Resonance is the phenomenon of one person
unconsciously mirroring the motor actions as
basis of emotional expressions of another
person. This shared representation serves as a
basis for sharing physiological and emotional
states of others and is an important component
of empathy.
Contagious laughing and contagious yawning
are examples of resonance. In the interpersonal
contact with individuals with schizophrenia we
can often experience impaired empathic
resonance. The aim of this study is to determine
differences in empathic resonance-in terms of
contagion by yawning and laughing-in individuals
with schizophrenia and healthy controls in the
context of psychopathology and social
functioning.
We presented video sequences of yawning,
laughing or neutral faces to 43 schizophrenia
outpatients and 45 sex- and age-matched healthy
controls. Participants were video-taped during
the stimulation and rated regarding contagion by
yawning and laughing. In addition, we assessed
self-rated empathic abilities (Interpersonal
Reactivity Index), psychopathology (Positive and
Negative Syndrome Scale in the schizophrenia
group resp. Schizotypal Personality
Questionnaire in the control group), social
dysfunction (Social Dysfunction Index) and
executive functions (Stroop, Fluency).
Individuals with schizophrenia showed lower
contagion rates for yawning and laughing.
Self-rated empathic concern showed no group
difference and did not correlate with contagion.
Low rate of contagion by laughing correlated
with the schizophrenia negative syndrome and
with social dysfunction.
We conclude that impaired resonance is a
handicap for individuals with schizophrenia in
social life. Blunted observable resonance does
not necessarily reflect reduced subjective
empathic concern.
Introduction
Empathic resonance is the phenomenon of one
person unconsciously mirroring the motor actions
as basis of emotional expressions of another
person. This shared representation serves as a
basis for the ability to share physiological and
emotional states of others and makes up one
component of empathy [19, 22, 42, 61].
Empathy is not a unitary function; it is more
likely based on at least partially dissociable
functional systems which can be divided into
motor empathy, i.e., empathic resonance, a
cognitive and an emotional part of empathy
[4, 12, 13]. The cognitive part of
empathy comprises the ability to understand and
explain mental states of others (known as theory
of mind, ToM), whereas the emotional part of
empathy includes the own experience of the other
person's actual or inferred emotional state.
Resonance can be seen as a bottom-up input for
the emotional and cognitive part of empathy and
is mediated by shared representations in the
mirror neuron system (MNS) and frontoparietal
networks [14, 18, 26, 34, 47, 61]. This
so-called perception-action link has also been
referred to as "chameleon effect" [8,
42]: an unconscious mimicry of the postures,
facial expressions, and other behaviors of one's
interaction partners, such that one's behavior
passively and unintentionally changes to match
that of others in one's current social
environment. It constitutes a basic way of
getting in contact with another person.
This basic way of establishing contact can
be impaired. When these subtle alterations in
communication are experienced during contact
with an individual suffering from schizophrenia,
they subsequently lead to an intuitive diagnosis
of schizophrenia. The Dutch psychiatrist
Henricus Cornelis Rumke first mentioned this
phenomenon in the literature in 1941. He used
the term "praecox feeling" to describe "the
inability to come in contact as a whole" with a
person who suffers from schizophrenia
[50]. We assume that this phenomenon is
based on reduced resonance. This intuitive
reasoning based on subliminal information is
still used today by some psychiatrists in daily
practice in addition to standardized diagnostic
classification [21]. Impaired empathy
has recently been assumed to be involved in
schizophrenia [2, 19, 51, 54]. Long
before, Karl Jaspers stated that a failure of
empathy and understanding are common elements in
diagnosing schizophrenia [23]. The
"inability to come into contact as a whole" can
indeed be a diagnostic tool for psychiatrists
but is most notably a handicap for affected
individuals in interpersonal communication in
everyday life. Reduced resonance forms a barrier
for interpersonal contacts and adequate social
functioning [56] and has stigmatizing
potential [17]. The hypothetical
assumption of deficits in resonance as basis of
the "praecox feeling" puts the specificity of
the sign in question with respect to other
diagnoses with altered social reciprocity such
as schizotypal personality disorder or high
functioning autism.
Contagious yawning (cY) and contagious
laughing (cL) are easily observable signs of
resonance as an interaction between two
individuals, with one person experiencing and
sharing the physiological and emotional state of
the other. The implicit link between two persons
in cY has been discussed in the literature as a
sign reflecting the motor mimicry component of
human empathy [33, 40, 41, 43, 53]
and
as evidence of empathic abilities in
chimpanzees [1], and dogs [24].
Platek et al. [40] showed a correlation
between higher scores on the Schizotypal
Personality Questionnaire (SPQ) and lower rates
of cY in a sample of undergraduate students.
Recently, impairment in cY in children with
autism spectrum disorder was reported by Senju
et al. [55]. To the best of our
knowledge, no study has examined cY and cL in
individuals suffering from schizophrenia so far.
We hypothesize that (1) cY and cL are impaired
in individuals suffering from schizophrenia
compared to healthy controls. Furthermore, we
hypothesize that (2) a reduced ability to
resonate-measured in terms of contagion-is
associated with severe psychopathology and
impaired social functioning in individuals with
schizophrenia.
To test our hypotheses, we assessed two
observable measures of empathic resonance (cY
and cL) and one selfassessment measure of
empathy (Interpersonal Reactivity Index, IRI) in
individuals with schizophrenia and healthy
controls. In both groups, we compared the
ability to resonate with their psychopathology
[i.e. with the Positive and Negative
Syndrome Scale (PANSS) in individuals with
schizophrenia, and with the SPQ in healthy
controls]. In the schizophrenia group, we
additionally compared the measures of resonance
and the self-reported empathic abilities with
the Social Dysfunction Index (SDI).
Discussion
We compared the ability to resonate
(observable contagion and self-report) in
individuals with schizophrenia with healthy
controls in the context of psychopathology and
social functioning. We hypothesized a lack of cL
and cY in the schizophrenia group and an
association between the lack of contagion and
impairments in social functioning.
Group differences in
contagion
Our first hypothesis was confirmed by the
main finding in our study: the significant
reduction of cL and cY in the schizophrenia
group compared with healthy controls. The mean
incidence rate of cY in our control group
(38.3%) matches the 41.5% reported by Platek et
al. [40].
The impaired contagion as a sign of empathic
resonance in the schizophrenia group can be
explained by different influences, in particular
by psychomotor constrictions due to illness or
medication. We may state, that we found no
significant correlation of medication dosage (in
CPZe) and contagion. Executive cognitive
functions were as expected impaired in the
schizophrenia group but did not correlate with
contagion. The analysis of stimulus-incongruent
laughing and yawning (siL, siY) allows an
inference on the overall psychomotor activity of
the participants. The group difference with less
response in the schizophrenia group is seen in
siL but not in siY. A negative influence of
general illness related factors such as negative
symptoms or medication (in CPZe) is also seen in
siL but not in siY. Furthermore in the
schizophrenia group, siL correlates
significantly with the intended contagion
(cL).
This means that the recorded laughing in the
schizophrenia group was not specific to the
phenomenon of contagion but might reflect the
general level of unspecific social
responsiveness, psychomotor activity, or
attention. In contrast, siY-as a general
disposition to yawn-correlated not with cY, and
showed no influence of psychopathology or
medication. We see this as an indicator of a
higher specificity of the more basal yawning
stimulus. The situation is inverted in the
control group. Here, cL is not the continuation
of the high level social responsiveness
reflected by siL, but is distinct by the
specific stimulation. Our interpretation is that
in the control group, the (preexisting high)
laughing response is highly modulated by the
external stimulation. We assume that this effect
is not only due to contagion but also other
(possibly social-cognitive) factors which are
more pronounced in the control than in the
schizophrenia group. One possible explanation
for the unspecific yawning response in the
control group (i.e. high correlation between siY
and cY) could be a gating effect: a
reinforcement of the automatic process of
contagion by repetitive stimulation. The initial
lower level of contagiousness may hamper this
gating mechanism in the schizophrenia
group.
Furthermore, one might discuss if
individuals with schizophrenia feel more
uncomfortable in the test situation, thus
reducing their ability to resonate. However, our
analysis of the distractor task data showed that
there was no significant difference between the
two groups in their judgment how comfortable and
likeable the stimulation was.
Psychopathology and social
functioning
Due to the homogenous low scoring of our
control group on the SPQ (compared to the
original population described by Raine
[45], the variance was too low to answer
our question about association of reduced
contagion with schizotypal symptoms in the
control group. The lack of contagion in the
schizophrenia group responds to the clinical
impression of the illness, and is reflected in
the negative correlation of cL with the PANSS
negative scale. However, the overall PANSS
scores of our sample were rather low,
corresponding to full or partial remission,
thus, restricting our conclusion to less severe
psychopathological states. As stated above, cY
seems to detect variances (partly) independent
of obvious psychopathology and points towards an
underlying phenomenon, whose embedding in the
common concepts of empathy has further to be
discovered. It has further to be studied, how
impairments of cY are related to an experienced
psychiatrist's praecox feeling.
To the best of our knowledge, this is the
first empirical evidence about the contribution
of empathic resonance on social functioning in
schizophrenia. Other empathic abilities such as
the ToM (part of the cognitive part of empathy)
have already been studied and are known to be
impaired in schizophrenia and to contribute to
the variance of social functioning [5, 7,
35, 48]. The negative correlation of cL with
the SDI gives some support to our second
hypothesis. However, we see this correlation
only in one stimulus condition and it is of low
significance. The correlation is based on
clearly significant correlations of cL and cY
with only one domain: dysfunction in "Family
relationships". A lack of contagion in
individuals with schizophrenia seems to occur
mainly in close social contacts within the
family circle. Social networks of individuals
with schizophrenia consist largely of
unidirectional therapeutic relationships. By
contrast, family members have their own
interpersonal needs and desires in face of their
impaired relative. This may make this domain
especially vulnerable to interpersonal
challenges [31, 37]. However, an
interpersonal handicap due to impairments in
resonance leaves room to be coped/for
rehabilitation in many domains of social
life.
Self-report
The observable signs cY and cL are perceived
in daily contact as nonverbal statements in
social interaction. The absence of these signs
leads us to make psychopathological
interpretations about the affective state of the
observed individual, and it may lead us to
speculate about a deficient perception of
social-emotional information. The interpretation
of self-report measures in individuals with
schizophrenia is limited, since deficits in ToM
may affect the representation of own mental
states [16]. Nevertheless, it is the
most direct way to understand the subjective
experience of an affected individual.
The TRI was already used for individuals
with schizophrenia in a recent study by Montag
et al. [36]. The results of our study
replicate the group differences reported by
Montag et al.: individuals with schizophrenia
reported less perspective taking and more
personal distress in response to difficult
situations of others compared to healthy
controls. No group difference was found on the
Fantasy scale, in measuring the ability to
fantasize about fictional characters and in
empathic concern.
The reduced subjective perspective taking
ability is in line with objective findings on
ToM deficits reported in the literature [6,
16, 58] and evidence of a certain insight
into social cognitive deficits. Unimpaired
empathic concern combined with increased
personal distress suggests that the perception
of social-emotional content may be intact but
cannot be processed adequately, suggesting a
problem of the output and not predominantly of
the input. This view was already expressed by
Kring et al. [29, 30] and supported by
facial emotional EMG findings. A core process
involved in the handling of social-emotional
information is the distinction between self and
other. This function is known to be impaired in
schizophrenia [9, 11, 20, 60]. On the
one hand this can lead to a dysfunction of
action attribution, contributing to positive
symptoms such as verbal hallucinations or
delusions of control [15, 27, 52, 62].
On the other hand, it can lead to difficulties
in attributing shared representations, e.g.,
social-emotional information, which can produce
self-oriented responses such as personal
distress to difficult situations of others
[32]. The positive correlation between
the "personal distress" scale and the PANSS
negative scale indicates the stressful component
of a clinically blunted affect.
The comparison of the observed contagion
with the selfreport in our sample revealed only
a minor association: only one of the four
subscales of the TRI, the Fantasy scale, showed
a significant correlation with contagion on the
behavioral level. Particularly the two scales
Empathic concern and Personal distress, that one
could expect to be the most influenced by motor
empathy regarding contagion, showed no
correlation. The absence of this correlation in
both groups suggests its being a general
dissociation between behavioral and experiential
response, rather than an expression of
illness-related lack of insight.
Clinical implications
The observation of the ability to resonate
is implicitly part of each clinical examination.
It may even serve as an intuitive diagnostic
instrument for schizophrenia, and is possibly
related to the so-called "praecox feeling"
[50]. This intuitive notice is more
subtle than the clinical identification of
negative symptoms. To what extent our low
contagion data resemble a clinician's praecox
feeling has yet to be determined. Rumke, who
first described this clinical phenomenon
[50], already mentioned the problem of
subjectivity when considering the "praecox
feeling". An "objective" measurement of
resonance using defined and invariant contagious
stimuli (e.g. video sequences) allows
controlling for (counter-) transference in
personal contact-not in the Freudian sense, but
in the sense of mutual resonance.
Limitations and suggestions for
further research
We cannot discuss depressive numbness as
reason for impaired resonance in consequence of
lacking clinical rating for depression.
Likewise, subjective tiredness as reason for
facilitated cY was not assessed and limits the
interpretation of the data.
Since this is a cross-sectional examination,
we cannot predict if the so measured resonance
is a state or a trait. Regarding the lack of
Resonance in the (at least partial) remission
state of our sample, reflected in low PANSS
scores, we could speculate that this impairment
is not statedependent. A retesting or
longitudinal study is needed to evaluate
contagion over time and in various
psychopathological states.
We are aware of the problem of multiple
testing. As this is the first study of this
kind, we decided not to raise the significance
level, as not to exclude potential
interpretations for future research.
Our explanations of the differences between
cY and cL are only speculative. We used these
two phenomena in our study presuming a common
basis. Up to now, we can only hypothesize about
top down cognitive influences that make laughing
more contagious and yawning a purer resonance
stimulus. The examination of the two stimulation
conditions together with social-/cognitive
parameters could provide further information
about their differences. The combination of
contagion response with a broader spectrum of
other empathy-related functions (e.g. ToM,
selfother distinction, emotional tasks) stimuli
is needed to integrate these easily observable
signs in the diverse conceptions of
empathy.
Our paradigm could be used to further
investigate the role of the MNS in schizophrenia
[2, 19, 51]. Furthermore, imaging
studies could reveal differences in the neural
substrates of cY and cL.
On the level of clinical use, a cY test with
higher resolution in the lower range could
reveal further insight into the group of most
impaired individuals.