Petrocchi & Cheli

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Psychology and Psychotherapy: Theory, Research and Practice (2019)


© 2019 The British Psychological Society
www.wileyonlinelibrary.com

Special issue paper


The social brain and heart rate variability:
Implications for psychotherapy
Nicola Petrocchi1,2* and Simone Cheli3,4
1
Economics and Social Sciences, John Cabot University, Rome, Italy
2
Compassionate Mind Italia, Rome, Italy
3
School of Human Health Sciences, University of Florence, Italy
4
Center for Psychology and Health, Tages Onlus, Florence, Italy

Purpose. Humans evolved within the mammalian line as a highly social species. Indeed,
sociality has been a major driver of human social intelligence. From birth, social
relationships have emotional and self-regulating properties and operate through different
body systems. This paper will explore how heart rate variability (HRV), an index of the vagal
regulation of the heart and a central element of the physiological underpinnings of sociality,
is related to mental health problems, with important implications for psychotherapy.
Methods. We conducted a narrative review of the literature on the bi-directional links
between prosocial motivations, HRV, and psychophysiological functioning.
Results. HRV is associated not only with the ability to downregulate physiological
arousal, but also with a variety of psychological and behavioural variables which are usually
the target of psychotherapeutic interventions. A modern neurovisceral integration model
can be employed to explain the complex intercorrelation between HRV and
psychophysiological functioning. In particular, the link between HRV, the experience of
inter- and intrapersonal safeness, and the inhibitory function of the prefrontal cortex will
be explored in the context of prosocial motives, such as compassion, that alleviate and
help prevent mental health difficulties.
Conclusions. Our knowledge of the social brain and its physiological underpinnings
might influence important elements of a therapeutic intervention, from the initial
assessment of patient’s difficulties to the evaluation of therapy outcomes.

Practitioner points
! Social relationships have emotional and self-regulating properties.
! The experience of inter- and intrapersonal safeness is connected to prosocial motives, such as
compassion, and the inhibitory function of the prefrontal cortex.
! Social relationships and compassion influence different body systems, such as the vagus nerve.
! Many forms of psychopathology represent the activation of evolved, defensive strategies especially in
contexts where there are few stimuli indicating safeness and social support.
! Heart rate variability predicts psychotherapy outcome.

*Correspondence should be addressed to Nicola Petrocchi, Economics and Social Sciences, John Cabot University, Via della
Lungara 233, Rome 00165, Italy (email: [email protected]).

DOI:10.1111/papt.12224
2 Nicola Petrocchi and Simone Cheli

While most species engage in social behaviour, be it competing for resources, mating, and
offspring caring (see Gilbert, this volume), the human brain is unusually eusocial, capable
of extended caregiving, complex cooperation, and coherent social behaviour. These
adaptations were associated with major changes in the brain. Around two million years
ago, early humanoids known as Homo habilis had a brain capacity of 650–700 cm3.
Today, our brain capacity is twice that, at around 1,450 cm3, with the frontal cortex being
especially important. The ratio of cortex to total brain size is estimated to be 67% in
monkeys, 75% in apes, and 80% in humans. These changes provide the physiological
underpinning for wide range of complex competencies, including language, fine motor
movements, symbolic thinking, self-awareness, and empathy. We are also highly
physiologically regulated via our relationships (see Gilbert, this volume; Siegel, this
volume).
According to the ‘social brain hypothesis’ (Dunbar, 2009), human intelligence and
psychophysiological functioning evolved primarily as a means to solve problems, namely
surviving and reproducing, in the specific human ecology characterized by larger and
more complex social groups. In particular, a range of emotional and motivational systems
evolved because they helped meet the challenges of survival and gene replication in
competitive environments (Gilbert, 2015a, 2015b). Our social evolution, with its new
motives, needs and competencies have extensive implications for understanding mental
health problems and psychotherapy.
A central evolutionary adaptation for mammals, and especially humans, that stands
out above those of sex, fighting, and status seeking is ‘affiliative’ sociality (Atzil, Gao,
Fradkin, & Barrett, 2018), a core feature of which is caregiving and responding to
care, help, and support (Gilbert, 1989; Mayseless, 2016). Caring and affiliative
motivations are embedded in human nature and rooted in evolutionarily developed
brain systems that we share with other mammals (Panksepp, 1998). In fact, ‘unlike
reptiles and other phylogenetically more ancient vertebrates, birth for mammals is not
a transition into independence, but an extension of the period of dependence that
begins in utero’ (Porges & Furman, 2010, p. 3). Even when humans become more
physically and emotionally independent of their caregivers, they create dyads with
appropriate others (partners, friends, therapist, etc.) with whom they initiate patterns
of interaction to create psychophysiological co-regulation. These patterns of complex
co-regulating interactions are like ‘social dances’ and are rooted in social mentalities
(see Gilbert, this volume). The sections below explore how upregulation of the
parasympathetic system in humans, as indexed by heart rate variability (HRV), is
linked to the experience of safeness and to prosocial motives and emotions that
alleviate and help prevent mental health difficulties. As such, these processes are new
targets for psychotherapy interventions.

The vagus nerve and the neurovisceral integration model


As detailed by Porges in the polyvagal theory, the evolution of caring and the ‘hyper-
affiliative’ tendencies of human being were paralleled by changes in neural regulation of
the autonomic nervous system (ANS; Porges, 2007). One major adaptation has been the
evolution of a branch of the parasympathetic system, the myelinated vagus nerve (to the
heart), that inhibits sympathetically driven threat-defensive behaviours (e.g., fight/flight)
and hypothalamic–pituitary–adrenal (HPA) axis activity, and promotes a calm physiolog-
ical state that enables social affiliations, caring, and sharing. According to this theory, the
myelinated vagus nerve evolved with attachment and the ability for infants’ sympathetic
The social brain and heart rate variability 3

activity to be calmed by parental caring behaviours (Depue & Morrone-Strupinsky, 2005).


This is reflected in the dynamic balancing of the sympathetic and parasympathetic
nervous systems that gives rise to the variability in heart rate (HRV; Porges, 2007). Without
the influence of the vagal nerve, the cardiac pacemaker naturally creates a heart rate of
approximately 120 beats per minute. In the absence of perceived threats and in
conditions of perceived interpersonal (and later, intrapersonal) safeness, the vagal nerve
activity acts as a brake to slow down heart rate (toning down threat processing). The
synchronous operation of the two branches of the ANS generates a fluctuating pattern of
speeding up (via sympathetic activity) and then slowing down (via parasympathetic
braking) in heart’s beat-to-beat activity. The consequence is that the time between each
beat of the heart (the inter-beat interval) is never the same – it varies as the patterns of
speeding up and slowing arise. A measure of the degree of this variation in the times
between each heartbeat is called HRV. In conditions of perceived threats and reduced
safeness, the vagal brake is disengaged, which leads to an increase in heart rate. The
capacity to spontaneously disengage and re-engage the vagal brake is indicated by higher
HRV: Thus, higher HRV (i.e., more variability of the inter-beat intervals) is related with
greater abilities to regulate stress and arousal (Thayer & Lane, 2000, 2009). Lower resting
HRV has been implicated with chronic reduced ability to downregulate psychophysio-
logical arousal observed in chronic stress activation (Thayer, ! Ahs, Fredrikson, Sollers, &
Wager, 2012).
What is crucial for psychotherapists is that the vagal tone is associated not only with
the ability to downregulate physiological arousal, but also with a variety of psychological
and behavioural variables which are usually the target of psychotherapeutic interven-
tions. Higher HRV is associated with greater capacity for emotion regulation (Appelhans &
Luecken, 2006; Mather & Thayer, 2018), metacognitive awareness and mind reading
(Lischke, Lemke, Neubert, Hamm, & Lotze, 2017; Meessen, S€ utterlin, Gauggel, &
Forkmann, 2018), empathy and alexithymia (Lischke et al., 2018), and with greater
performance on several cognitive tasks involving attention, working memory, and
inhibitory control (Hansen, Johnsen, & Thayer, 2003, 2009; Ottaviani et al., 2018; Saus
et al., 2006). Relevantly, higher vagal tone has also been associated with better physical
health: better glucose regulation, better HPA axis function, reduced inflammation,
reduced risk for cardiovascular disease, and all-cause mortality (Hillebrand et al., 2013;
Rothberg, Lees, Clifton-Bligh, & Lal, 2016; Thayer & Fischer, 2009; Thayer, Yamamoto, &
Brosschot, 2010).
To explain the complex intercorrelation between HRV and psychophysiological
functioning, Thayer and Lane (2000, 2009), in their neurovisceral integration model, have
described a central autonomic network (CAN), a set of neural structures (including the
anterior cingulate, insula, ventromedial prefrontal cortex [PFC], amygdala, and hypotha-
lamus) through which the brain regulates visceromotor, neuroendocrine, and behavioural
responses that are critical for goal-directed behaviour and adaptability. This regulation is
mainly exerted trough inhibitory processes. In fact, in line with current neurobiological
evidence (Motzkin, Philippi, Wolf, Baskaya, & Koenigs, 2015) and evolutionary reasoning
(Gilbert, 1993; Nesse, 2005), it has been postulated that ‘the stress response is a default
response of the organism, and that it is the response the organism automatically falls back
upon when no other information (i.e., safeness) is available’ (Brosschot, Verkuil, &
Thayer, 2018, p. 2). The CAN and the PFC, in particular, are crucial structures in this
process. In safe contexts, the amygdala appears to be inhibited by the PFC. This has been
confirmed by studies in healthy humans showing tonic inhibition of the amygdala by the
PFC (Delgado, Nearing, Ledoux, & Phelps, 2008). Under conditions of unsafeness and
4 Nicola Petrocchi and Simone Cheli

threat, critical areas of the PFC become hypoactive: The removal of inhibition ‘permits’
rather than ‘causes’ the activation of the amygdala and the threat response, with parallel
reductions in HRV (Makovac et al., 2016). In fact, the primary output of the CAN is
mediated through parasympathetic neurons (the vagus nerve) which innervate the heart,
exerting an inhibitory control over it, and generating the variability in the timing of
heartbeats (HRV). Crucially, the heart and the brain are connected bi-directionally:
Efferent inputs from the brain affect the heart and afferent outflow from the heart affects
the brain (Critchley, Nagai, Gray, & Mathias, 2011). The vagus is a central component of
this heart–brain system: Thus, vagally mediated HRV is more than just an index of healthy
heart function and represents a marker of the inhibitory prefrontal processes, as a recent
meta-analysis confirms (Thayer et al., 2012). Consistent with the hypothesis that the
stress response is a default response of the organism and that tonic inhibition is reflected
by high HRV, it has been shown that greater HRV is associated with a smaller negativity
bias (the tendency to prioritize negative information over positive), greater willingness to
approach novelty (Shook, Fazio, & Vasey, 2007), and more rapid extinction in an fear
conditioning paradigm (Pappens et al., 2014). On the other hand, abnormally low resting
HRV and large reductions in HRV to different tasks (e.g., emotion evocation) are
associated with a wide range of psychopathological syndromes including anxiety
disorders, attention problems, autism, callousness, depression, and schizophrenia
(Beauchaine & Thayer, 2015).

Evolved caring: compassion, safeness, and HRV


The characterization above has important implications for future clinical psychologists
and psychotherapists. For example, as suggested by Brosschot et al. (2018), when a client
comes to our office presenting problems of chronic stress response, dysregulated
negative emotions, and massive defence mechanisms, the problem should not be
formulated as ‘What triggers this stress/anxiety response?’ but as ‘When/why do the
mechanisms that normally downregulate the default threat response fail to work?’ In line
with evolutionary theory, it has been hypothesized that the mechanism that explains most
threat responses is the perception of interpersonal unsafeness (Brosschot, Verkuil &
Thayer, 2017; Gilbert, 1989, 1993). In fact, it has long been recognized that the sense of
interpersonal safeness is ‘an evolutionary adaptive, information-organizing system which
has major effects on biological patterns, social behaviour, relationships and the
maturation of self-constructs’ (Gilbert, 1993, p. 131). When organisms fail to perceive
safeness (e.g., in social environments dominated by loneliness, separation–rejection or
dynamics of power and subordination), subcortical inhibition by the PFC is decreased and
amygdala activity is enhanced, causing the default threat response to remain activated (a
condition indexed by lower vagally mediated HRV). In fact, it has long been suggested that
many forms of psychopathology represent the activation of evolved, defensive strategies
especially in contexts where there are few stimuli indicating safeness and social support
(Gilbert, 2015b). In addition, our evolved human minds are capable of creating internal
relationships with ourselves (we can feel supportive, indifferent, or hostile to ourselves)
which generate a sense ‘intrapersonal unsafeness’ (Longe et al., 2010). Accordingly, both
interpersonal and intrapersonal (i.e., self-criticism) maltreatment have shown a strong
link with reduced HRV (Dale et al., 2018; Petrocchi, Ottaviani, & Couyoumdjian, 2017).
On the other hand, it is increasingly becoming clear that certain motivational
orientation with prosocial focus on self and others, such as compassion, is more strongly
The social brain and heart rate variability 5

conducive to a sense of perceived social safeness, and thus to increased emotion


regulation and inhibition of the default threat response (Gilbert, 2014, 2015a,b; Hermanto
& Zuroff, 2016; Petrocchi & Couyoumdjian, 2016). Compassion can be considered the
expression of the extended caregiving system, which has emerged from evolutionarily
ancient motivations to detect and respond to the need of dependent offspring. The caring
motivation would extend, through evolution, to the welfare of all living beings and,
crucially, to the self (Gilbert, 1989; Goetz, Keltner, & Simon-Thomas, 2010; Mayseless,
2016; Wang, 2005). This is captured in such definitions as ‘having a sensitivity to suffering
in self and others, with a commitment to alleviate and prevent it’ (Gilbert, 2017).
Experimental research has consistently shown that triggering the motivational state of
compassion both for others and for ourselves is, in fact, linked to higher HRV. For
example, showing videos of other’s suffering has found to induce vagally mediated heart
rate deceleration (higher HRV) in children (Eisenberg, Fabes, Bustamante, Mathy, & Al,
1988); moreover, increased HRV was positively related not only to self-reports of
sympathy and compassion (Eisenberg, Fabes, Schaller, Miller, & Al, 1991), but also to
subsequent helping behaviour (Eisenberg, Fabes, Miller, Fultz, & Al, 1989). Increased HRV
in adults has been found to be specifically connected to the emotional state of compassion
and not to positive affect in general (Stellar, Cohen, Oveis, & Keltner, 2015). Thus, HRV
seems to be linked to the sense of safeness that derives from greater ability to self-soothe
when stressed, which inhibits the distress-related tendencies to fight with or withdraw
from suffering, facilitating engagement with the suffering (in one selves and others). From
an evolutionary point of view, it is crucial to put the sense of safeness and its
psychophysiological marker (increased HRV) in the context of interpersonal motivations,
that is, what makes the internal and external world safe for humans (Gilbert, 2015b).
Importantly, the element of sensitivity to suffering and caring seems to be particularly
linked to increased HRV. For example, a very similar prosocial motivation, cooperation, is
not always connected to increased vagal tone (Sari~ nana-Gonz#alez, Romero-Mart#ınez, &
Moya-Albiol, 2018). In fact, cooperating with someone does not necessarily imply
sensitiveness to the suffering of the other and the desire to alleviate it; nor does it imply
affiliation, benevolence, or any interest in the well-being of the other. Moreover,
cooperation can be Machiavellian and rooted in self-interest. One may temporarily
cooperate with a stranger or even an ‘enemy’ towards a common goal without being
sensitive to his/her suffering or concerned with their well-being. Accordingly, activating
caring motivations, and benevolent intent, such as compassion (both for ourselves and
others), in order to downregulate threat responses and achieve better emotion regulation,
is at the core of modern evolutionary and biopsychosocial psychotherapeutic approaches,
such as compassion-focused therapy (Gilbert, 2010, 2014, 2015b).
The focus on prosocial affiliative motivations such as compassion becomes salient
when a psychotherapist employs other well-validated mind training processes to help
with emotion regulation. For example, mindfulness practices are now a common thread
across different modern psychotherapeutic approaches. However, the rationale of
applying such approaches can vary. On the one hand, mindfulness techniques are
intended to promote ‘an uncoupling of the sensory dimension of pain experience from
the affective evaluative alarm reaction’ (Kabat-Zinn, 1982, p. 33). They were developed as
a way to modulate the threat and self-protection system. On the other hand, mindfulness
can be employed to develop awareness of evolutionary-based mental processes and
mechanisms that generate suffering, while increasing sensitivity and compassionate
commitment to alleviate that suffering (Gilbert, 2010). This latter approach, with its focus
on developing a caring orientation towards our own needs and suffering, and increase a
6 Nicola Petrocchi and Simone Cheli

sense of inner safeness, might potentially have a higher impact on vagal tone in the long
run, even if, at first, might require more effort and face more resistances (Lumma, Kok, &
Singer, 2015).

Biofeedback and compassion to increase HRV


What is particularly relevant for psychotherapists is that HRV does not only serve as an
indicator of the functioning of brain regulatory systems, but it also influences brain and
emotional functions. Accordingly, increasing parasympathetic regulation of the heart is
becoming a core target of modern integrative psychotherapeutic interventions. For
example, in studies on HRV biofeedback (for a review, see Lehrer & Gevirtz, 2014),
participants are taught to increase their HRV by breathing at around 10 s per breath (i.e.,
about 5 breaths per minute, for at least 20 min a day for several weeks), and they get
immediate feedback from a monitor on how successfully they are at increasing their HRV.
Paced breathing increases the amplitude of heart rate oscillations thanks to its ability to
synchronize with the physiological rhythm of the baroreflex (with a lag time of
approximately 10 s), which also has a strong influence over the heart rate. The rhythm of
the baroreflex cannot be directly manipulated, but it is possible to slow down our own
breathing to the frequency of the baroreflex, generating a non-linear effect (called
resonance frequency; Lehrer et al., 2013). This synchronization heightens the amplitude
of heart rate oscillations. It has been shown that high amplitude oscillations in heart rate
(i.e., higher vagal tone) regulate oscillatory activity in brain regions associated with
emotion regulation (Mather & Thayer, 2018), leading to heightened functional connec-
tivity in these emotion regulation networks. In fact, research indicates that emotion
regulation and HRV share the same structural underpinnings: Higher HRV is significantly
associated with blood flow in ventromedial PFC and the amygdala (Thayer et al., 2012),
higher medial PFC and amygdala functional connectivity (Sakaki et al., 2016), and greater
structural thickness in prefrontal regions (Yoo et al., 2017).
The psychotherapeutic benefits of actively modulating HRV are now widely
confirmed. A recent meta-analysis of 24 studies by Goessl, Curtiss, and Hofmann (2017)
revealed that HRV biofeedback training is associated with a large reduction in self-
reported stress and anxiety (the pre–post within-group effect size [Hedges’ g] was 0.81).
Combining HRV biofeedback with psychotherapy improves outcome in the treatment of
major depressive disorder (Caldwell & Steffen, 2018). Moreover, HRV biofeedback
protocols have shown to be highly effective in treating a variety of conditions (e.g.,
irritable bowel syndrome, Stern, Guiles, & Gevirtz, 2014; fibromyalgia, Hassett et al.,
2007; substance use disorders, Eddie, Kim, Lehrer, Deneke, & Bates, 2014; psychotic
symptoms, Clamor, Koenig, Thayer, & Lincoln, 2016), but also in improving psychical and
cognitive performances. Intriguingly, as noted by Mather and Thayer (2018), many
meditative and religious chanting practices (e.g., reciting either the rosary Ave Maria
prayer or a yoga mantra) lead to breathing at a 10-s/breath rate. This is crucial, considering
that benefits of meditative practices are usually attributed to the role of attentional training
and body awareness with little emphasis on the role of psychophysiological changes
induced by slow-paced breathing (H€ olzel et al., 2011).
In support of the inextricable and bidirectional link between HRV and prosocial
orientation (see Colonnello, Petrocchi, Farinelli, & Ottaviani, 2017 for a narrative review),
Bornemann, Kok, B€ ockler, and Singer (2016) have recently shown that participants asked
to voluntarily upregulate their HRV (using a novel biofeedback task) reported significant
The social brain and heart rate variability 7

increases in altruistic prosocial behaviour (i.e., helping behaviour, charitable donations,


generosity, interpersonal trust), but not non-altruistic forms of prosociality (i.e., not based
in care-motivation but rather in norm-adherence or self-focused motivation). Not
surprisingly, practices aimed to deliberately upregulate the parasympathetic system in
order to influence cognitive and emotional processes are at the core of modern
psychotherapeutic approaches based on integrative evolutionary and biopsychosocial
understanding of human functioning (Gilbert, 2010, 2015b). For example, in compassion-
focused therapy (a psychotherapy that actively targets physiological processes with
specific interventions), slow breathing and body-based practices are combined with
practices designed to activate compassionate motivation. So, training in body posture,
voice tone, facial expressions, and breathing patterns is padded with visualizations and
memory practices of receiving compassion and care from another sentient caring mind,
generating compassionate wishes for another, visualizing and acting as becoming a
compassionate person, using one’s compassionate mind state to work on various
difficulties such as trauma memories, shame, and self-criticism. A recent randomized
controlled trial found that this training increased HRV for participants (Matos et al., 2017)
and decreased shame, self-criticism, depression, and stress. Single practices aimed to
increase compassionate orientation towards ourselves, and others are also found to
increase HRV (Petrocchi et al., 2017; Rockliff, Gilbert, McEwan, Lightman, & Glover,
2008).

HRV, assessment, and psychotherapy outcome


An evolutionary and ‘social brain’ perspective on psychopathology and psychotherapy
highlights the co-regulating processes of emotions and motives and their impact on range
of physiological systems, including genetic expression (Gilbert, 2015a; Kumsta, this
volume). However, the contribution of psychophysiological methods is often under-
played in psychotherapy (Lehrer, 2018), and most psychotherapeutic approaches
emphasize verbal, cognitive, and behavioural treatment and assessment procedures
rather than body state assessments. Given the increasing importance of our understanding
of a range of body-based processes, such as even gut microbes and their impact on mental
states (Dinan & Cryan, 2017), future therapists will need to be knowledgeable on body
states including those associated with threat and safeness processing. Moreover, cultural
and linguistic diversity or psychopathological severity may significantly alter the viability
of cognitive and verbal processes. Integrating our standard strategies with assessment
tools and models that are focused also on physiological parameters (e.g., HRV) might
allow psychotherapists to assess and monitor patients’ sense of social threat versus social
safeness, and their ability to feel comfortable in operating in various social mentalities.
Indeed, change in these physiological parameters may affect the patient’s ability to
mentalize (Lischke et al., 2017, 2018; Meessen et al., 2018), and a threat to significant
relationships (therapeutic relationship too) may have a profound effect on physiological
systems (Liotti & Gilbert, 2011). Thus, as suggested by evolutionary approaches,
psychopathological assessment and diagnosis need to focus not only on symptoms and
syndromes, but also on the complex regulation of evolved strategies (such as the various
social mentalities; Gilbert, 2014, this volume), and their psychophysiological markers,
such as HRV. For example, Geisler, Kubiak, Siewert, and Weber (2013) found that baseline
HRV was positively associated with self-reported habitual use of strategies indicating
engagement coping (situation control, response control, positive self-instructions, social
support seeking). Moreover, baseline HRV predicted more use of socially adaptive
8 Nicola Petrocchi and Simone Cheli

emotion regulation strategies (i.e., social support seeking and making a concession as a
reaction to anger) after 28 days.
Measuring HRV as part of the initial assessment of a patient approaching
psychotherapy might also provide valuable indications of the tolerability of the therapy
process itself, and ultimately of its success. Considering that HRV levels reflect the ability
of an organism to respond and adapt flexibly to changing environments (e.g., to the
absence of an expected threat), it is not surprising to find correlations between HRV and
outcomes of psychotherapeutic interventions. In fact, entering and remaining in
psychotherapy, which often implies exposure to situations in which patients confront
what they most fear, demand high levels of self-regulation. Patients with particularly low
pre-treatment vagal tone may have lower levels of self-regulatory capacity and, therefore,
more pronounced difficulties in entering and/or remaining in psychotherapy. This is
particularly true for patients with high levels of fear of compassion, for whom the
therapeutic relationship per se can elicit a threat response (Dentale et al., 2017; Gilbert,
McEwan, Matos, & Rivis, 2011). Recent research has investigated the association
between pre-treatment vagal tone, dropout, and residual symptoms after exposure
therapy in a sample of 228 patients with panic disorder and agoraphobia (Wendt et al.,
2018). 17.1% of patients dropped out from therapy prior to post-assessment. In the
patients completing treatment, 12.3% showed a full recovery, and 70.6% still presented
residual symptoms (partial recovery) at the end of the treatment. Interestingly, the group
with residual symptoms and the treatment dropout group did not differ from the fully
recovered group with regard to initial levels of symptom severity. However, both the
group with residual symptoms and the treatment dropout group had lower pre-
treatment HRV than the fully recovered group. These findings indicate that patients with
panic disorder and agoraphobia with low pre-treatment HRV are more likely to drop out
or show residual symptoms after completing therapy. Similarly, baseline HRV predicts
psychotherapy outcomes in other disorders, such as pain-predominant multisomatoform
disorder (Angelovski, Sattel, Henningsen, & Sack, 2016), social anxiety (Thayer, 2018),
and depression (Jain et al., 2014), also when treated with antidepressant medication
(Kircanski, Williams, & Gotlib, 2018). Assessing pre-treatment levels of HRV might
become a common practice in future psychotherapeutic treatments. In fact, given the
strong influence of vagal tone on psychological functioning, a particularly low pre-
treatment level of HRV might compromise the effectiveness of some therapeutic
procedures. It can also indicate the need for a more body-based compassion-focused
work aimed at upregulating the parasympathetic system (e.g., soothing rhythm
breathing or compassionately dealing with self-criticism) before embarking in any
cognitive and behavioural technique (Gilbert, 2015b; Kirby, Doty, Petrocchi, & Gilbert,
2017).
On a similar note, HRV is increasingly used as a measure of treatment success in clinical
and research settings. In fact, even if self-report measurements are widely employed in
both clinical and research settings, we know that response to self-reports is influenced by
the ability of patients to identify and describe their emotional and motivational states, and
gives honest answers when such answers are socially undesirable. Unlike self-reports,
physiological measures are not subject to social desirability bias, and they might capture
elements of psychophysiological functioning that are beyond respondents’ conscious
control. Interestingly, data show that HRV is not influenced by placebo effect (Casadei,
Conway, Forfar, & Sleight, 1996) and it does not change over periods of months in the
absence of any intervention (Stein, Rich, Rottman, & Kleiger, 1995). Thus, HRV seems to
be an optimal indicator of therapeutic success. In fact, HRV changes have proved helpful
The social brain and heart rate variability 9

to evaluate the effects of different psychiatric treatments, such as drugs, cognitive


behavioural therapy, and transcranial magnetic stimulation (Frustaci, Lanza, Fernandez,
Giannantonio, & Pozzi, 2010). Not surprisingly, it is considered a primary outcome in
research exploring the efficacy of compassion-focused treatments (Kirby & Gilbert,
2017).

Therapeutic alliance, counsellors’ skills, and the parasympathetic system


When people engage in positive social interactions, they unintentionally tend to
synchronize their gestures, vocal pitch, postures, speaking rates, and length of pauses
(Hatfield, 1994). We are now discovering that also other important aspects of their
physiology can become synchronized, shedding new light on the therapeutic relationship
(or alliance) and its role within psychotherapy (Koole & Tschacher, 2016). For example,
Feldman, Greenbaum, and Yirmiya (1999) have shown that during face-to-face interac-
tions, both the mother and her infant unconsciously adapt their heart rhythms, resulting in
a biological synchronization between the accelerations and decelerations of their heart
rates. Importantly, mutual synchrony with the mother at the age of 9 months predicted
self-control abilities at age 2 years, showing how micro-level synchronizations play an
important role in the development of the child’s emotional security, and in particular, the
ability to downregulate emotional distress, also when caregivers are physically absent
(Feldman, 2015).
Links between interpersonal physiological synchrony and emotion regulation remain
crucial in adulthood and are at the core of the therapeutic alliance (TA). If we look at
psychotherapy from an evolutionary perspective, it is evident that the regulatory systems
of social brain (i.e., the different social mentalities) play a key role not only in terms of
developmental history of a patient but also in terms of experience-dependent plasticity
(Cozolino, 2014; Gilbert, 2007). For nearly all patient difficulties, the therapist is asked to
confront the patient’s experience of threat (and lack of safeness). Compassion from the
therapist creates internal conditions of attachment-like processes, such as offering a
secure base (for exploration and challenge), and safe haven for soothing, grounding, and
containing (Holmes, 2014). These can help deactivate threat and self-protective
strategies, and facilitate the process of growth and change (Gilbert, 2010; Wang, 2005).
Given that our minds have evolved to co-regulate each other (Dunbar, 2009), a
therapeutic relationship characterized by compassionate interactions is a core active
therapeutic agent which helps the patient acquire a greater emotion regulation.
This is confirmed by studies on the link between a client’s vagal tone (HRV) and the
forming of a TA during psychotherapy. Doukas, D’Andrea, Doran, and Pole (2014)
investigated the predictors of the working alliance among treatment-seeking women with
complex trauma exposure. Higher alliance ratings were predicted by higher pre-
treatment HRV, even when controlling for pre-therapy symptoms. Moreover, Stratford,
Meara, and Lal (2014) showed that changes in HRV of 30 anxious clients over six sessions
of psychotherapy paralleled changes in levels of TA, measured both with subjectively
(Working Alliance Inventory) and objectively (skin conductance resonance between the
patients and the therapist). Thus, variations in the ANS are an important determinant in
the neurophysiological response of clients during therapy, and they are strongly
associated with the degree of TA over therapeutic sessions. Similarly, Kiema, Rantanen,
Laukka, Siipo, and Soini (2014) have examined the change in HRV of 10 clients during a
counselling session and found that it was correlated with a measure of the level of
10 Nicola Petrocchi and Simone Cheli

counselling skills exhibited by counsellors. Thus, skilled counselling increases parasym-


pathetic activity in the client, which indicates that the stress level has decreased.
However, reduced stress levels were not the result of emotional numbing. In fact, patients
showed more emotional expression during sessions characterized by higher scores in
counselling skills and significant change in HRV than in counselling sessions with lower
scores in counselling skills and a less significant change in HRV. These results are
paralleled by findings of another recent experimental study which compared the impact
of an empathic conversation and a neutral one on the client experiencing depth (inner
contact with the experiencing flow in any given moment) and vagal tone during therapy
sessions. A non-empathetic context produced a progressive withdrawal of vagal activity
and precluded experiencing depth especially in participants expressing a better
interpersonal functioning at baseline.
The regulating effect of the therapeutic relationship, as indexed by increased HRV in
the patient, can also help the therapist implement more behaviourally oriented
approaches. In a controlled multiple case design study, children with severe intellectual
disabilities and severe challenging behaviour underwent therapy sessions with an
‘empathetic’ therapist stimulating therapeutic attachment, alternating with a control
therapist providing personal attention only. Children’s HRV (the physiological marker of
children emotion regulation) was higher when, in the second phase of the experiment,
the warm and compassionate therapist applied behaviour modification than when the
control therapist did.
The experience of safeness is specifically generated by certain social cues (e.g.,
touch, voice tone, facial expressions) from others, and it does not automatically derive
from the absence of threat (Gilbert, 2014). Thus, a compassion-focused therapeutic
relationship inhibits threat-based systems and opens up new cognitive and emotional
processing options. This is particularly relevant also for therapists employing cognitive
interventions. As highlighted by Gilbert (2007), ‘Cognitive behavioural therapy, no
less than any other therapy, is highly invested in trying to ensure that the processes
that facilitate people’s ability to overcome their difficulties (for example, expose
themselves to the feared and develop new ways of thinking) are adopted by patients.
Teachers, coaches, mentors and therapists who engage in their crafts compassionately
may be more likely to form collaborative relationships that increase the chances that
patients will adopt healing practices and walk the sometimes difficult road of change’
(p. 136).

Conclusions
This paper explored how our knowledge of the social brain and its physiological
underpinnings can influence our understanding of the challenges and opportunities for
effective therapeutic intervention. The evidence clearly suggests that the ‘psychotherapy
of the future’ will be based on increasingly well-developed biopsychosocial approaches
with a special focus on the nature and functions of the social brain. The challenge will be
the integration between the different types of scientific knowledge: genetic, evolution,
and physiological processes; the nature of both conscious and unconscious mental
processing; and social, contextual, and ontogenetic/historical approaches (Siegel, this
volume). The days when we can only focus on cognition or only focus on behaviours or
emotions are coming to an end because we are increasingly seeing people’s bodies, brains,
and social relationships as sets of interconnected mutually influencing processes; patterns
The social brain and heart rate variability 11

of dances from the evolved social mentalities that guide individuals in their life tasks, and
that become targets for therapeutic intervention and prevention.

Acknowledgements
The authors would like to express sincere gratitude to Prof. Paul Gilbert for his constant
compassionate encouragement, and for his expert, sincere, and valuable guidance in the
revising and editing of this paper.

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Received 23 February 2019

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