ArticlePDF Available

Abstract

It has been suggested that " sharing the same body " between the observer and the observed subject allows for a direct form of understanding and emotional attuning by a process of simulation. Then, what happens when we don't share the same body? The aim of the present paper is to review available evidence of intra-and inter-species empathic and prosocial behaviours, with respect to within-human, within-animals and cross-specifies interactions. Similarities and differences will be evaluated using a comparative perspective, and some possible moral and ethical implications for human-animal interactions will be discussed. According to Charles Darwin's work, the perceived differences between human and animal empathy could be more quantitative than qualitative, suggesting a common affective core which allows both categories to mirror and tune to conspecifics' feelings, where in the case of humans it can be integrated with more complex cognitive processes.
RIVISTA INTERNAZIONALE DI FILOSOFIA E PSICOLOGIA
DOI: 10.4453/rifp.2015.0007
ISSN 2039-4667; E-ISSN 2239-2629
Vol. 6 (2015), n. 1, pp. 88-109
1 Unità di Ricerca in Neuroscienze Sociali e delle Emozioni, Università Cattolica del Sacro Cuore
di Milano, Largo A. Gemelli, 1 - 20123 Milano (I)
M.E. Vanutelli: mariaelide.vanutelli@unicatt.it (
); M. Balconi: michela.balconi@unicatt.it ()
M. Balconi - Facoltà di Psicologia, Università Cattolica del Sacro Cuore di Milano, L.go A. Gemelli,
Empathy and Prosocial Behaviours.
Insights from Intra- and Inter-species Interactions
Maria Elide Vanutelli1 & Michela Balconi1
Ricevuto: 21 novembre 2014; accettato: 4 febbraio 2015
Abstract It has been suggested that “sharing the same body” between the observer and the observed
subject allows for a direct form of understanding and emotional attuning by a process of simulation.
Then, what happens when we don’t share the same body? The aim of the present paper is to review avail-
able evidence of intra- and inter-species empathic and prosocial behaviours, with respect to within-
human, within-animals and cross-specifies interactions. Similarities and differences will be evaluated us-
ing a comparative perspective, and some possible moral and ethical implications for human-animal inter-
actions will be discussed. According to Charles Darwin’s work, the perceived differences between human
and animal empathy could be more quantitative than qualitative, suggesting a common affective core
which allows both categories to mirror and tune to conspecifics’ feelings, where in the case of humans it
can be integrated with more complex cognitive processes.
KEYWORDS: Empathy; Emotion; Prosocial Behaviours; Intra- and Inter-species Interaction.
Riassunto Empatia e comportamenti prosociali. Evidenze dalle interazioni intra- e interspecie Si è ipo-
tizzato che la “condivisione di correlati corporeitra soggetto osservante e soggetto osservato permetta
una forma diretta di comprensione e sintonizzazione emotiva mediante un processo di simulazione. E
quindi, che cosa accade quando non condividiamo lo stesso corpo? Scopo di questo lavoro è fornire una
rassegna delle evidenze disponibili circa i comportamenti empatici e prosociali intra- e inter-specie, in re-
lazione alle interazioni tra umani, tra animali e inter-specie. Similarità e differenze saranno valutate se-
condo un’ottica comparativa e verranno discusse alcune possibili implicazioni morali ed etiche sul piano
delle interazioni tra umani e animali. Secondo quanto suggerito da Charles Darwin, le differenze percepite
tra l’empatia umana e quella animale potrebbe essere più di tipo quantitativo che qualitativo, deponendo
a favore di un comune nucleo affettivo che permetterebbe a entrambe le categorie di riflettersi e sintoniz-
zarsi con i sentimenti dei propri conspecifici, dove, nel caso degli umani, questo nucleo potrebbe essere
integrato con processi cognitivi più complessi.
PAROLE CHIAVE: Empatia; Emozione; Comportamenti prosociali; Interazioni intra- e inter-specie.
Introduction
EMPATHY IS A FUNDAMENTAL MOTIVA-
TION for prosocial behavior and knowledge
of the processes underlying this capacity is
crucial to understanding why and how we
engage in prosocial behaviours.
1
The ability
to perceive and understand others’ mental
Ricerche
Creative Commons - Attribuzione- 4.0 Internazionale
Empathy and Prosocial Behaviours
89
states and moods is critical to reinforcing and
maintaining our social bonds. Thus, empathy
and altruism are most commonly considered
forms of compassion that human beings ex-
press toward one another. What is not clear,
however, is the extent to which non-human
animals can feel empathy.
Although researchers on human empathy
have recently published many new articles,
the current interest in the topic draws on a
line of animal research that began almost half
a century ago, while human studies began
first in the 1970s with young children and
continued, in the 1980s, with adults. Finally,
since the 1990s, researchers began placing
humans in brain scanners to monitor them
while viewing pictures or videos depicting
others in pain or distress, to find out about
the neural correlates of empathy and com-
passion.
2
Ethologists and sociobiologists have
identified many behaviors within other spe-
cies that may be viewed as prosocial or altru-
istic, as well as behaviors reflecting apparent
concern for others, even if a possible compar-
ison between human and animal empathy
still needs to be elucidated.
Research suggests that we more readily
empathize with those to whom we feel closer
and more similar. In fact, there is less evi-
dence of altruism across species, even if be-
haviors reflecting apparent concern for oth-
ers seem to occur between different species
as well. For example, animal owners some-
times report that their pets show emotional
concern for others. The recent spate of re-
search on animal assisted therapy attests to
the capacity of animals to provide comfort to
persons suffering from a variety of physical
and emotional problems.
In intra-human studies several factors that
can increase the perception of similarity, and
consequently empathy, have been investigated,
with cultural similarity, sentience or social cir-
cumstance being the most influential.
3
The
perception of similarity has also been thought
to underlie empathic behaviors towards ani-
mals: it has been theorized by many philoso-
phers that the amount of empathy shown to-
wards animals may indicate a more general ca-
pacity for empathy and related prosocial be-
haviors.
4
Furthermore, the link between hu-
man-human and human-animal relationships is
being given increasing attention by empirical
research and suggests that the lack of empathy
demonstrated by some individuals is a general
deficit not simply restricted to its expression
towards other human beings.
5
Preliminary self-
report empathy research currently supports a
relationship between human- and animal-
orientated empathy.
6
However, there is a need
for improved objectivity in these measures.
Therefore, the aim of the present paper is
to discuss empathic and prosocial behaviors
in human studies, taking into account the
main behaviors which can be considered as
explicit markers of empathic attitudes. A se-
cond major intent is to systematically review
the available literature on empathic-like be-
haviours in non-human animals, with partic-
ular attention to resonance mechanisms, af-
filiative behaviours and pain sharing. Then,
possible insights on cross-species empathy
will be furnished with respect to both hu-
mans’ and animals’ attitudes. Finally, some
moral and ethical implications about human-
animal relationship will be considered.
Intra-species interactions: Empathy with-
in humans
Empathy is an aspect of social cognition
that concerns our interactions with the people
around us. Indeed humans perceive and rep-
resent themselves in a very different and spe-
cific way in respect to non-human objects and
events. Despite the diverse terminology used
by different authors, there is wide agreement
that empathy involves three primary ele-
ments: the cognitive ability to adopt the per-
spective of another person, the presence of
monitoring and self regulatory mechanisms
that keep track of the origins of own and oth-
er emotions, and the affective response to an-
other person’s emotional state, that often en-
tails the capacity to share this state.
7
These aspects may be experienced inde-
Vanutelli & Balconi
90
pendently from one another, and may be ex-
pressed at different levels of complexity with-
in the empathic experience, from mimicry to
sympathy. Affective components include the
ability to monitor and regulate own and oth-
er’s emotional processes
8
and coincide with
the ability to share and imitate them.
A basic resonance mechanism is thought
to lie underneath the emotional empathic re-
sponse and includes: the capacity to know
what the other person is feeling, by monitor-
ing external cues such as emotional facial ex-
pressions; to have the intention to respond
compassionately to another person’s distress;
to mimic what another person is feeling by
responding with similar emotional behavior.
9
These aspects together with their functional
relevance and their neural substrates have
been extensively illustrated by simulation
10
and emotional contagion
11
theories. Interest-
ingly, unlike other components that require
intentional processing, such as cognitive per-
spective-taking and, in part, emotion regula-
tion, these phenomena can occur automati-
cally and without awareness.
12
In this light, empathy seems related to the
ability to comprehend emotions and feelings
of others, where resonance mechanisms per-
mit a direct form of understanding between
the observer and the observed. But how can
we understand and learn about these feelings?
It has been observed that the perceptual
ability to attend to socially relevant stimuli,
including facial expressions of emotions, is a
central mechanism, together with motiva-
tional and attentional components.
13
This
ability allows us to acquire information about
the intentions and future actions of others, to
support effective social communication and
to develop the motivation for prosocial and
cooperative behaviour.
14
Empathy and the detection of emotional
cues
Consistent evidence suggests a close rela-
tionship between the experience of emotion-
al empathy and the ability to recognize emo-
tions from facial expressions.
15
Previous stud-
ies demonstrated that the degree of emotion-
al empathy was linked to sensitivity to facial
expressions.
16
In a recent study
17
Balconi and
Bortolotti found trait empathy affected the
degree of subjective responsiveness to facial
cues, where subjects with higher empathy
scorings were also more accurate in respond-
ing to emotional faces. Moreover, viewing
another’s emotional expression automatically
triggers that emotion in oneself, and elicits
unintentional mimicry of that expression.
18
Current findings involving people with dis-
orders of emotional experience, such as au-
tism, schizophrenia and major depressive
disorder, assume that these populations may
have abnormal psychophysiological respons-
es to emotional cues and anomalous empath-
ic behaviours.
19
Thus, different degrees of empathic expe-
riences may also affect psychophysiological
responses:
20
facial muscle reactions are
thought to be related to emotional responses
and their electrical activity is thought to be
related to emotional empathy. Previous stud-
ies demonstrated that individuals with a
greater autonomic tendency to reciprocate
facial expressions score higher on an empa-
thy questionnaire.
21
Interestingly, Balconi
proved that facial expression detection and
autonomic mimicry reaction to emotional
faces (measured by electromyography; EMG)
are strictly related.
22
Empathy-related brain networks
These mechanisms are supported by cog-
nitive and emotive competences and could be
based on specific neural networks.
23
Neu-
roimaging studies on emotion have revealed
a very wide range of areas activated in re-
sponse to emotional cues, specifically the
medial prefrontal cortex (MPFC) for general
emotional processing,
24
the dorsolateral pre-
frontal cortex (DLPFC) for decisions and
supportive behaviours
25
and the sensorimo-
tor cortex
26
when a subject simulates per-
ceived emotions.
Empathy and Prosocial Behaviours
91
The MPFC has been shown to be in-
volved in empathic responsiveness and regu-
lation of facial recognition in response to an
emotional task.
27
Studies on clinical popula-
tions, such as schizophrenic subjects, have re-
vealed a significant relationship between the
impairment of comprehension of emotional
cues, empathic behavior, and structural ab-
normalities of this area.
28
It has been recently demonstrated by Bal-
coni and colleagues
29
that the ability to recog-
nise facial expressions of emotion and facial
mimicry are modulated by prefrontal func-
tioning: in fact, the use of the TMS technique
allowed researchers to prove its relevance in
empathic mechanisms by temporally inhibit
MPFC. Participants were required to empa-
thise with the situation by entering into the
picture’s feelings: the four emotions portrayed
were anger, fear, happiness, and neutral. Re-
sults showed an impaired performance on
both facial expression recognition and mimic-
ry when TMS stimulation resulting in inhibi-
tion of the MPFC was carried out.
Besides MPFC, the contribution of DLPFC
has also proved crucial for empathic responses,
with respect to prosocial behaviors: electro-
physiological studies, in fact, have shown the
presence of a clear ERP marker, the N200 ef-
fect, correlated with a predisposition to inter-
vene, support and help other people, with a
main cortical localization within the frontal
sites.
30
Moreover, it has been recently found
that excitatory rTMS stimulation on DLPFC
can induce a facilitatory effect on engagement
in prosocial behaviours.
31
Finally, sensorimotor cortices has been
implicated in empathic behaviors: simulation
models of emotion recognition, in fact, sug-
gest that understanding another’s emotions
requires that individuals map the observed
state onto their own representations.
32
Ac-
cording to theories of embodied cognition, in
fact, visual mechanisms alone are insufficient
to elicit simulating responses associated with
the observed emotion.
33
On the other hand,
there is growing evidence that sensorimotor
activity plays a crucial role in facial emotion
recognition by linking emotion perception
with representations of somatic states previ-
ously engendered by emotions.
34
In fact, the ability to monitor emotional
cues and behavioral empathic responsiveness
was shown to be partially compromised in the
case of frontal activity disruption, highlighting
the central role of the sensorimotor system in
empathic social skills. These findings demon-
strate that regions in the sensorimotor circuits
guarantee a correspondence between emo-
tional recognition and the ability to provide
an empathic response, by allowing the simula-
tion of that emotional behavior with recourse
to previous somatic states.
Thus, the abovementioned evidence may
suggest the existence of inter-individual differ-
ences in emphatic cerebral activations.
35
These
differences in neural activity appear to corre-
late with measures of behavioral trait empathy
assessed behaviorally through questionnaires.
Interestingly an increase in autonomic respon-
siveness recorded through Heart Rate (HR)
measure and Skin Conductance Response
(SCR) was also observed as a function of em-
pathic measures, with high empathic subjects
being more responsive to empathy-related situ-
ations than low empathic subjects.
36
Thus, au-
tonomic measures could be interpreted as a
functional mechanism for mirroring and un-
derstanding the emotional conditions displayed
by other people, while sharing similar emotion-
al and somatic responses.
37
Intra-species interactions: Empathy with-
in animals
Empathy is a social phenomenon that has
for decades attracted the interest of philoso-
phers and psychologists and, more recently
of neuroscientists and evolutionary biolo-
gists. Non-human empathy, in fact, is receiv-
ing growing attention, even if the presence of
observable examples of emotional contagion
in animals has only been mentioned in the
literature, while objective experimental evi-
dence is beginning to emerge.
38
Moreover, the influential paper of Preston
Vanutelli & Balconi
92
and de Waal published in 2002
39
contributed
to empathy being considered as a phylogenet-
ically continuous ability, ranging across ani-
mals with more basic and automatic reactions
in response to the emotions of others, to per-
spective-taking. The authors, in fact, pro-
posed a sequence of progressively complex
levels of empathy across animals that parallels
the development of empathy in humans. Evi-
dence in this field suggests that empathic and
sympathetic concern may even have emerged
on a pre-human basis, in that some species,
especially primates, show consolation-like and
prosocial behaviours.
40
Social species like hu-
mans and primates need to regulate group in-
teractions between members to coordinate
travel, communicate about danger, assist
group mates in need and facilitate cohesion
and emotional balance, so that the capacity to
interpret behavioral signals and react to the
emotional state of the other seems favorable.
41
These mechanisms have been described
with reference to the social brain hypothesis,
which states that primates with bigger neo-
cortices are better able to catch social sig-
nals.
42
However, growing evidence is suggest-
ing the presence of empathy-related respons-
es also in other mammals and birds, despite
the absence of a large neocortex; this fact
raises the hypothesis that other mechanisms
are involved in sharing the affective state of a
conspecific.
43
Nevertheless, whereas human
pro-social behavior is often driven by em-
pathic concern for another, it is unclear
whether other animals can experience a simi-
lar motivational state.
Despite the difficulty of establishing the ca-
pacity for empathy in animals, recent evidence
suggests that many species are sensitive to suf-
fering in others. A possible definition of empa-
thy with respect to non-human animals can be
described as a situation in which an animal per-
ceives a reciprocal state of feeling in another
animal and identifies with its concerns. In this
context, empathy can be recognized when an
animal seems to be sympathizing with another
animal’s mental state, and can be seen in help-
ing or prosocial situations.
44
The advantageous role of empathy is sus-
tained in a theoretical model described by Pres-
ton and de Waal
45
which proposed that empa-
thy is linked to all facilitation behaviors relying
on perception-action, including imitation, co-
ordination and unconscious mimicry. Accord-
ing to the Perception-Action model (PAM), the
observation of another’s emotional states au-
tomatically and unconsciously activates neural
representations of congruent states in the ob-
server. The more similar and socially close two
individuals are, the easier the tuning with the
partner.
46
This consideration explains why, in
this context, empathy is considered essential
for directional cooperation in achieving a
shared goal and in some social interactions.
47
The evolution of empathy is thought to
go back to mammalian maternal care.
Whether a human or a rat, a mother must be
in tune with behavioral indicators of hunger,
danger, or discomfort in her offspring. Sensi-
tivity to emotional signals confers clear adap-
tive value also to the dyad as well as the
group of conspecifics; this fact would explain
observed sex differences (see herein for de-
tails).
48
As previously discussed current evo-
lutionary evidence suggests that empathy is a
multilayered phenomenon with different in-
termediate forms, ranging from motor mir-
roring and mere agitation at the distress of
others to complex forms of perspective tak-
ing.
49
While subtle, complex and cognitive
forms of empathy exist, any empathic pro-
cess relies to some extent on personal distress
and emotional contagion.
50
Despite the arguments against the pres-
ence of empathy in non-human animals,
51
there is growing evidence for the presence of
behaviours which appear to be driven by em-
pathy in the context of contagious yawning
(CY), affiliative behaviours towards dis-
tressed individuals, and modulation of pain
sensitivity. In the following paragraphs these
contexts will be exhaustively discussed.
Contagious yawning
Contagious Yawning (CY) is a useful can-
Empathy and Prosocial Behaviours
93
didate behaviour to explore basic forms of
empathy across species and different types of
social systems. In fact, it is present in both
humans and non-human animals and it
seems related to empathy and affective tun-
ing.
52
In fact, describing the phenomenon of
contagious yawning (CY) first in humans, with-
in a comparative perspective, the susceptibility
to contagion has been theoretically and empiri-
cally related to our capacity for empathy: yawn-
ing when seeing other people yawn is associat-
ed with activations in neural networks related
to action simulation, social behavior and empa-
thy,
53
such as the ventromedial prefrontal cor-
tex
54
and the mirror neuron system,
55
though its
role in yawn contagion remains unclear.
Moreover, CY has been reported to occur
more frequently in individuals with higher
scores on questionnaires evaluating empa-
thy
56
and less in clinical populations charac-
terized by impaired empathic abilities, like
autistic and schizotypic patients.
57
Addition-
ally, it has been demonstrated recently that
the social-emotional bond between individu-
als influences the occurrence, frequency, and
latency of yawn contagion. Cross-cultural ob-
servations in humans have shown the CY ef-
fect to be stronger in response to the yawns
of kin, then friends, then acquaintances, and
lastly strangers.
58
Thus, although contagious
yawning is not an emotional reaction itself,
its occurrence has been clinically, psychologi-
cally, neurobiologically, and behaviorally
linked to our capacity for empathy.
59
Different theories have tried to explain
the possible functions of yawning:
60
commu-
nication theories propose yawning as a way
to synchronize group behaviors or communi-
cate tiredness or stress. Arousal theories pro-
pose, instead, that yawning should help sub-
jects maintain their attention levels and pro-
mote maintenance of vigilance and shared
attention.
61
Because of its relevance to evolu-
tionary biology and its evident expression,
this phenomenon has been the focus of re-
cent investigations in non-human species:
62
in fact, humans are not the only species af-
fected by contagious yawning. Chimpanzees,
bonobos,
63
gelada baboons
64
and domestic
dogs,
65
have been reported to yawn in rela-
tion to a conspecific yawning. In contrast, no
CY has been demonstrated in tortoises,
66
a
solitary species, lending some empirical sup-
port to the notion that CY serves to coordi-
nate and synchronize group behaviour.
67
Palagi and colleagues in a study with gela-
da baboons found that contagious yawning
seems unrelated to external stressful events
and that it is more frequent between socially
close individuals. Moreover they demonstrat-
ed CY to be more common between individu-
als with higher levels of affiliation, thus sug-
gesting that the roots of empathy may be pre-
sent in non-human primates. Moreover, yawn
contagion was present only in adults.
This is particularly interesting in that also
humans show a developmental increase in sus-
ceptibility to yawn contagion, with children
displaying a substantial increase at the age of
four, together with the development of related
cognitive abilities such as the identification of
others’ emotions.
68
Finally, adult females
showed an additional feature, that is the capa-
bility to match the type of yawn. These findings
fit the empathy-based hypothesis of contagious
yawning since similarity, familiarity, and close-
ness are known to facilitate empathy.
69
Although empathic abilities outside the
human domain were previously thought to
be present only in primates and animals with
a large neocortex, some new evidence sug-
gests that simpler forms exist in other animal
species. Romero and colleagues
70
using a
highly standardized observational approach
under naturalistic settings found that yawn-
ing is contagious in wolves and that, accord-
ing to the empathy-based hypothesis, the
susceptibility to yawn contagion is biased
toward close social partners.
The importance of this study relies in the
fact that it is the first to demonstrate intraspe-
cies contagious yawning in a carnivore species,
suggesting that this ability might be deeply
rooted in the Mammalia class for within-
species social communication, which can be
transferred to animal-human interactions (see
Vanutelli & Balconi
94
below). Again, sex differences were observed,
with female wolves responding quicker than
males when the initial yawner was a close asso-
ciate, suggesting a higher ability for female
wolves to react to the emotional stimulus.
Affiliative behaviors
Following the discovery that chimpanzees
often kiss and embrace shortly after a fight
within the group,
71
numerous studies have
documented reconciliation-like behaviours
in non-human primates. Specific methodolo-
gies allow comparing post-conflict observa-
tions with baseline behaviours to determine
how species members behave before and af-
ter antagonism. Such comparisons show that
primates are generally attracted to previous
opponents, seeking friendly contact. This
kind of consolation reduces the recipient’s
arousal and follows the same sex difference
reported in humans, with female apes
providing comfort more often than males.
72
In research conducted on empathy be-
tween chimpanzees
73
O’Connell found that
these animals show empathy of varying types
and levels, and across a wide spectrum of sit-
uations. Of particular interest is understand-
ing the perspective of another individual to
support it and even rescue it from life-
threatening circumstances, suggesting the
possession of second order intentionality.
Studying titi monkeys, Clyvia and col-
leagues
74
reported an intriguing finding about
the presence of empathetic responses to-
wards an individual of a different group.
Thus, if empathy is more likely to occur
when there is social proximity between indi-
viduals, it does not mean that unrelated indi-
viduals do not have the perception of mental
and emotional states of other individuals.
As already stated, empathy is thought to
be unique to higher primates; nevertheless
Bates and colleagues
75
described elephants as
showing a rich social organization and dis-
playing a number of behaviours that have the
potential to reveal signs of empathic under-
standing, such as coalition formation, the of-
fering of protection and comfort to others,
retrieving and “babysitting” calves, aiding
individuals that would otherwise have diffi-
culty in moving, and removing foreign ob-
jects attached to others. These capabilities
demonstrate that elephants can diagnose
animacy and goal directedness, and under-
stand the physical competence, emotional
state and intentions of others, even if they
differ from their own.
Also, Ben-Ami Bartal and colleagues
76
tested empathically motivated pro-social be-
havior in rats, positioning a free individual
besides a cagemate trapped in a restrainer.
After several attempts, the free rat learned to
intentionally and quickly open the restrainer
and free the cagemate, in response to its con-
specific’s distress, thus providing strong evi-
dence for the biological roots of empathically
motivated helping behaviour. More interest-
ingly, when liberating a cagemate was pitted
against chocolate contained within a second
restrainer, rats opened both restrainers and
typically shared the chocolate; they also freed
cagemates when social contact was prevented,
while they did not open empty or object-
containing restrainers. This study proves that
rats can behave pro-socially when they per-
ceive a conspecific experiencing nonpainful
psychological restraint stress, acting to end
that distress through deliberate action, in the
absence of training or social reward, and even
when in competition with highly desired food.
Modulation of pain sensitivity
In a paper by Russell Church entitled
Emotional Reactions of rats to the Pain of Oth-
ers,
77
he describes that, after training a rat to
obtain food by pressing a lever, if it saw an-
other rat in a neighboring cage receiving a
shock from an electrified cage floor, the first
rat would interrupt its activity. The bigger
question is whether the rat was worried
about their companions or just afraid that
something bad might happen to it, as well.
Nearly fifty year later, Langford and col-
leagues
78
reported the modulation of pain
Empathy and Prosocial Behaviours
95
sensitivity in mice produced by exposure to
their cagemates in pain. Pairs of mice were
placed in two transparent Plexiglas cylinders,
so that they could see each other, and were
injected with acetic acid, which is known to
cause a mild stomachache and characteristic
stretching movements. The researchers
found that an injected mouse showed in-
creased pain behaviors if its partner dis-
played the same behaviour, especially for
mouse pairs who were cage mates.
Moreover, when familiar mice were given
noxious stimuli of different intensities, their
pain behavior was influenced by their neigh-
bor’s status bidirectionally. Overlooking the
huge ethical implications that such studies
should raise, this research showed that rodents
can recognize and show emotional reactions
to the pain of conspecifics, and that their pain
sensitivity can be altered by social factors.
Inter-species interactions: Can animals
feel empathy for humans?
Contagious yawning and affiliative behav-
iors
Most studies on yawn contagion in non-
human animals have demonstrated the intra-
specific effect of yawn contagion. However,
studies on primates and dogs have also been
able to demonstrate cross-species contagious
yawning. Madsen and colleagues
79
examined
whether emotional closeness affected the
strength of contagion in orphaned chimpan-
zees observing unfamiliar and familiar hu-
mans, demonstrating the existence of cross-
species contagious yawning. Specifically,
viewing a human yawn elicited yawning in 48
per cent of juvenile chimpanzees, while in-
fants were immune to contagion. In fact, like
humans and dogs,
80
chimpanzees are subject
to a developmental increase in susceptibility
to yawn contagion.
Following recent studies suggesting that
contagion yawning in humans, and some oth-
er primates, is empathy-related, some authors
have considered the possibility that the same
mechanism may underlie contagious yawning
in dogs, with increasing interest of researchers
in the field of animal cognition. Joly-
Mascheroni and colleagues
81
have been the
first to demonstrate that the observation of
yawns elicits yawning in a non-primate species
like dogs, and to suggest the possibility of con-
tagious yawning between different species.
In this study the presentation of human
yawning elicited yawns in 72 per cent of the
dogs tested, which is higher than the rate re-
ported in humans (45-60%) and chimpanzees
(33%). The presence of contagious yawning in
dogs suggests that this phenomenon is not re-
stricted to primate species, and may indicate
that dogs possess the capacity for at least a
basic form of empathy. Since yawning is
known to modulate the level of arousal,
82
it
may help coordinate interactions as well as
communication between humans and dogs.
Madsen and Persson explored the ontog-
eny of dogs’ susceptibility to yawn contagion
and demonstrated that, like humans, they
show a developmental increase in susceptibil-
ity to yawn contagion, with consistent evi-
dence of contagion starting from 7 months.
Romero and colleagues also demonstrated
that human yawning can elicit CY in domestic
dogs, and that the social bond, associated with
empathy, mediates its occurrence; indeed
dogs yawn more frequently when watching
the familiar model than the unfamiliar one,
demonstrating once again the correlation with
the level of emotional proximity.
Similar findings have been found by Silva
and colleagues with the presentation of a
mere sound of a human yawn.
83
Results sug-
gest that dogs possess unique social skills in
interacting with humans, which may derive
from the process of domestication.
84
It has
been shown that they can follow human gaze
and pointing,
85
show sensitivity to others’
knowledge states
86
and match their actions to
observed human ones.
87
Silva and De Sousa
88
suggested three main
reasons for why dogs may be able to empa-
thize with humans. First, dogs originated
from wolves, which are highly social animals
Vanutelli & Balconi
96
that maintain cooperative activities and that
have some capacity for empathy towards fa-
miliar conspecifics. Second, biological chang-
es produced during domestication may have
allowed dogs to use their inherited empathic
capacities to synchronize with humans and
predict their behavior more flexibly than
their ancestors. Third, the selection for in-
creasingly complex cognitive capacities may
have led to more complex forms of empathy
that now resemble certain traits of human
emotional communication.
Besides contagious yawning, which reflects
automatic and involuntary behaviors elicited
by affective resonance and tuning mecha-
nisms, further evidence of voluntary prosocial
acts has been provided especially by human-
dog experiments. Their affectional bond is
particularly evident and relies on the fact that
dogs appear empathically well-tuned to hu-
man emotions.
89
They seem to celebrate our
joy and commiserate with our sorrow. Alt-
hough owners often report empathic behav-
iors in their pets, systematic empirical confir-
mation remains elusive.
90
Even if, as previous-
ly discussed, it has been found that dogs con-
tagiously yawn in response to a human yawn-
ing,
91
such behavior seems very different from
empathically responding to human emotional
displays such as distress.
In an attempt to solve this query, Cus-
tance and Mayer
92
performed an experiment
where dogs were exposed to their owner or a
stranger while he was talking, humming or
feigning to cry. They succeeded in showing
that dogs behave in an upset manner when
people fake distress and cry. In fact, the ma-
jority of dogs showed comfort-offering and
responded differently when both their owner
and the stranger were crying, in contrast with
humming or talking conditions. This behav-
ior strongly suggests sympathetic concern.
Inter-species interactions: Can humans
feel empathy for animals?
The majority of previous human studies
attempting to characterize empathy-related
responses did not separate empathy towards
humans from that towards animals. Fur-
thermore, in some studies, scenes showing an-
imals were treated as a neutral condition.
93
Nevertheless many people have a strong emo-
tional attachment to their pets and half of pet
owners consider their pet as much a part of
the family as any member of the household.
94
Literature on attachment measures
showed very similar results for human in-
fants’ and dogs’ behaviors with their mother
or owner during high and low stress condi-
tions.
95
Similar neurobiologic mechanisms of
bonding have been found in human-human
and owner-dog pairs, with increased levels of
oxytocin, beta-endorphin, prolactin, beta-
phenylethylamine, and dopamine in pet
owners and their dogs during
96
and after
97
a
positive interaction. Nevertheless, neural
substrates underlying the human-pet rela-
tionship are largely unknown.
A recent paper by Stoeckel and col-
leagues
98
examined brain activation patterns
by means of fMRI when mothers viewed im-
ages of their own child and dog, or an unfa-
miliar child and dog, with the aim of compar-
ing the functional neuroanatomy of human-
pet bonds with that of maternal-child bonds.
The authors reported substantial overlap in
brain activation patterns elicited by images
of both a mother’s own child and dog in re-
gions involved in reward (medial Orbito-
Frontal Cortex, mOFC; putamen),
99
emotion
and affiliation, together with similar pleas-
antness (valence) and excitement (arousal)
ratings for their child and dog compared to
unfamiliar pictures.
Moreover the amygdala was activated by
both the own child and dog images; it is
thought to be a critical region for bond for-
mation, and it may be involved in providing
the emotional tone and incentive salience that
directs attention to the needs of the child and
dog, which is critical for the formation of the-
se pair bonds. Such similarities between the
human-dog and the human-infant relation-
ship have been described within the frame-
work of human attachment theory, developed
Empathy and Prosocial Behaviours
97
to explain the role of the human infant-
caregiver relationship in development, to en-
sure safety, security and survival.
In this context the attachment bond has
been also extended to adult-adult caregivers,
peer, and romantic relationships,
100
and it
may be applied to the formation and mainte-
nance of people’s relationship with their
pets.
101
Anyway, while a common brain net-
work involved in reward, emotion, and affili-
ation was activated when mothers viewed
images of their child and dog, a specific acti-
vation emerged in response to images of their
child, localized in the dopamine, oxytocin,
and vasopressin-rich midbrain, a key region
involved in reward and affiliation. This result
replicates previous reports of maternal mid-
brain activation to stimuli related to their
child.
102
This area was not involved during
the observation of subjects’ own dog, indicat-
ing that, in humans, it is essential for the
formation and maintenance of pair bonds
that sustain and propagate our species. On
the other hand, own-dog images elicited
greater activation in the fusiform gyrus com-
pared to viewing own child. This region is
central to visual and face processing and so-
cial cognition.
103
Considering the primacy of language for
human-human communication, facial cues
may be a more central device for dog-human
interaction, by helping owners identify their
dog, use gaze direction to communicate, and
interpret emotional states.
104
To conclude,
despite the presence of similarities in the
perceived emotional experience and brain
function associated with the mother-child
and mother-dog bonds, there are also key dif-
ferences that may reflect variance in the evo-
lutionary course and function of these rela-
tionships.
An overlapping of brain region activation
when viewing human and animal images has
also been found in the case of suffering:
Franklin and colleagues,
105
in fact, asked their
human participants to observe images of
humans and animals in pain. They found
that many of the same brain regions known
to be involved in human empathy were active
when perceiving both human and animal suf-
fering, including the anterior cingulate gyrus
and anterior insula.
Anyway, despite these similarities, direct
comparisons also revealed distinct patterns
of activation in response to pictures of hu-
mans versus animals, suggesting that differ-
ent neural mechanisms may underlie how we
derive our empathic responses to humans
and animals: human suffering yielded signifi-
cantly greater medial prefrontal (MPFC), in-
ferior parietal and posterior cingulate activa-
tion, which are known to be implicated in
taking a third-person perspective of others’
situations
106
and distinguishing between
one’s own emotions and the emotions of
those who are suffering.
107
On the other
hand, observing dog versus human suffering
led to increased activation in the anterior in-
sula (AI), the inferior frontal gyrus (IFG) and
the precuneus.
The AI is important in the affective na-
ture of empathy, suggesting that perceiving
animal suffering elicits greater emotional re-
sponses than human suffering. The IFG, in-
stead, is active in mentalizing and empathy-
related tasks using picture-based stimuli.
108
This may reflect the greater effort needed to
understand the actions of scenes including
dogs than to perceive human suffering,
which can require more perspective-taking
mechanisms. Also, the IFG is involved in at-
tention allocation as part of the ventral atten-
tion system and is important in allocating at-
tention upon detecting salient stimuli and un-
expected changes in the environment.
109
Then, another possible explanation is that dog
suffering, being less familiar, captures atten-
tion to a greater degree than human suffering.
These results indicates that there are
many overlapping regions in humans’ em-
pathic responses to viewing animal and hu-
man suffering, particularly in areas classically
associated with empathic responses; also,
they indicate the presence of different and
specific neural substrates, suggesting that the
way we develop our empathic responses to
Vanutelli & Balconi
98
the suffering of dogs or humans may be dif-
ferent. More interestingly, many of the cited
regions differentially recruited for the two
conditions were significantly active for both
conditions if compared to baseline, indicat-
ing that although they represent potentially
different networks for similar empathic re-
sponses, they are not mutually exclusive, but
rather differentially predominant. This sug-
gests that empathy is not simply a response
we save for humans alone, but can also be ex-
tended to familiar animals.
Perceived closeness and similarity, in fact,
is thought to affect how much empathy is at-
tributed to suffering animals. Plous
110
has ex-
amined human responses to suffering in an-
imals with particular interest in the use of an-
imals for human gain. In his research, he
found that animals perceived as more similar
to humans were also judged as being more
capable of perceiving pain, and the viewing
of pictures depicting them in pain elicited
greater skin conductance responses (SCR),
indicating that perceiving suffering in those
animals aroused more anxiety than perceiv-
ing suffering in animals judged as being less
similar to humans. A couple of years later
Hills
111
investigated the relationship between
empathy towards animals and the attribution
of animal mind, which refers to the belief
that an animal is capable of thinking and
feeling. Six different emotional scenarios
were presented with printed text to farmers,
urban dwellers, and animal rights activists:
results showed that animals that were closer
phylogenetically to humans (mammals) were
rated higher in terms of the belief that they
possessed a mind than more distant animals
(cold-blooded animals and invertebrates).
In 2008 Westbury and Neumann
112
per-
formed an experiment in which participants
were exposed to ecological real-life film
stimuli depicting humans, primates, quadru-
ped mammals and birds in victimized cir-
cumstances while their SCR was recorded.
Participants also completed a subjective trait
empathy questionnaire. The authors hypoth-
esized that a linear pattern of responses
across increasing phylogenetic relatedness
would be found for each of the subjective and
psychophysiological measures of empathic
responding, with respect to the similarity hy-
pothesis. Consistent with Preston and de
Waal’s
113
interpretation of proximal empath-
ic mechanisms (the PAM of empathy), the
predicted linear pattern of empathy-related
responses as a function of phylogenetic simi-
larity was supported for both subjective em-
pathy ratings and SCR. Bird stimuli tended
to elicit less self-reported scorings than the
mammalian stimuli, while SCR decreased as
a function of phylogenetic distance. Moreo-
ver, high trait empathy participants gave
higher subjective empathy ratings and exhib-
ited greater corrugator electromyographic
activity than moderate and low trait empathy
participants. These results provide evidence
that human feelings of empathy tend to gen-
eralize easily towards animals perceived to be
similar, such as other mammals, but starts to
decline in response to non-mammals.
As previously discussed, empathic behav-
iors can be traced back to group life preserva-
tion, but also to nurturance and offspring
protection. In this framework, innate releas-
ing stimuli like infants could be particularly
salient and elicit stronger empathy-related
responses than older individuals, in particu-
lar during negative contexts. Prguda and
Neumann
114
presented their participants with
images of both infant and adult human and
wild non-human animals (non-human pri-
mates, quadruped wild mammals, and wild
birds) depicted in negative, victimizing situa-
tions. Subjective empathy and arousal ratings
were greater for human infants but this did
not extend to the non-human infants. Psy-
chophysiological measures did not differ
across species, but HR was lower during in-
fant than adult stimuli presentations, while a
pattern of HR deceleration followed by an
acceleration and subsequent deceleration was
observed for infant stimuli. Such a pattern
pertains to orienting behaviors, enhanced at-
tention and information intake.
115
Also, this study confirmed previous find-
Empathy and Prosocial Behaviours
99
ings that more empathic individuals produce
significantly higher subjective empathy rat-
ings than the lower empathy individuals,
suggesting that empathetic responding at the
inter-species level may shed further light on
human empathetic processes in general.
Moral and ethical issues related to
human-animal interactions
According to what has been discussed
above, it seems that the degree of empathy
shown towards animals may indicate a more
general capacity for empathy and prosocial
behavior. This is particularly interesting for
our discussion in that it has been theorized
by many philosophers that a humane treat-
ment of non-human animals is an indicator
of general moral propensity and ethical con-
duct. This hypothesis has recently found sup-
port by empirical studies demonstrating a link
between intra-human and human-animal vio-
lence.
116
However, little research has investi-
gated how human empathic responding ex-
tends towards non-human animals.
This association suggests that a lack of
empathy could be a general deficit, and not
simply restricted to expression towards other
human beings:
117
in fact, from criminal rec-
ord studies we know that offenders who en-
gage in animal abuse are also more likely to
have a history of violent
118
and concomitant
anti-social behaviors, such as drug, public
disorder and property offenses.
Even if the subjective attitude held to-
ward suffering individuals does not com-
pletely coincide with empathic behaviours, it
can be used to explore empathic responses
with respect to these and other ethical issues.
Filippi and colleagues
119
explored brain acti-
vations related to dietary preferences based
on avoidance of animal product consump-
tion for ethical reasons. In detail, they
scanned vegetarians, vegans and omnivores
while perceiving negatively valenced images
of injured and dead animals in comparison to
threatening images of violence in humans.
Vegetarians and vegans guided by ethical
issues were selected for this study as a possi-
ble example of people with humane concern
for animals, and they have been thought to
show different neural representation of con-
ditions of abuse and suffering, thanks to dif-
ferent motivational factors and beliefs. Re-
sults showed that people with greater interest
in animals consistently display higher en-
gagement of empathy-related areas while ob-
serving negative scenes, independently of the
species of the individuals involved, which is
characterized by an increased recruitment of
the ACC and the IFG. Moreover, they show
a higher engagement of empathy-related are-
as while observing negative scenes regarding
animals rather than humans, with the addi-
tional recruitment of the amygdala, for the
regulation of intense emotions, the MPFC
and the Posterior Cingulate Cortex (PCC).
These regions are frequently observed in
conditions involving representation of the
self and self values and the PCC, in particu-
lar, is also thought to be involved in memory
and visuospatial processing in relation to
emotions and social behavior. These results
reveal that distinct brain responses are
evoked by emotionally significant pictures of
humans and animals in people with particu-
lar concern for animals, suggesting that dif-
ferent motivational factors underlying pref-
erences and moral attitudes could reflect spe-
cific regulatory processes due to complicity
in the suffering of animals.
Starting from these results and the as-
sumption that vegetarians and vegans show
increased empathic responses to animal suf-
fering because of their propensity to identify
with them, Filippi and colleagues
120
hypothe-
sized that they could also show brain re-
sponses to animals behaviors performed by
humans, monkeys, and pigs, different from
omnivores. To prove this the authors showed
participants oral communicative actions
(OCA) vs biting. Results showed an in-
creased functional connectivity between re-
gions of the fronto-parietal and temporal
lobes during observation of mouth actions
performed by humans and, to the same de-
Vanutelli & Balconi
100
gree, animals, in people with more animal-
oriented empathy.
During human scenes they showed an in-
creased activity of the right amygdala, which
contributes to the analysis of body move-
ments for perception of actions through its
connections with the Superior Temporal Sul-
cus (STS) and the frontal cortex,
121
thus as-
signing emotional salience to sensory inputs.
Therefore, its increased activity suggests a
different analysis of dispositions and inten-
tions of other people in these individuals. Be-
sides these shared network activation, vege-
tarians and vegans also showed specific pat-
tern of brain response: vegetarians showed
an increased recruitment of the right medial
frontal gyrus (MFG) and right posterior in-
sula, which contributes to social perception,
to social cognitive processes (such as infer-
ences about others
122
), and to interoception,
perception and emotion,
123
respectively. In-
terestingly, the insula also modulates connec-
tions between the MNS and the limbic sys-
tem during social mirroring, and the ability
to empathize with others.
124
Vegans, on the other hand, recruited the
left MFG, Inferior Frontal Gyrus (IFG; pars
opercularis) and MTG (posterior portion),
which are part of the MNS. Such a system in-
cludes Broca’s area, which is involved in lan-
guage processing in humans. These results
indicate the presence of different portions of
empathy-related networks in people with
special attitudes towards animals, which con-
tribute to the modulation of social interac-
tions with other individuals.
Nevertheless, despite their particular pat-
tern of brain activation while processing ani-
mal mouth actions, the activity of this system
remains higher also for conspecifics. Also,
phylogenetical proximity with humans can
modulate MNS recruitment in these subjects,
as suggested by the between-group differences
observed for monkey, but not pig OCAs.
Discussion and conclusion
Starting from a systematic review of hu-
man studies it was possible to describe empa-
thy as a multifaceted and multilayered phe-
nomenon which ranges from relatively simple
processes such as behavioural or physiological
emotional tuning, to more complex events
which involve interaction between emotional
and cognitive perspective taking systems.
125
In
any case, a basic resonance mechanism is
thought to underlie the emotional empathic
response and includes (1) the capacity to
know what the other person is feeling, (2) to
mimic corresponding emotional behavior, to-
gether with (3) the intention to respond com-
passionately to another person’s distress.
126
These phenomena can occur automatically
and without awareness.
127
These three main
points will be discussed with respect to both
intra-human and intra-animal interactions.
With respect to the first point, consistent
evidence suggests a close relationship be-
tween trait empathy and the degree of sub-
jective responsiveness to facial cues, with
higher empathic subjects producing more ac-
curate responses to emotional faces.
128
More-
over, consistent with the second point, view-
ing another’s emotional expression automat-
ically triggers that emotion in oneself, and
elicits facial muscle reactions especially for
high empathic subjects,
129
together with in-
creased autonomic responsiveness.
130
Thus,
autonomic measures could be interpreted as
a mechanism for mirroring and understand-
ing the emotional condition displayed by
other people, while sharing similar emotional
and somatic responses.
131
Finally, it has been
found that the decision to engage in prosocial
behaviors is associated with measures of be-
havioral trait empathy assessed through
questionnaires.
Since animals cannot furnish verbal re-
sponses, more indirect ways to measure em-
pathic attitudes should be found: being part
of a more general process of emotional con-
tagion, a number of researchers have pro-
posed that humans and some other species
show a specific phenomenon of affective tun-
ing, contagious yawning. This is a useful
candidate behaviour to explore basic forms
Empathy and Prosocial Behaviours
101
of empathy across species in that it is present
in both humans and non-human animals. It
is more frequent in high empathic subjects
and it is related to empathy-related brain ar-
eas. Thus, although it is not an emotional re-
action itself, its occurrence has been clinical-
ly, psychologically, neurobiologically, and
behaviorally linked to our capacity for empa-
thy;
132
also, it is thought to represent the
commonest, developmentally earliest, and
phylogenetically oldest process by which
emotional empathy can arise.
133
Because of
its relevance to evolutionary biology CY has
been the focus of recent investigations in
non-human species which have demonstrat-
ed that chimpanzees,
134
bonobos,
135
gelada
baboons,
136
wolves
137
and domestic dogs,
138
yawn in relation to a conspecific yawning.
Besides CY, which reflects automatic and
involuntary behaviors elicited by affective
resonance and tuning mechanisms, further
evidence of voluntary prosocial acts has been
provided that many species are sensitive to
suffering in others. The extent to which ani-
mals are affected by the distress or pain of
conspecifics probably depends on the etho-
logical characteristics and the socializing atti-
tudes of the species. Prosocial attitudes have
been proved to be present in primates,
139
rats,
140
mice
141
and elephants,
142
while no CY
has been demonstrated in solitary species.
143
When we inquire into the presence of em-
pathic competencies in animals, distinctions
between species must be taken into account.
Consolation behaviors, coalition formation,
offering of protection and comfort are only
some of the available examples in the litera-
ture on animal-animal empathy.
Interestingly, empathy is more likely to
occur when there is perceived social proximi-
ty between individuals. This is also applicable
to animal-human interaction, in that the
available literature on the theme shows that
dogs-human bonds are particularly strong
since they rely on the domestication process.
Evidence proves that dogs show comfort-
offering in the presence of people crying,
which strongly suggests sympathetic concern.
Moreover it has been found that dogs
144
and
primates
145
can catch a human’s yawn.
Finally, and once again, evidence suggests
that, because of the similarity hypothesis,
human feelings of empathy also tend to gen-
eralize easily towards animals perceived to be
similar, such as other mammals, but starts to
decline in response to non-mammals. Alt-
hough the majority of available human stud-
ies did not separate empathy towards hu-
mans from that towards animals when we
consider human empathic attitudes towards
animals we must take into account that many
people have a strong emotional attachment
to their pets.
Available literature showed the presence
of similarities between the human-infant and
the human-animal relationship, which can be
interpreted as useful for the formation and
maintenance of people’s relationship with
their pets.
146
Moreover, results indicate that
there are many overlapping regions of activa-
tion in humans’ brain responses while view-
ing animal and human suffering, particularly
in areas classically associated with empathic
responses.
147
However, according to Gallese and col-
leagues,
148
“sharing the same body” between
the observer and the observed permits a di-
rect form of understanding by a process of
simulation in the mirror neuron system. If so,
what happens when we don’t share the same
body? With respect to cross-species interac-
tions perceived social proximity seems to be
crucial for animals expressing empathic atti-
tudes and for humans with high animal-
oriented empathy, with a series of moral and
ethical implications.
To conclude, previous attempts to meas-
ure empathic responsiveness in animals have
suffered from a lack of terminological
agreement over precise definitions of empa-
thy and emotional empathy. By now it is
shared knowledge that empathy is a phyloge-
netically continuous ability, ranging across
animals from more basic and automatic reac-
tions in response to the emotions of others,
up to at least basic forms of perspective-
Vanutelli & Balconi
102
taking in primates.
149
In fact, evidence in this
field suggests that empathic and sympathetic
concern may even have emerged from a pre-
human basis with a series of adaptive ad-
vantages.
From this perspective it seems that, ac-
cording to Charles Darwin’s work, the per-
ceived differences between human and ani-
mal empathy could be more quantitative
than qualitative, suggesting a common affec-
tive core which allows both categories to mir-
ror and tune to conspecifics’ feelings, where
in the case of humans it can be integrated
with more complex cognitive processes.
Notes
1
See H.R. WESTBURY, D.L. NEUMANN, Empathy-
related Responses to Moving Film Stimuli Depicting
Human and Non-human Animal Targets in Nega-
tive Circumstances, in: «Biological Psychology»,
vol. LXXVIII, n. 1, 2008, pp. 66-74.
2
See B. INBAL BEN-AMI, J. DECETY, P. MASON,
Empathy and Pro-Social Behavior in Rats, in:
«Science», vol. CCCXXXIV, 2011, pp. 1427-
1430.
3
See H.R. WESTBURY, D.L. NEUMANN, Empathy-
related Responses to Moving Film Stimuli Depicting
Human and Non-human Animal Targets in Nega-
tive Circumstances, cit.
4
See K.L. THOMPSON, E. GULLONE, Promotion of
Empathy and Prosocial Behaviour in Children
Through Humane Education, in: «Australian Psy-
chologist», vol. XXXVIII, n. 3, 2003, pp. 175-182.
5
See F.R. ASCIONE, Animal Abuse and Youth Vio-
lence, in: «Juvenile Justice Bulletin», 2001, pp. 1-
16, available at <https://www.ncjrs.gov/html/
ojjdp/jjbul2001_9_2/contents.html>; A.C. BALD-
RY, Animal Abuse Among Preadolescents Directly
and Indirectly Victimized at School and at Home,
in: «Criminal Behaviour and Mental Health»,
vol. XV, n. 2, 2005, pp. 97-110; P. BEIRNE, From
Animal Abuse to Interhuman Violence? A Critical
Review of the Progression Thesis, in: «Society and
Animals», vol. XII, n. 1, 2004, pp. 39-65.
6
See E.S. PAUL, Empathy with Animals and with
Humans: Are they Linked?, in: «Anthrozoös»,
vol. XIII, n. 4, 2000, pp. 194-202.
7
See M. BALCONI, A. BORTOLOTTI, L. GONZAGA,
Emotional Face Recognition, EMG Response, and
Medial Prefrontal Activity in Empathic Behavior,
in: «Neuroscience Research», vol. LXXI, n. 3,
2011, pp. 251-259; M. BALCONI, A. BORTOLOTTI,
Detection of the Facial Expression of Emotion and
Self-report Measures in Empathic Situations are
Influenced by Sensorimotor Circuit Inhibition by
Low-frequency rTMS, in: «Brain Stimulation»,
vol. V, n. 3, 2012, pp. 330-336; M. BALCONI, A.
BORTOLOTTI, Emotional Face Recognition, Em-
pathic Trait (BEES), and Cortical Contribution in
Response to Positive and Negative Cues. The Effect
of rTMS on Dorsal Medial Prefrontal Cortex, in:
«Cognitive Neurodynamics», vol. VII, n. 1, 2013,
pp. 13-21; M. BALCONI, A. BORTOLOTTI, Reso-
nance Mechanism in Empathic Behavior. BEES,
BIS/BAS and Psychophysiological Contribution, in:
«Physiology & Behavior», vol. CV, n. 2, 2012,
pp. 298-304; M. BALCONI, A. BORTOLOTTI, Self-
report, Personality and Autonomic System Modula-
tion in Response to Empathic Conflictual versus
Non Conflictual Situation, in: «Cognition &
Emotion», vol. XXVIII, n. 1, 2014, pp. 153-162;
M. BALCONI, A. BORTOLOTTI, Empathy in Coop-
erative Versus Non-cooperative Situations: The
Contribution of Self-Report Measures and Auto-
nomic Responses, in: «Applied Psychophysiology
and Biofeedback», vol. XXXVII, n. 3, 2012, pp.
161-169; M. BALCONI, A. BORTOLOTTI, D.
CRIVELLI, Self-report Measures, Facial Feedback,
and Personality Differences (BEES) in Cooperative
vs. Noncooperative Situations: Contribution of the
Mimic System to the Sense of Empathy, in: «Inter-
national Journal of Psychology», vol. XLVIII, n.
4, 2013, pp. 631-640; C.D. BATSON, K. SAGER, E.
GARST, M. KANG, K. RUBCHINSKY, K. DAWSON, Is
Empathy-induced Helping due to Self-other Merg-
ing?, in: «Journal of Personality and Social Psy-
chology», vol. LXXIII, n. 3, 1997, pp. 495-509; J.
DECETY, P.L. JACKSON, The Functional Architec-
ture of Human Empathy, in: «Behavioral and
Cognitive Neuroscience», vol. III, n. 7, 2004, pp.
71-100; E. HARMON-JONES, P. WINKIELMAN, So-
cial Neuroscience: Integrating Biological and Psy-
chological Explanations of Social Behavior, Guil-
ford Press, New York 2007; C.I. HOOKER, S.C.
VEROSKY, L.T. GERMINE, R.T. KNIGHT, M.
D’ESPOSITO, Mentalizing about Emotion and its
Relationship to Empathy, in: «Social, Cognitive
and Affective Neuroscience», vol. III, n. 3, 2008,
pp. 204-217; S.D. PRESTON, F.B.M. DE WAAL,
Empathy: Its Ultimate and Proximate Bases, in:
«Behavioral and Brain Sciences», vol. XXV, n. 1,
2002, pp. 1-71.
Empathy and Prosocial Behaviours
103
8
See B. CHAUHAN, C.J. MATHIAS, H.D. CRITCH-
LEY, Autonomic Contributions to Empathy: Evi-
dence from Patients with Primary Autonomic Fail-
ure, in: «Autonomic Neuroscience», vol. CXL, n.
1-2, 2008, pp. 96-100; T.W. LEE, R.J. DOLAN, H.D.
CRITCHLEY, Controlling Emotional Expression:
Behavioral and Neural Correlates of Nonimitative
Emotional Responses, in: «Cerebral Cortex», vol.
XVIII, n. 1, 2008, pp. 104-113.
9
See V. GALLESE, A.I. GOLDMAN, Mirror Neurons
and the Simulation Theory of Mind-reading, in:
«Trends in Cognitive Sciences», vol. II, n. 12,
1998, pp. 493-501.
10
See A.I. GOLDMAN, C.S. SRIPADA, Simulationist
Models of Face-based Emotion Recognition, in:
«Cognition», vol. XCIV, n. 3, 2005, pp. 193-213
11
See V. GALLESE, C. KEYSERS, G. RIZZOLATTI, A
Unifying View of the Basis of Social Cognition, in:
«Trends in Cognitive Sciences», vol. VIII, n. 9,
2004, pp. 396-403.
12
See M.L. HOFFMAN, Is Altruism Part of Human
Nature?, in: «Journal of Personality and Social
Psychology», vol. XL, n. 1, 1981, pp. 121-137.
13
See M. BALCONI, A. BORTOLOTTI, Detection of the
Facial Expression of Emotion and Self-report Measures
in Empathic Situations are Influenced by Sensorimo-
tor Circuit Inhibition by Low-frequency rTMS, cit.
14
See F. DE VIGNEMONT, T. SINGER, The Empathic
Brain: How, When and Why?, in: «Trends in Cog-
nitive Sciences», vol. X, n. 10, 2006, pp. 435-441
15
See M. BALCONI, A. BORTOLOTTI, L. GONZAGA,
Emotional Face Recognition, EMG Response, and Me-
dial Prefrontal Activity in Empathic Behavior, cit.
16
See P. ANDRÉASSON, U. DIMBERG, Emotional
Empathy and Facial Feedback, in: «Journal of
Nonverbal Behavior», vol. XXXII, n. 4, 2008, pp.
215-224; L.D.S. BESEL, Empathy: The Role of Faci-
al Expression Recognition, in: «Dissertation Ab-
stract International», vol. LXVIII, 2007, pp.
2638.
17
See M. BALCONI, A. BORTOLOTTI, Emotional
Face Recognition, Empathic Trait (BEES), and
Cortical Contribution in Response to Positive and
Negative Cues. The Effect of rTMS on Dorsal Me-
dial Prefrontal Cortex, cit.
18
See S.D. PRESTON, F.B.M. DE WAAL, Empathy, cit.
19
See M. BALCONI, A. BORTOLOTTI, L. GONZAGA,
Emotional Face Recognition, EMG Response, and Me-
dial Prefrontal Activity in Empathic Behavior, cit.
20
See S.D. PRESTON, A. BECHARA, H. DAMASIO,
T.J. GRABOWSKI, R.B. STANSFIELD, S. MEHTA,
A.R. DAMASIO, The Neural Substrates of Cognitive
Empathy, in: «Social Neuroscience», vol. II, n. 3-
4, 2007, pp. 254-275.
21
See M. SONNY-BORGSTRÖM, Automatic Mimic-
ry Reactions as Related to Differences in Emotional
Empathy, in: «Scandinavian Journal of Psycholo-
gy», vol. XLIII, n. 5, 2002, pp. 433-443; T.W. LEE,
R.J. DOLAN, H.D. CRITCHLEY, Controlling Emo-
tional Expression: Behavioral and Neural Corre-
lates of Nonimitative Emotional Responses, cit.
22
See M. BALCONI, A. BORTOLOTTI, L. GONZAGA,
Emotional Face Recognition, EMG Response, and
Medial Prefrontal Activity in Empathic Behavior,
cit.; M. BALCONI, Y. CANAVESIO, Emotional Con-
tagion and Trait Empathy in Prosocial Behavior in
Young People: The Contribution of Autonomic (Fa-
cial Feedback) and Balanced Emotional Empathy
Scale (BEES) Measures, in: «Journal of Clinical
and Experimental Neuropsychology», vol.
XXXV, n. 1, 2013, pp. 41-48; M. BALCONI, A.
BORTOLOTTI, D. CRIVELLI, Self-report Measures,
Facial Feedback, and Personality Differences
(BEES) in Cooperative vs. Noncooperative Situa-
tions: Contribution of the Mimic System to the
Sense of Empathy, cit.
23
See M. BALCONI, A. BORTOLOTTI, Detection of the
Facial Expression of Emotion and Self-report Measures
in Empathic Situations are Influenced by Sensorimo-
tor Circuit Inhibition by Low-frequency rTMS, cit. ;
V. GALLESE, A.I. GOLDMAN, Mirror Neurons and the
Simulation Theory of Mind-reading, cit.
24
See S.G. SHAMAY-TSOORY, Impaired Empathy
Following Ventromedial Prefrontal Brain Damage,
in: T. FARROW, P. WOODRUFF (eds.), Empathy in
Mental Illness, Cambridge University Press, New
York 2007, pp. 89-110.
25
See M. BALCONI, Y. CANAVESIO, High-frequency
rTMS on DLPFC Increases Prosocial Attitude in
case of Decision to Support People, in: «Social Neu-
roscience», vol. IX, n. 1, 2014, pp. 82-93.
26
See B. CHAKRABARTI, E. BULLMORE, S. BARON-
COHEN, Empathizing with Basic Emotions: Com-
mon and Discrete Neural Substrates, in: «Social
Neuroscience», vol. I, n. 3-4, 2006, pp. 364-384.
27
See S.G. SHAMAY-TSOORY, Impaired Empathy
Following Ventromedial Prefrontal Brain Damage,
cit.; C.J. HARMER, K.V. THILO, J.C. ROTHWELL,
G.M. GOODWIN, Transcranial Magnetic Stimula-
tion of Medialfrontal Cortex Impairs the Pro-
cessing of Angry Facial Expressions, in: «Nature
Neuroscience», vol. IV, n. 1, 2001, pp. 17-18; L.T.
RAMESON, M.D. LIEBERMAN, Empathy: A Socio
Cognitive Neuroscience Approach, in: «Social and
Vanutelli & Balconi
104
Personality Psychology Compass», vol. III, n. 1,
2009, pp. 94-110.
28
See S.G. SHAMAY-TSOORY, Impaired Empathy Fol-
lowing Ventromedial Prefrontal Brain Damage, cit.
29
See M. BALCONI, A. BORTOLOTTI, L. GONZAGA,
Emotional Face Recognition, EMG Response, and Me-
dial Prefrontal Activity in Empathic Behavior, cit.
30
See M. BALCONI, Y. CANAVESIO, Prosocial Attitudes
and Empathic Behavior in Emotional Positive versus
Negative Situations: Brain Response (ERPs) and
Source Localization (LORETA) Analysis, in: «Cogni-
tive Processing», vol. XIV, n. 1, 2013, pp. 63-72.
31
See M. BALCONI, Y. CANAVESIO, High-frequency
rTMS on DLPFC Increases Prosocial Attitude in
case of Decision to Support People, cit.
32
See A.I. GOLDMAN, C.S. SRIPADA, Simulationist
Models of Face-based Emotion Recognition, cit.; R.
ADOLPHS, Neural Systems for Recognizing Emo-
tion, in: «Current Opinion in Neurobiology»,
vol. XII, n. 2, 2002, pp. 169-177; C. KEYSERS, V.
GAZZOLA, Towards a Unifying Neural Theory of
Social Cognition, in: «Progress in Brain Re-
search», vol. CLVI, 2006, pp. 379-401.
33
See L. CARR, M. IACOBONI, M.C. DUBEAU, J.C.
MAZZIOTTA, G.L. LENZI, Neural Mechanisms of
Empathy in Humans: A Relay from Neural Systems
for Imitation to Limbic Areas, in: «Proceedings of
the National Academy of Sciences of the United
States of America», vol. C, 2003, pp. 5497-5502;
P.M. NIEDENTHAL, Embodying Emotion, in: «Sci-
ence», vol. CCCXVI, 2007, pp. 1002-1005.
34
See R. ADOLPHS, Neural Systems for Recognizing
Emotion, cit.; R. ADOLPHS, H. DAMASIO, D.
TRANEL, G. COOPER, A.R. DAMASIO, A Role for
Somatosensory Cortices in the Visual Recognition of
Emotion as Revealed by Three-dimensional Lesion
Mapping, in: «The Journal of Neuroscience»,
vol. XX, n. 7, 2000, pp. 2683-2690; R. ADOLPHS,
Recognizing Emotion from Facial Expressions: Psy-
chological and Neurological Mechanisms, in: «Be-
havioral and Cognitive Neuroscience Review»,
vol. I, n. 1, 2002, pp. 21-62.
35
See G. HEIN, T. SINGER, I Feel How You Feel but
not Always: The Empathic Brain and its Modula-
tion, in: «Current Opinion in Neurobiology»,
vol. XVIII, n. 2, 2008, pp. 153-158.
36
See M. DE WIED, A. VAN BOXTEL, R. ZAALBERG,
P.P. GOUDENA, W. MATTHYS, Facial EMG Re-
sponses to Dynamic Emotional Facial Expressions
in Boys with Disruptive Behavior Disorders, in:
«Journal of Psychiatric Research», vol. XL, n. 2,
2006, pp. 112-121; M. BALCONI, A. BORTOLOTTI,
Resonance Mechanism in Empathic Behavior, cit.;
M. BALCONI, A. BORTOLOTTI, Empathy in Coop-
erative Versus Non-cooperative Situations, cit.; M.
BALCONI, A. BORTOLOTTI, D. CRIVELLI, Self-
report Measures, Facial Feedback, and Personality
Differences (BEES) in Cooperative vs. Noncoopera-
tive Situations, cit.
37
See O.N. FRASER, D. STAHL, F. AURELI, Stress
Reduction Through Consolation Chimpanzees, in:
«Proceedings of the National Academy of Sci-
ences of the United States of America», vol. CV,
2008, pp. 8557-8562.
38
See K. SILVA, L. DE SOUSA, Canis Empathicus’?
A Proposal on Dogs’ Capacity to Empathize with
Humans, in: «Biology Letters», vol. VII, n. 4,
2011, pp. 489-492
39
See S.D. PRESTON, F.B.M. DE WAAL, Empathy, cit.
40
See O.N. FRASER, D. STAHL, F. AURELI, Stress
Reduction Through Consolation Chimpanzees, cit.;
O.N. FRASER, T. BUGNYAR, Do Ravens show Con-
solation? Responses to Distressed Others, in: «PLoS
ONE», vol. V, 2010, art. n. e10605
41
See F.B.M. DE WAAL, The Antiquity of Empathy,
in: «Science», vol. CCCXXXVI, 2012, pp. 874-876.
42
See R.I.M. DUNBAR, The Social Brain Hypothe-
sis, in: «Evolutionary Anthropology», vol. VI, n.
5, 1998, pp. 178-190.
43
See B. INBAL BEN-AMI, J. DECETY, P. MASON,
Empathy and Pro-Social Behavior in Rats, cit.;
C.A.F. WASCHER, I.B.R. SCHEIBER, K. KO-
TRSCHAL, Heart Rate Modulation in by Standing
Geese Watching Social and Non-social Events, in:
«Proceedings of the National Academy of Sci-
ences of the United States of America», vol.
CCLXXV, 2008, pp. 1653-1659.
44
See S.M. O’CONNELL, Empathy in Chimpanzees:
Evidence for Theory of Mind?, in: «Primates»,
vol. XXXVI, n. 3 1995, pp. 397-410.
45
See S.D. PRESTON, F.B.M. DE WAAL, Empathy, cit.
46
See F.B.M. DE WAAL, Putting the Altruism Back
into Altruism: The Evolution of Empathy, in:
«Annual Review of Psychology», vol. LIX, 2008,
pp. 279-300.
47
See A. CLYVIA, M.C. KAIZER, R.V. SANTOS, R.J.
YOUNG, C. CÄSAR, Do Wild Titi Monkeys show
Empathy?, in: «Primate Biology», vol. I, 2014,
pp. 23-28.
48
See F.B.M. DE WAAL, The Antiquity of Empathy,
cit.
49
See C.D. BATSON, K. SAGER, E. GARST, M.
KANG, K. RUBCHINSKY, K. DAWSON, Is Empathy-
induced Helping due to Self-other Merging?, cit. J.
Empathy and Prosocial Behaviours
105
DECETY, P.L. JACKSON, The Functional Architec-
ture of Human Empathy, cit.; S.D. PRESTON,
F.B.M. DE WAAL, Empathy: Its Ultimate and Prox-
imate Bases, cit.
50
See A. CLYVIA, M.C. KAIZER, R.V. SANTOS, R.J.
YOUNG, C. CÄSAR, Do Wild Titi Monkeys show
Empathy?, cit.
51
See J.B. SILK, Empathy, Sympathy, and Prosocial
Preferences in Primates, in: L. BARRETT, R.I.M.
DUNBAR (eds.), Oxford Handbook of Evolutionary
Psychology, Oxford University Press, Oxford
2007, pp. 115-126.
52
See T. ROMERO, M. ITO, A. SAITO, T. HASEGA-
WA, Social Modulation of Contagious Yawning in
Wolves, in: «PLoS ONE», vol. IX, n. 8, 2014, art.
n. e105963.
53
See S.M. PLATEK, F.B. MOHAMED, G.G. GAL-
LUP, Contagious Yawning and the Brain, in:
«Cognitive Brain Research», vol. XXIII, n. 2-3,
2005, pp. 448-452; S.R. ARNOTT, A. SINGHAL,
M.A. GOODALE, An Investigation of Auditory Con-
tagious Yawning, in: «Cognitive, Affective and
Behavioral Neuroscience», vol. IX, n. 3, 2009, pp.
335-342; F.B. NAHAB, N. HATTORI, Z.S. SAAD, M.
HALLETT, Contagious Yawning and the Frontal
Lobe: An fMRI Study, in: «Human Brain Map-
ping», vol. XXX, n. 5, 2009, pp. 1744-1751.
54
See I. NORSCIA, E. PALAGI, Yawn Contagion and
Empathy in Homo sapiens, in: «PLoS ONE», vol.
VI, n. 7, 2011, art. n. e28472; F.B. NAHAB, N.
HATTORI, Z.S. SAAD, M. HALLETT, Contagious
Yawning and the Frontal Lobe: An fMRI Study,
cit.; S.D. PRESTON, F.B.M. DE WAAL, Empathy, cit.
55
See F.B. NAHAB, N. HATTORI, Z.S. SAAD, M. HAL-
LETT, Contagious Yawning and the Frontal Lobe: An
fMRI Study, cit.; I. NORSCIA, E. PALAGI, Yawn Con-
tagion and Empathy in Homo sapiens, cit.; J.R. AN-
DERSON, M. MYOWA-YAMAKOSHI, T. MATSUKAWA,
Contagious Yawning in Chimpanzees, in: «Proceed-
ings of the Royal Society: Biological Science, Series
B», vol. CCLXXI, 2004, pp. 468-470.
56
See S.M. PLATEK, S.R. CRITTON, T.E.J. MYERS,
G.G. GALLUP, Contagious Yawning: The Role of
Self-awareness and Mental State Attribution, in:
«Cognitive Brain Research», vol. XVII, n. 2,
2003, pp. 223-227.
57
See A. SENJU, M. MAEDA, Y. KIKUCHI, T. HA-
SEGAWA, Y. TOJO, H. OSANAI, Absence of Conta-
gious Yawning in Children with Autism Spectrum
Disorder, in: «Biology Letters», vol. III, n. 6,
2007, pp. 706-708.
58
See I. NORSCIA, E. PALAGI, Yawn Contagion and
Empathy in Homo sapiens, cit.
59
See T. ROMERO, M. ITO, A. SAITO, T. HASEGA-
WA, Social Modulation of Contagious Yawning in
Wolves, cit.
60
See B.L. DEPUTTE, Ethological Study of Yawning
in Primates. I. Quantitative Analysis and Study of
Causation in two Species of Old World Monkeys
(Cercocebus albigena and Macaca fascicularis), in:
«Ethology», vol. XCVIII, n. 3-4, 1994, pp. 221-
245; O. WALUSINSKY, Yawning: Unsuspected Ave-
nue for a Better Understanding of Arousal and In-
teroception, in: «Medical Hypotheses», vol.
LXVII, n. 1, 2006, pp. 6-14.
61
See R. BAENNINGER, Some Comparative Aspects
of Yawning in Betta splendens, Homo sapiens, Pan-
thera leo, and Papio sphinx, in: «Journal of Com-
parative Psychology», vol. CI, n.4, 1987, pp. 349-
354; A.C. GALLUP, G.G. GALLUP JR., Yawning as a
Brain Cooling Mechanism: Nasal Breathing and
Forehead Cooling Diminish the Incidence of Conta-
gious Yawning, in: «Evolutionary Psychology»,
vol. V, n. 1, 2007, pp. 92-101.
62
See T. ROMERO, A. KONNO, T. HASEGAWA,
Familiarity Bias and Physiological Responses in
Contagious Yawning by Dogs Support Link to Em-
pathy, in: «PLoS ONE», vol. VIII, n. 8, 2013, art.
n. e71365; M.W. CAMPBELL, J.D. CARTER, D.
PROCTOR, M.L. EISENBERG, F.B.M. DE WAAL,
Computer Animations Stimulate Contagious
Yawning in Chimpanzees, in: «Proceedings of the
Royal Society: Biological Science, Series B», vol.
CCLXXVI, 2009, pp. 4255-4259.
63
See T. ROMERO, M. ITO, A. SAITO, T. HASEGA-
WA, Social Modulation of Contagious Yawning in
Wolves, cit.
64
See E. PALAGI, A. LEONE, G. MANCINI, P.F. FER-
RARI, Contagious Yawning in Gelada baboons as a
Possible Expression of Empathy, in: «Proceedings of
the National Academy of Sciences of the United Sta-
tes of America», vol. CVI, 2009, pp. 19262-19267.
65
See E.A. MADSEN, T. PERSSON, Contagious
Yawning in Domestic Dog Puppies (Canis lupus
familiaris): The Effect of Ontogeny and Emotional
Closeness on Low-level Imitation in Dogs, in: «An-
imal Cognition», vol. XVI, n. 2, pp. 233-240;
R.M. JOLY-MASCHERONI, A. SENJU, A.J. SHEP-
HERD, Dogs Catch Human Yawns, in: «Biology
Letters», vol. IV, n. 5, 2008, pp. 446-448.
66
See A. WILKINSON, N. SEBANZ, I. MANDL, L.
HUBER, No Evidence of Contagious Yawning in the
Red-footed Tortoise Geochelone carbonaria, in:
«Current Zoology», vol. LVII, n. 4, 2011, pp.
Vanutelli & Balconi
106
477-484.
67
See E. PALAGI, A. LEONE, G. MANCINI, P.F. FER-
RARI, Contagious Yawning in Gelada baboons as a
Possible Expression of Empathy, cit.
68
See E.A. MADSEN, T. PERSSON, Contagious
Yawning in Domestic Dog Puppies (Canis lupus
familiaris): The Effect of Ontogeny and Emotional
Closeness on Low-level Imitation in Dogs, cit.
69
See S.D. PRESTON, F.B.M. DE WAAL, Empathy,
cit.; F.B.M. DE WAAL, Putting the Altruism back
into Altruism, cit.
70
See T. ROMERO, M. ITO, A. SAITO, T. HASEGA-
WA, Social Modulation of Contagious Yawning in
Wolves, cit.
71
See F.B.M. DE WAAL, The Antiquity of Empathy, cit.
72
See T. ROMERO, M.A. CASTELLANOS, F.B.M. DE
WAAL, Consolation as Possible Expression of Sym-
pathetic Concern Among Chimpanzees, in: «Pro-
ceedings of the National Academy of Sciences of
the United States of America», vol. CVII, 2010,
pp. 12110-12115.
73
See S.M. O’CONNELL, Empathy in Chimpanzees:
Evidence for Theory of Mind?, cit.
74
See A. CLYVIA, M.C. KAIZER, R.V. SANTOS, R.J.
YOUNG, C. CÄSAR, Do Wild Titi Monkeys show
Empathy?, cit.
75
See L.A. BATES, P.C. LEE, N. NJIRAINI, J.H.
POOLE, K. SAYIALEL, S. SAYIALEL, C.J. MOSS, R.W.
BYRNE, Do Elephants show Empathy?, in: «Jour-
nal of Consciousness Studies», vol. XV, n. 10-11,
2008, pp. 204-225.
76
See B. INBAL BEN-AMI, J. DECETY, P. MASON,
Empathy and Pro-Social Behavior in Rats, cit.
77
See R.M. CHURCH, Emotional Reactions of Rats
to the Pain of Others, in: «Journal of Comparative
and Physiological Psychology», vol. LII, n. 2,
1959, pp. 132-134.
78
See D.J. LANGFORD, S.E. CRAGER, Z. SHEHZAD,
S.B. SMITH, S.G. SOTOCINAL, Social Modulation of
Pain as Evidence for Empathy in Mice, in: «Sci-
ence», vol. CCCXII, 2006, pp. 1967-1970.
79
See E.A. MADSEN, T. PERSSON, S. SAYEHLI, S. LEN-
NINGER, G. SONESSON, Chimpanzees show a Devel-
opmental Increase in Susceptibility to Contagious
Yawning: A Test of the Effect of Ontogeny and Emo-
tional Closeness on Yawn Contagion, in: «PLoS
ONE», vol. VIII, n. 10, 2013, art. n. e76266.
80
See E.A. MADSEN, T. PERSSON, Contagious
Yawning in Domestic Dog Puppies (Canis lupus
familiaris): The Effect of Ontogeny and Emotional
Closeness on Low-level Imitation in Dogs, cit.
81
See R.M. JOLY-MASCHERONI, A. SENJU, A.J.
SHEPHERD, Dogs Catch Human Yawns, cit.
82
See G. DAQUIN, J. MICALLEF, O. BLIN, Yawning,
in: «Sleep Medicine Reviews», vol. V, n. 4, 2001,
pp. 299-312.
83
See T. ROMERO, A. KONNO, T. HASEGAWA,
Familiarity Bias and Physiological Responses in
Contagious Yawning by Dogs Support Link to Em-
pathy, cit.; K. SILVA, J. BESSA, L. DE SOUSA, Audi-
tory Contagious Yawning in Domestic Dogs (Canis
familiaris): First Evidence for Social Modulation,
in: «Animal Cognition», vol. XV, n. 4, 2012, pp.
721-724
84
See B. HARE, M. TOMASELLO, Human-like Social
Skills in Dogs?, in: «Trends in Cognitive Scienc-
es», vol. IX, n. 9, 2005, pp. 439-444; A. MIKLÒSI,
J. TOPÀL, V. CSÀNYI, Big Thoughts in Small
Brains? Dogs as a Model for Understanding Human
Social Cognition, in: «Neuroreport», vol. XVIII,
n. 5, 2007, pp. 467-471.
85
See B. HARE, M. BROWN, C. WILLIAMSON, M.
TOMASELLO, The Domestication of Social Cogni-
tion in Dogs, in: «Science», vol. CCXCVIII, 2002,
pp. 1634-1636.
86 See A. MIKLÒSI, K. SOPRONI, A Comparative
Analysis of Animals’ Understanding of the Human
Pointing Gesture, in: «Animal Cognition», vol.
IX, n. 2, 2006, pp. 81-93.
86
See Z. VIRÀNYI, J. TOPÀL, A. MIKLÒSI, V. CNYI,
A Nonverbal Test of Knowledge Attribution: A Com-
parative Study on Dogs and Children, in: «Animal
Cognition», vol. IX, n. 1, 2006, pp. 13-26.
87
See J. TOPÀL, R. BYRNE, A. MIKLÒSI, V. CSÀNYI,
Reproducing Human Actions and Action Sequences:
“Do as I do!” in a Dog, in: «Animal Cognition»,
vol. IX, n. 4, 2006, pp. 355-367.
88
See K. SILVA, L. DE SOUSA, Canis empathicus?, cit.
89
See W.F. VITULLI, Attitudes Toward Empathy
in Domestic Dogs and Cats, in: «Psychological Re-
ports», vol. XCIX, n. 3, 2006, pp. 981-991.
90
See K. SILVA, L. DE SOUSA, Canis empathicus?, cit.
91
See R.M. JOLY-MASCHERONI, A. SENJU, A.J.
SHEPHERD, Dogs Catch Human Yawns, cit.
92
See D. CUSTANCE, J. MAYER, Empathic-like Re-
sponding by Domestic Dogs (Canis familiaris) to
Distress in Humans: An Exploratory Study, cit.
93
See M. FILIPPI, G. RICCITELLI, A. FALINI, F. DI
SALLE, P. VUILLEUMIER, G. COMI, M.A. ROCCA,
The Brain Functional Networks Associated to Hu-
man and Animal Suffering Differ Among Omni-
vores, Vegetarians and Vegans, in: «PLoS ONE»,
vol. V, n. 5, 2010, art. n. e10847.
94
See L.E. STOECKEL, L.S. PALLEY, R.L. GOLLUB,
Empathy and Prosocial Behaviours
107
S.M. NIEMI, A.E. EVINS, Patterns of Brain Activa-
tion when Mothers View Their Own Child and
Dog: An fMRI Study, in: «PLoS ONE», vol. IX, n.
10, 2014, art. n. e107205.
95
See J. TOPÀL, A. MIKLÒSI, V. CSANYI, A. DOKA,
Attachment Behavior in Dogs (Canis familiaris): A
New Application of Ainsworth’s (1969) Strange
Situation Test, in: «Journal of Comparative Psy-
chology», vol. CXII, n. 3, 1998, pp. 219-229; E.
PRATO-PREVIDE, D.M. CUSTANCE, C. SPIEZIO, F.
SABATINI, Is the Dog-human Relationship an At-
tachment Bond? An Observational Study Using
Ainsworth’s Strange Situation, in: «Behaviour»,
vol. CXL, n. 2, 2003, pp. 225-254; R. PALMER, D.
CUSTANCE, A Counterbalanced Version of Ains-
worth’s Strange Situation Procedure Reveals Se-
cure-base Effects in Dog-human Relationships, in:
«Applied Animal Behaviour Science», vol. CIX,
n. 2, 2008, pp. 306-319.
96
See J.S. ODENDAAL, R.A. MEINTJES, Neurophysi-
ological Correlates of Affiliative Behaviour Between
Humans and Dogs, in: «The Veterinaty Journal»,
vol. CLXV, n. 3, 2003, pp. 296-301.
97
See M. NAGASAWA, T. KIKUSUI, T. ONAKA, M.
OHTA, Dog’s Gaze at its Owner Increases Owner’s
Urinary Oxytocin During Social Interaction, in:
«Hormones and Behavior», vol. LV, n. 3, 2009,
pp. 434-441; S.C. MILLER, C. KENNEDY, D.
DEVOE, M. HICKEY, T. NELSON, L. KOGAN, An
Examination of Changes in Oxytocin Levels in Men
and Women before and after Interaction with a
Bonded Dog, in: «Anthrozoös», vol. XXII, n. 1,
2009, pp. 31-42; L. HANDLIN, E. HYDBRING-
SANDBERG, A. NILSSON, M. EJDEBACK, A. JANS-
SON, K. UVNÄS-MOBERG, Short-term Interaction
between Dogs and Their Owners: Effects on Oxyto-
cin, Cortisol, Insulin and Heart Rate. An Explora-
tory Study, in: «Anthrozoös», vol. XXIV, n. 3,
2011, pp. 301-315.
98
See L.E. STOECKEL, L.S. PALLEY, R.L. GOLLUB,
S.M. NIEMI, A.E. EVINS, Patterns of Brain Activa-
tion when Mothers View Their Own Child and
Dog: An fMRI Study, cit.
99
See J.E. SWAIN, J.P. LORBERBAUM, S. KOSE, L.
STRATHEARN, Brain Basis of Early Parent-infant
Interactions: Psychology, Physiology, and in vivo
Functional Neuroimaging Studies, in: «Journal of
Child Psychology and Psychiatry», vol. XLVIII,
n. 3-4, 2007, pp. 262-287; C.E. PARSONS, K.S.
YOUNG, L. MURRAY, A. STEIN, M.L. KRINGEL-
BACH, The Functional Neuroanatomy of the Evolv-
ing Parent-infant Relationship, in: «Progress in
Neurobiology», vol. XCI, n. 3, 2010, pp. 220-241.
100
See M.D. AINSWORTH, Attachments beyond In-
fancy, in: «American Psychologist», vol. XLIV, n.
4, pp. 709-716.
101
See L.A. KURDEK, Pet Dogs as Attachment Fig-
ures for Adult Owners, in: «Journal of Family Psy-
chology», vol. XXIII, n. 4, 2009, pp. 439-446; L.
HORN, L. HUBER, F. RANGE, The Importance of the
Secure Base Effect for Domestic Dogs - Evidence from
a Manipulative Problem-solving Task, in: «PLoS
ONE», vol. VIII, n. 5, 2013, art. n. e65296.
102
See A. BARTELS, S. ZEKI, The Neural Correlates of
Maternal and Romantic Love, in: «Neuroimage»,
vol. XXI, n. 3, 2004, pp. 1155-1166; L. STRATHEARN,
J. LI, P. FONAGY, P.R. MONTAGUE, What’s in a
Smile? Maternal Brain Responses to Infant Facial
Cues, in: «Pediatrics», vol. CXXII, n. 1, 2008, pp.
40-51; J.P. LORBERBAUM, J.D. NEWMAN, A.R. HOR-
WITZ, J.R. DUBNO, R.B. LYDIARD, M.B. HAMNER,
D.E. BOHNING, M.S. GEORGE, A Potential Role for
Thalamocingulate Circuitry in Human Maternal Be-
havior, in: «Biological Psychiatry», vol. LI, n. 6,
2002, pp. 431-445.
103
See N. KANWISHER, J. MCCERMOTT, M.M.
CHUN, The Fusiform Face Area: A Module in Hu-
man Extrastriate Cortex Specialized for Face Per-
ception, in: «The Journal of Neuroscience», vol.
XVII, n. 11, 1997, pp. 4302-4311; D.A. LEOPOLD,
G. RHODES, A Comparative View of Face Percep-
tion, in: «Journal of Comparative Psychology»,
vol. CXXIV, n. 3, 2010, pp. 233-251.
104
See D.A. LEOPOLD, G. RHODES, A Comparative
View of Face Perception, cit.; T. BLOOM, H.
FRIEDMAN, Classifying Dogs’ (Canis familiaris)
Facial Expressions from Photographs, in: «Behav-
ioural Processes», vol. XCVI, 2013, pp. 1-10.
105
See R.J. FRANKLIN JR., A.J. NELSON, M. BAKER,
J.E. BEENEY, T.K. VESCIO, A. LENZ-WATSON, R.G.
ADAMS JR., Neural Responses to Perceiving Suffer-
ing in Humans and Animals, in: «Social Neuro-
science», vol. VIII, n. 3 2013, 217-227.
106
See P. RUBY, J. DECETY, Effect of Subjective Per-
spective Taking During Simulation of Action: A
PET Investigation of Agency, in: «Nature Neuro-
science», vol. IV, n. 5, 2001, pp. 546-550.
107
See J. DECETY, J. GRÈZES, The Power of Simula-
tion: Imagining One’s Own and Other’s Behavior, in:
«Brain Research», vol. MLXXIX, n. 1, pp. 4-14.
108
See C. LAMM, J. DECETY, T. SINGER, Meta-
analytic Evidence for Common and Distinct Neural
Networks Associated with Directly Experienced
Pain and Empathy for Pain, in: «Neuroimage»,
Vanutelli & Balconi
108
vol. LIV, n. 3, 2011, pp. 2492-2502.
109
See M. CORBETTA, J.M. KINCADE, J.M.
OLLINGER, M.P. MCAVOY, G.L. SHULMAN, Volun-
tary Orienting is Dissociated from Target Detection
in Human Posterior Parietal Cortex, in: «Nature
Neuroscience», vol. III, n. 3, 2000, pp. 292-297.
110
See S. PLOUS, Psychological Mechanisms in the
Human Use of Animals, in: «Journal of Social Is-
sues», vol. XLIX, n. 1, 1993, pp. 11-52.
111
See A.M. HILLS, Empathy and Belief in the
Mental Experience of Animals, in: «Anthrozoös»,
vol. VIII, n. 3, 1995, pp. 132-142.
112
See H.R. WESTBURY, D.L. NEUMANN, Empa-
thy-related Responses to Moving Film Stimuli De-
picting Human and Non-human Animal Targets in
Negative Circumstances, cit.
113
See S.D. PRESTON, F.B.M. DE WAAL, Empathy:
Its Ultimate and Proximate Bases, cit.
114
See E. PRGUDA, D.L. NEUMANN, Inter-human
and Animal-directed Empathy: A Test for Evolu-
tionary Biases in Empathetic Responding, in: «Be-
havioural Processes», vol. CVIII, 2014, pp.
S0376-6357(14)00208-3.
115
See M.M. BRADLEY, P.J. LANG, Motivation and
Emotion, in: J.T. CACIOPPO, L.G. TASSINARY,
G.G. BERNTSON (eds.), Handbook of Psychophysi-
ology, Cambridge University Press, New York
2006, pp. 581-607, III ed.
116
See K.L. THOMPSON, E. GULLONE, Promotion of
Empathy and Prosocial Behaviour in Children
Through Humane Education, cit.; F.R. ASCIONE,
Animal Abuse and Youth Violence, cit.; P. BEIRNE,
From Animal Abuse to Interhuman Violence?, cit.
117
See F.R. ASCIONE, Animal Abuse and Youth Vi-
olence, cit.; A.C. BALDRY, Animal Abuse Among
Preadolescents Directly and Indirectly Victimised
at School and at Home, cit.; P. BEIRNE, From Ani-
mal Abuse to Interhuman Violence?, cit.;
118
See L. MERZ-PEREZ, K.M. HEIDE, I.J. SILVER-
MAN, Childhood Cruelty to Animals and Subse-
quent Violence against Humans, in: «International
Journal of Offender Therapy and Comparative
Criminology», vol. XLV, n. 5, 2001, pp. 556-573.
119
See M. FILIPPI, G. RICCITELLI, A. FALINI, F. DI
SALLE, P. VUILLEUMIER, G. COMI, M.A. ROCCA,
The Brain Functional Networks Associated to Hu-
man and Animal Suffering Differ Among Omni-
vores, Vegetarians and Vegans, cit.
120
See M. FILIPPI, G. RICCITELLI, A. MEANI, A.
FALINI, G. COMI, M.A. ROCCA, The ‘‘Vegetarian
Brain’’: Chatting with Monkeys and Pigs?, in:
«Brain Structure and Function», vol. CCXVIII,
n. 5, 2013, pp. 1211-1227.
121
See T. ALLISON, A. PUCE, G. MCCARTHY, Social
Perception from Visual Cues: Role of the STS Re-
gion, in: «Trends in Cognitive Sciences», vol. IV,
n. 7, 2000, pp. 267-278.
122
See V. P. MURTY, M. RITCHEY, R.A. ADCOCK,
K.S. LABAR, fMRI Studies of Successful Emotional
Memory Encoding: A Quantitative Metaanalysis,
in: «Neuropsychologia», vol. XLVIII, n. 12,
2010, pp. 3459-3469.
123
See F. CAUDA, T. COSTA, D.M. TORTA, K. SAC-
CO, F. D’AGATA, S. DUCA, G. GEMINIANI, P.T. FOX,
A. VERCELLI, Meta-analytic Clustering of the Insular
Cortex: Characterizing the Meta-analytic Connec-
tivity of the insula when Involved in Active Tasks, in:
«Neuroimage», vol. LXII, n. 1, 2012, pp. 343-355.
124
Se M. IACOBONI, Imitation, Empathy, and Mir-
ror Neurons, in: «Annual Review of Psychology»,
vol. LX, 2009, pp. 653-670.
125
See S.D. PRESTON, F.B.M. DE WAAL, Empathy:
Its Ultimate and Proximate Bases, cit.; S.D. PRES-
TON, A. BECHARA, H. DAMASIO, T.J. GRABOWSKI,
R.B. STANSFIELD, S. MEHTA, A.R. DAMASIO, The
Neural Substrates of Cognitive Empathy, cit.
126
See M. BALCONI, A. BORTOLOTTI, L. GON-
ZAGA, Emotional Face Recognition, EMG Response,
and Medial Prefrontal Activity in Empathic Behav-
ior, cit.; M. BALCONI, A. BORTOLOTTI, Detection
of the Facial Expression of Emotion and Self-report
Measures in Empathic Situations are Influenced by
Sensorimotor Circuit Inhibition by Low-frequency
rTMS, cit.; M. BALCONI, A. BORTOLOTTI, Emo-
tional Face Recognition, Empathic Trait (BEES),
and Cortical Contribution in Response to Positive
and Negative Cues. The Effect of rTMS on Dorsal
Medial Prefrontal Cortex, cit.
127
See M.L. HOFFMANN, Is Altruism Part of Hu-
man Nature?, cit.
128
See M. BALCONI, A. BORTOLOTTI, L. GONZAGA,
Emotional Face Recognition, EMG Response, and Me-
dial Prefrontal Activity in Empathic Behavior, cit.
129
See M. BALCONI, A. BORTOLOTTI, L. GON-
ZAGA, Emotional Face Recognition, EMG Response,
and Medial Prefrontal Activity in Empathic Behav-
ior, cit.; M. BALCONI, A. BORTOLOTTI, D.
CRIVELLI, Self-report Measures, Facial Feedback,
and Personality Differences (BEES) in Cooperative
vs. Noncooperative Situations, cit.; M. BALCONI, Y.
CANAVESIO, Emotional Contagion and Trait Em-
pathy in Prosocial Behavior in Young People, cit.
130
See M. BALCONI, A. BORTOLOTTI, Resonance
Mechanism in Empathic Behavior, cit.; M. BALCONI,
Empathy and Prosocial Behaviours
109
A. BORTOLOTTI, Empathy in Cooperative Versus
Non-cooperative Situations, cit.; M. BALCONI, A.
BORTOLOTTI, D. CRIVELLI, Self-report Measures,
Facial Feedback, and Personality Differences (BEES)
in Cooperative vs. Noncooperative Situations, cit.
131
See M. BALCONI, A. BORTOLOTTI, Resonance
Mechanism in Empathic Behavior, cit.
132
See T. ROMERO, M. ITO, A. SAITO, T. HASEG-
AWA, Social Modulation of Contagious Yawning in
Wolves, cit.
133
See S.D. PRESTON, F.B.M. DE WAAL, Empathy:
Its Ultimate and Proximate Bases, cit.
134
See E.A. MADSEN, T. PERSSON, S. SAYEHLI, S.
LENNINGER, G. SONESSON, Chimpanzees show a
Developmental Increase in Susceptibility to Conta-
gious Yawning, cit.
135
See T. ROMERO, M. ITO, A. SAITO, T. HASEG-
AWA, Social Modulation of Contagious Yawning in
Wolves, cit.
136
See PALAGI, E., LEONE, A., MANCINI, G.,
FERRARI, P.F. (2009), Contagious yawning in gela-
da baboons as a possible expression of empathy, cit.
137
See T. ROMERO, M. ITO, A. SAITO, T. HASEG-
AWA, Social Modulation of Contagious Yawning in
Wolves, cit.
138
See E.A. MADSEN, T. PERSSON, Contagious
Yawning in Domestic Dog Puppies (Canis lupus
familiaris), cit.; R.M. JOLY-MASCHERONI, A. SEN-
JU, A.J. SHEPHERD, Dogs Catch Human Yawns, cit.
139
See S.M. O’CONNELL, Empathy in Chimpan-
zees: Evidence for Theory of Mind?, cit.; A. CLYVIA,
M.C. KAIZER, R.V. SANTOS, R.J. YOUNG, C.
CÄSAR, Do Wild Titi Monkeys show Empathy?, cit.
140
See B. INBAL BAN-AMI, J. DECETY, P. MASON,
Empathy and Pro-Social Behavior in Rats, cit.
141
See D.J. LANGFORD, S.E. CRAGER, Z. SHEHEZAD,
S.B. SMITH, S.G. SOTOCINAL, Social Modulation of
Pain as Evidence for Empathy in Mice, cit.
142
See L.A. BATES, P.C. LEE, N. NJIRAINI, J.H.
POOLE, K. SAYIALEL, S. SAYIALEL, C.J. MOSS, R.W.
BYRNE, Do Elephants show Empathy?, cit.
143
See A. WILKINSON, N. SEBANZ, L. MANDL, L.
HUBER, No Evidence of Contagious Yawning in the
Red-footed Tortoise Geochelone carbonaria, cit.
144
See E.A. MADSEN, T. PERSSON, S. SAYEHLI, S.
LENNINGER, G. SONESSON, Chimpanzees show a
Developmental Increase in Susceptibility to Conta-
gious Yawning, cit.
145
See R.M. JOLY-MASCHERONI, A. SENJU, A.J.
SHEPHERD, Dogs Catch Human Yawns, cit.
146
See M. BALCONI, A. BORTOLOTTI, Resonance
Mechanism in Empathic Behavior, cit.; M. BALCO-
NI, A. BORTOLOTTI, Self-report, Personality and
Autonomic System Modulation in Response to Em-
pathic Conflictual versus Non conflictual Situation,
cit.; M. BALCONI, A. BORTOLOTTI, Empathy in
Cooperative Versus Non-cooperative Situations, cit.
147
See R.J. FRANKLIN JR., A.J. NELSON, M. BAKER,
J.E. BEENEY, T.K. VESCIO, A. LENZ-WATSON, R.G.
ADAMS JR., Neural Responses to Perceiving Suffer-
ing in Humans and Animals, cit.
148
See V. GALLESE, M.N. EAGLE, P. MIGONE, In-
tentional Attunement: Mirror Neurons and the
Neural Underpinnings of Interpersonal relations,
in: «Journal of the American Psychoanalytic As-
sociation», vol. LV, n. 1, 2007, pp. 131-175.
149
See S.M. O’CONNELL, Empathy in Chimpan-
zees: Evidence for Theory of Mind?, cit.
... At the same time, we find dog domestication as an active factor promoting human selfdomestication, as increased interspecific contacts are expected to have reinforced our trend toward enhanced prosociality (Jung and Pörtl, 2015. Current research shows that humandog relationships provoke similar patterns of brain activation in areas involved in reward, emotion, affiliation, and empathy than human-infant interactions, although some differences can be observed as well (see Vanutelli and Balconi, 2015 for review). Interestingly, as noted, domestication results in neotenic, childish features, which are expected to increase our affiliative and empathic responses, and ultimately, to promote our prosociality. ...
Article
Full-text available
Different factors seemingly account for the emergence of present-day languages in our species. Human self-domestication has been recently invoked as one important force favoring language complexity mostly via a cultural mechanism. Because our self-domestication ultimately resulted from selection for less aggressive behavior and increased prosocial behavior, any evolutionary or cultural change impacting on aggression levels is expected to have fostered this process. Here, we hypothesize about a parallel domestication of humans and dogs, and more specifically, about a positive effect of our interaction with dogs on human self-domestication, and ultimately, on aspects of language evolution, through the mechanisms involved in the control of aggression. We review evidence of diverse sort (ethological mostly, but also archeological, genetic, and physiological) supporting such an effect and propose some ways of testing our hypothesis.
... Nonetheless, observations made in both natural populations and in laboratory conditions are sometimes controversial. For example, as already The boundaries of cooperation: sharing and coupling from ethology to neuroscience reported in Vanutelli and Balconi (2015), although the growing interests in emotional and social lives of non-human animals, the presence of objective experimental evidence has just begun to emerge. A first interesting example is described in a paper by Church (1959) concerning rats' behaviors towards conspecifics in pain. ...
Article
Cooperation is usually described as a human tendency to act jointly that involves helping, sharing, and acting prosocially. Nonetheless clues of cooperative actions can be found also in non-humans animals, as described in the first section of the present work. Even if such behaviors have been conventionally attributed to the research of immediate benefits within the animal world, some recent experimental evidence highlighted that, in highly social species, the effects of cooperative actions on others' wellbeing may constitute a reward per se, thus suggesting that a strictly economic perspective can't exhaust the meaning of cooperative decisions in animals. Here we propose, in the second section, that a deeper explanation concerning cognitive and emotional abilities in both humans and animals should be taken into account. Finally, the last part of the paper will be devoted to the description of synchronization patterns in humans within complex neuroscientific experimental paradigms, such as hyperscanning.
Article
Full-text available
We observed a putative case of empathy among wild black-fronted titi monkeys (Callicebus nigrifrons) from two different groups (D and R). In over 10 years of behavioural observations of five habituated groups of this species, only low levels of inter-group tolerance have been observed. However, on one day, we encountered the adult male from group D limping (poor hind limb motor coordination) as he travelled alone along the ground. Interestingly, we observed that members of group R did not express any agonistic behaviour towards this neighbouring male and apparently allowed this disabled individual to follow them in the forest for over 5 h. They stayed low in the forest (< 2 m above the ground) and < 10 m horizontally from the individual, and remained in visual contact with him. At the end of the day, this male from group D slept in the sleeping site of group R and was groomed by the adult female of group R. Such tolerance between members of different groups has never been previously observed in this species. Furthermore, group R exposed themselves to increased predation risk by staying close to the ground for protracted periods. The behaviour of group R could be interpreted by as a putative case of empathic responding in this species.
Article
Full-text available
Neural substrates underlying the human-pet relationship are largely unknown. We examined fMRI brain activation patterns as mothers viewed images of their own child and dog and an unfamiliar child and dog. There was a common network of brain regions involved in emotion, reward, affiliation, visual processing and social cognition when mothers viewed images of both their child and dog. Viewing images of their child resulted in brain activity in the midbrain (ventral tegmental area/substantia nigra involved in reward/affiliation), while a more posterior cortical brain activation pattern involving fusiform gyrus (visual processing of faces and social cognition) characterized a mother's response to her dog. Mothers also rated images of their child and dog as eliciting similar levels of excitement (arousal) and pleasantness (valence), although the difference in the own vs. unfamiliar child comparison was larger than the own vs. unfamiliar dog comparison for arousal. Valence ratings of their dog were also positively correlated with ratings of the attachment to their dog. Although there are similarities in the perceived emotional experience and brain function associated with the mother-child and mother-dog bond, there are also key differences that may reflect variance in the evolutionary course and function of these relationships.
Article
Full-text available
On the basis of observational and experimental evidence, several authors have proposed that contagious yawn is linked to our capacity for empathy, thus presenting a powerful tool to explore the root of empathy in animal evolution. The evidence for the occurrence of contagious yawning and its link to empathy, however, is meagre outside primates and only recently domestic dogs have demonstrated this ability when exposed to human yawns. Since dogs are unusually skilful at reading human communicative behaviors, it is unclear whether this phenomenon is deeply rooted in the evolutionary history of mammals or evolved de novo in dogs as a result of domestication. Here we show that wolves are capable of yawn contagion, suggesting that such ability is a common ancestral trait shared by other mammalian taxa. Furthermore, the strength of the social bond between the model and the subject positively affected the frequency of contagious yawning, suggesting that in wolves the susceptibility of yawn contagion correlates with the level of emotional proximity. Moreover, female wolves showed a shorter reaction time than males when observing yawns of close associates, suggesting that females are more responsive to their social stimuli. These results are consistent with the claim that the mechanism underlying contagious yawning relates to the capacity for empathy and suggests that basic building blocks of empathy might be present in a wide range of species.
Article
Conventional wisdom over the past 160 years in the cognitive and neurosciences has assumed that brains evolved to process factual information about the world. Most attention has therefore been focused on such features as pattern recognition, color vision, and speech perception. By extension, it was assumed that brains evolved to deal with essentially ecological problem-solving tasks. 1.
Article
Background: Little is known about the regional brain basis of human maternal behavior. To understand this better, we have been examining brain activity in mothers listening to infant cries. Methods: We measured functional Magnetic Resonance Imaging brain activity in healthy, breastfeeding first-time mothers with young infants while they listened to infant cries, white noise control sounds, and a rest condition. Based on the thalamocingulate theory of maternal behavior and pilot work, we hypothesized that the cingulate, medial thalamus, medial prefrontal cortex, and right orbitofrontal cortex would display more activity with infant cries than with white noise (comparison 1) and would uniquely activate with the cries, meaning that these regions would display activity with cry minus rest but not with white noise minus rest (comparison 2). Results: In hypothesized regions, the group displayed more activity in the medial thalamus, medial prefrontal and right orbitofrontal cortices with both comparisons. The anterior and posterior cingulate cortex displayed more activity only with comparison 1. In non-hypothesized brain regions, several other structures thought important in rodent maternal behavior displayed activity with both comparisons including the midbrain, hypothalamus, dorsal and ventral striatum, and vicinity of the lateral septal region. Conclusions: Our results partially support our hypotheses and are generally consistent with neuroanatomical studies of rodent maternal behavior.