
to update their existing beliefs. Implementing therapeutic touch
within a supportive environment can help patients infer that the
touch will aid in resolving their symptoms.
Touch exploration, developing and
adapting priors through coupled
action-perception cycles
Affective touch, particularly in social situations, has been
shown to play a role in direct affective and socio-affective
regulation through cognitive and embodied processes, including
behavioural synchrony, leading to physiological co-regulation
(24). Affective and therapeutic touch can aid in recreating
biofeedback loops that enhance the salience and learning of
allostatic regulation in specific contexts. Early social contact has
been linked to the development of positive evolutionary beliefs
and physiological mechanisms, such as dopaminergic and
opioidergic pathways, that promote and enjoy social touch and
attachments (126). Furthermore, the perception of affective touch
is not only associated with attachment patterns but also with the
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intent of the individual experiencing pain modulation from touch
(127). Caregiving affective touch, including touch used in daily
caregiving tasks such as feeding, washing, and transporting, has
been found to be soothing and linked to embodied mentalization
of interoception. This suggests that essential daily caregiving
tasks not only promote attachment but also help modulate infant
physiology and internal beliefs, shaping future allostatic
predictions and generative models (24,51). Caregiving affective
touch can secure interoceptive predictions, reducing prediction
errors and providing calming effects, reducing infant distress
(128). An example of this would be a caregiver who picks up a
crying infant to feed them, fulfilling their allostatic nutritional
needs while providing social support and comfort to reduce
distress. Affective touch in social environments has been
suggested to provide external opportunities for individuals to
learn how to self-regulate their own allostasis in specific social
and physical situations (112,129).
Stroking and other forms of affective touch activate CT fibres
thus activating the central hubs and pathways for oxytocinergic
modulation, triggering the release of oxytocin. Oxytocin plays a
significant role in both social attachments and providing allostatic
regulation through the modulation and regulation of social and
non-social behaviours within fluctuating social contexts (130,131).
Additionally, it has been suggested that social affective touch in
childhood may optimize an adult’s ability to utilize oxytocin when
dealing with stress as adults. Affective touch, by triggering the
release of oxytocin, allows individuals to expect and perceive touch
as being pleasant, therefore motivating, stress-regulating and
increasing the sense of safety in regard to their cognitive and
external environment (109,132). This sense of safety has been
suggested as the theoretical mechanism behind why Tanaka and
colleagues found that infants that received more social touch,
particularly affectionate affective touch, had enhanced object
exploration, both in reduced hesitancy to explore objects and spent
more time exploring them than infants that received less touch.
Additionally, the infants may be motivated to explore their external
environment to receive potential rewards with less risk, anxiety, or
punishment (133). This can be observed in infants who intuitively
adapt their sucking mechanism to different textures and
temperatures, such as from a mother’s nipple to a bottle plastic
nipple, to meet their nutritional requirements for survival, with
body temperature creating the most optimal conditions for the
activation of C-tactile afferents (134–136). Body movements and
tactile sensations are crucial for exploratory perceptual learning of
(the consequences of) foundational actions, with the changing
proprioceptive information helping reveal the object’s pure tactile
properties (137).
The intention behind therapeutic affective touch may
significantly impact how practitioners establish a therapeutic
alliance through their portrayal of therapeutic touch, implying an
enactive component to therapeutic touch (124). By using
therapeutic touch that activates CT fibres and triggers the release
of oxytocin, practitioners can communicate and reassure the
patient with a sense of safety about their clinical condition, as
reflected by an increase in heart rate variability of preterm
infants after experiencing CT-activating stroking, which helps
regulate their parasympathetic nervous system (138).
Additionally, therapeutic affective touch activates the brain to
develop sensitivity or trust to specific affective stimuli as a
modality for acquiring precise, safe, and newsworthy sensory
information, resulting in an increased sense of self-awareness
(139). Even at 14 weeks gestation, twins direct their movements
toward their co-twin to explore, communicate, and differentiate
self from others, thereby effectively developing self-awareness and
early social affective touch (140,141). It is important to note that
while exploration is predominantly detected through hedonic AB
fibres than CT fibres, research by Sailer and Ackerley (92)
concluded that individuals with reduced touch exposure interpret
hedonic touch differently from controls, controversially
perceiving it as more pleasant than affective touch, suggesting
that the normal perception of gentle dynamic touch can in some
cases overlap with other forms of touch. It has also been argued
that a significant proportion of infant exploration occurs within
social situations where the use of affective social touch is more
prominent and environmental safety plays a bigger role.
Coupled action-perception cycles
within treatment
The process of aligning one’s beliefs and actions with those of
others to create a shared understanding is known as the canonical
loop of coupled action-perception cycles (59). In clinical settings,
incorporating therapeutic affective touch into social interactions
between the practitioner, patient, and their families can enhance
alignment and synchrony at multiple levels (142). This allows for
the use of action-perception loops to infer and synchronize
mental states through touch as a means of communication.
Additionally, therapeutic affective touch can have a significant
impact when treating infants, as it allows for the constant
inference of mental states that may not be fully conveyed
through verbal explanations and reassurance (143).
It is important to note that in triadic relationships, personal
biases are often more pronounced and influential than in dyadic
interactions and are typically expressed through physical social
affective touch and social gaze (144). Additionally, factors such
as gender can affect the way in which caregivers display and
interpret social touch (145). For example, compared to mother-
infant interactions which are characterized by gradual positive
effects centred around intricate facial cues, father-infant
interactions are typically characterized by high, abrupt arousal
with numerous peaks centred on more physical play and games
(145,146). Similarly, it is suggested that similar mechanisms
occur in therapist-infant interactions, as they are more likely to
resemble a combination of affective slow movements as well as
physical object-focus play, with therapeutic affective touch as the
primary mode of communication.
Another important aspect to consider is that affective touch,
while being a fundamental building block for inferring an
infant’s internal state during caregiving tasks, is only one aspect
of multisensory interactions that also includes visual, auditory,
and olfactory stimuli. Within a clinical setting, while affective
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Frontiers in Pediatrics 06 frontiersin.org

therapeutic touch is often the primary mode of communication
during sessions, other sensory stimuli also play a role. Research
has shown that therapeutic touch, compared to verbal
reassurance, can significantly reduce stress by affecting
physiological, epigenetic, and neuroendocrine functions, thus
demonstrating its superiority in providing social support,
particularly in times of pain or distress (108,147,148).
We propose that the mechanism of developing neural synchrony
in a clinical setting is heavily influenced and enhanced by therapeutic
touch. This can be explained by expanding and combining the models
proposed by Shamay-Tsoory and Eisenberg (122) and Bilek and co-
workers (93). During consultations, the practitioner begins by
evaluating the patient’s clinical presentation in the context of
allostatic overload and disrupted homeostasis, which establishes the
diagnostic evaluation. Subsequently, the practitioner adjusts their
thinking to reflect this decision and accompanying mental state.
This mental state will manifest itself in the practitioner’sbehaviour,
such as their facial expressions and how they conduct their hands-
on evaluation and therapeutic intervention. The patient and
caregiver will observe and sense these behaviours, often through
affective touch, ultimately inferring the practitioner’s mental states.
Subsequently, their actions will influence the interpretation and
adaptation of their predictions and biases if the recipient
determines the suggested theory is more precise. Due to the
practitioner’s expertise and potentially therapeutic affective touch
through the triggering of oxytocin, their diagnosis is likely to be
regarded as more precise and trustworthy than the patient’sor
caregiver’s assessment of the source of the pain. Moreover, the
patient and caregivers will be able to assess rapport and the
robustness of the therapeutic alliance through touch and other non-
verbal cues (96). Anticipating how the patient and caregiver will
react is accomplished through top-down predictions made prior to
theresponseoccurring(149). The practitioner’s constant inference
about the patient’s mental states enables them to adapt their use of
therapeutic affective touch, helping to create opportunities for the
patient to modify and mitigate their predictions to increase the
success of the therapeutic intervention. The exteroceptive cues
obtained by the practitioner through therapeutic touch, in
conjunction with subsequent cognitive and affective reassurance and
empathy, is transferred to the insula during treatment and has been
proposed to integrate into the development of new and updated
priors to prepare for and regulate future allostatic disturbances (150,
151). As a result, the neural coupling, synchronization, and
alignment that occurs in the default, higher-level temporal and
parietal regions during this process will aid in the prediction of
future interactions like this one (152). Arguably, this process will
aid in the positive adaptation of maladaptive beliefs and learning in
paediatric patients and their caregivers.
The functional anatomy of touch and
empathy within a clinical encounter
Empathy is an essential element of establishing a robust
therapeutic alliance, enhancing patient satisfaction, clinical
outcomes, reassurance, compliance, and assisting in reducing
distress (153,154). Empathy is central for practitioners to
understand, acknowledge, and appreciate the patient’s symptoms
and difficulties on the road to recovery to foster trust and a strong
relationship (25). The more empathy and respect the practitioner
demonstrate to the patient and family, the stronger the therapeutic
alliance is likely to be within triadic interactions, thereby
increasing the clinical effectiveness of the intervention (98,122).
The capacity to empathise with another stems from prior
biobehavioural synchronous relationships, experiences, and
predictions about social interactions involving emotion
regulation, stress management, and cognitive control (33,104).
Through experience-dependent plasticity in the temporal,
prefrontal, parietal, amgydala and insula regions it has been
suggested that therapeutic touch in childhood enhances the
ability to accurately recognize other people’s emotions allowing
young adults to empathise with others (33). These adaptations
occur due to the integration of subcortical, paralimbic, and
cortical structures that combine bottom-up recognition of others’
emotions with top-down mentalization and emotional regulation
to display an empathic response (155). Moreover, the amygdala
and insula play an essential role in empathy and socio-emotional
regulation and the development of mother-infant synchrony,
which frequently indicates an individual’s future ability and level
of empathy (33,156,157). This is reflected in the fact that
children who receive affective touch consistently throughout their
childhood are more sensitive to the emotions of others as
adolescents and thus become more empathic and likely to build
better therapeutic alliances in the future.
Ulmer-Yanvi and colleagues (33) proposed that skin-to-skin
contact occurring from infancy contributes to establishing
integrative interoceptive cues that develop the complex
mechanisms needed to establish empathy. Research suggests that
the insula, during therapeutic affective touch, assists in updating
and creating prior beliefs via a mechanism of integrating
interoceptive cues and social values, which also correlates to the
neuronal activity when experiencing pain or displaying empathy
(158,159). Additionally, the insula projects to the temporal lobe,
which is involved in mentalization and theory of mind. The
temporal lobe further integrates salient socio-emotional sensory
inputs into higher-order concepts through its role as a paralimbic
region, before projecting to the amygdala (160). The amygdala
plays a role in emotional and social processing and goal setting
before developing a response to stimuli and emotional states,
which is then modulated by the ventral medial prefrontal cortex
(VMPFC). The VMPFC modulates the overall process once more
due to its significant reciprocal connections with both the insula
and temporal lobe. The VMPFC generates affect-specific
empathic responses by considering current arousal, social,
internal states, and emotional intensity. Furthermore, the
VMPFC plays a crucial role in developing synchrony, the
modulation of oxytocin-related stress, the sense of safety, and
pain, all of which can be modulated through therapeutic touch
and are integral to therapeutic care. This neurological framework
of touch and its subsequent biobehavioural synchrony within a
clinical setting corresponds to activation, particularly in the
anterior mid-cingulate cortex, inferior parietal lobes, and anterior
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insula, enabling individuals to demonstrate empathic qualities
essential for the formation of a successful alliance (21,161).
Moreover, the shared emotions experienced during synchrony
initiated by therapeutic affective touch allows for more efficient
communication and precise inference of emotions and actions by
reinforcing and increasing their relationship, attachment, feelings,
and priors. Unsurprising that empathy is subsequently regarded
as a crucial aspect of a superior practitioner and establishing a
robust alliance, given its interconnections with attachment and
synchrony, as well as its role in establishing a shared narrative,
experience, emotional transfer, and reinforcing the belief that
everyone is the same (see Figure 1).
The clinical role of touch in
overcoming uncertainty through
creating a safe clinical environment
Bowlby (1988) proposed that an attachment figure can provide
another individual with a strong sense of security (162).
Therapeutic touch, which includes slow movements, skin-to-skin
contact, and carrying, is a type of “comfort contact”that can help
the recipient feel at ease, supported, and secure in the presence of
another person, while also promoting stress regulation and healthy
physiological and psychological development (51,163,164). The
attachment bond between a mother and infant, which is often
strengthened and initiated through tactile afferent touch, also
underpins an infant’s safety and comfort (165,166). Moreover, it
has been demonstrated that an effective alliance centred around
treatment using therapeutic affective touch improves the child’s
safety and the child’s and parent’swell-being(98). Therapeutic
touch can serve as a “secure base”by instilling a sense of social
support and security in the clinical setting, thereby enhancing the
robustness of the alliance and relationship with the patient (167,
168). Additionally, therapeutic affective touch is associated with
decreased physiological arousal, bidirectional physiological
regulation, and decreased pain thresholds (163). The relationship
between the toucher and receiver seems to play a role in how
touch is modulated and interpreted, with a closer relationship
allowing for a higher variety of locations, slower tempo, and more
intimate gestures (169–171). This is reflected in the responses
observed in the insula to slow therapeutic touch, which is more
significant than fast touch, observed in both 2-month-old and 2-
year-old infants (68).
Additionally, the social content, including the identity and
relationship of the toucher, seems to be more critical than other
external factors (169). However, it is important to note that Pirazzoli
et al. (2019) suggested that younger infants at 5 months old may
need a more robust multisensory social experience than touch alone
to identify touch as affective (172). Moreover, it has been suggested
FIGURE 1
Putative neuromodulatory effects of touch from an interoceptive and interpersonal inference perspective.
McParlin et al. 10.3389/fped.2023.961075
Frontiers in Pediatrics 08 frontiersin.org

that the sense of safety often felt because of affective social touch loses
its sensitivity as the individual gets older, partly as the attention bias for
social threat decreases with age, correlating with the common desire to
be independent from their parents (109,173).
The sense of security achieved in the pediatric clinical setting has
been attributed in part to the significant use of therapeutic affective
touch, which has been associated with decreased physiological
arousal, bidirectional physiological regulation, and decreased pain
thresholds (163). Therapeutic affective touch can physically represent
increased social support, which contributes to a sense of security by
assisting in the modulation of pain, detecting potentially noxious
stimuli, and augmenting the precision of non-noxious stimuli. These
FIGURE 2
Active inference in paediatric care and neonatology. HCP: Health Care Provider.
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changes are attributed to increased activation of the prefrontal cortex,
which is involved in pain modulation, sense of safety, and neural
synchrony (131,174). Therapeutic touch involving C-Tactile
afferents modulates nociceptive signaling, preventing signals from
reaching the brain and mediating nociceptive input at a subcortical
level (175). The activation of CT fibers has been linked to having an
FIGURE 3
A map of the different processes involved in therapeutic touch.
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Frontiers in Pediatrics 10 frontiersin.org

anti-nociceptive role, suppressing C-nociceptive activity, weakening the
temporal summation of second pain, and mediation of allodynia (176–
178). Moreover, combined with emotional support and activation of
the reward system triggered by comforting affective therapeutic
touch, patients can have an increased tolerance for noxious
nociceptive signals and thus an increased sense of security in
knowing that their allostatic and emotional regulatory needs will be
met (Figure 1).Additionally,thisisreflected in chronic pediatric
patients who also improve following massage therapy for
musculoskeletal symptoms such as muscle spasms, tension, oedema,
pain, distress, and mood disorders (179).
Conclusion
Therapeutic touch plays a critical role in regulating allostasis and
promoting homeostasis, developing socioemotional and cognitive
systems, and achieving a robust therapeutic alliance in the paediatric
population. Our research presents an integrative (active inference)
model that helps explain the mechanisms by which therapeutic
touch works. Through the use of this model, we propose that
therapeutic touch is essential in laying the groundwork for
biobehavioural synchrony via biopsychosocial mechanisms
(Figures 2,3). Furthermore, we suggest that touch can be used to
establish and update priors in exchanges between parent and infant
and between the practitioner and the infant. The intentional
therapeutic touch delivered by a practitioner can promote allostatic
regulation and establish a successful therapeutic alliance. Additional
research on the quantifiable effects of therapeutic touch in children
may better understand the mechanisms underlying already
established treatments involving therapeutic affective touch.
Furthermore, the effects of touch on reducing and preventing the
development of maladaptive pain beliefs and pain itself may
significantly enhance the effects of therapeutic affective touch.
Data availability statement
The original contributions presented in the study are included
in the article/Supplementary Material, further inquiries can be
directed to the corresponding author.
Author contributions
All authors contributed to the conception of the manuscript.
ZMcP wrote the first draft of the manuscript. All authors
contributed to manuscript revision. All authors contributed to
the article and approved the submitted version.
Funding
The authors declare that the research was conducted in the
absence of any commercial or financial contributions. KJF is
supported by funding for the Wellcome Centre for Human
Neuroimaging (Ref: 205103/Z/16/Z) and a Canada-UK Artificial
Intelligence Initiative (Ref: ES/T01279X/1).
Acknowledgments
The authors thank Andrea Bacceli for his help in
realising the figures, and members from the Active
Inference Research Group for their productive feedback on
the framework.
Conflict of interest
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.
Publisher’s note
All claims expressed in this article are solely those of
the authors and do not necessarily represent those of their
affiliated organizations, or those of the publisher, the
editors and the reviewers. Any product that may be
evaluated in this article, or claim that may be made by
its manufacturer, is not guaranteed or endorsed by the
publisher.
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