Contagious yawning, emotional contagion and
empathy are characterized by the activation of
similar neurophysiological states or responses
in an observed individual and an observer. For
example, it is hard to keep one's mouth closed
when imagining someone yawning, or not feeling
distressed while observing other individuals
perceiving pain. The evolutionary origin of
these widespread phenomena is unclear, since a
direct benefit is not always apparent.
The authors explore a game theoretical model
for the evolution of mind-reading strategies,
used to predict and respond to others' behavior.
In particular we explore the evolutionary
scenarios favoring simulative strategies, which
recruit overlapping neural circuits when
performing as well as when observing a specific
behavior.
They show that these mechanisms are
advantageous in complex environments, by
allowing an observer to use information about
its own behavior to interpret that of others.
However, without inhibition of the recruited
neural circuits, the observer would perform the
corresponding downstream action, rather than
produce the appropriate social response.
They identify evolutionary trade-offs that
could hinder this inhibition, leading to
emotional contagion as a by-product of
mind-reading. The interaction of this model with
kinship is complex. They show that empathy
likely evolved in a scenario where kin- and
other indirect benefits co-opt strategies
originally evolved for mind-reading, and that
this model explains observed patterns of
emotional contagion with kin or group
members.
Réumé
Le bâillement contagieux, la contagion
émotionnelle et l'empathie se
caractérisent par l'activation
d'états ou de réponses
neurophysiologiques similaires chez un individu
observé et un observateur. Par exemple,
il est difficile de garder la bouche
fermée lorsque vous percevez quelqu'un
bâiller. De même vous vous sentez
angoissé lorsque vous observez d'autres
personnes percevoir une douleur. L'origine
évolutive de ces phénomènes
ubiquitaires n'est pas claire, car le
bénéfice direct n'est pas toujours
perceptible.
Les auteurs explorent un modèle
théorique de jeu afin d'évaluer
l'évolution des stratégies de
décodage de l'intentionnalité,
utilisées pour prédire et
réagir au comportement des autres. Ils
explorent, en particulier, les scénarios
privilégiant les stratégies de
simulation, qui recrutent des circuits neuronaux
communs lors de l'action et lorsqu'un
comportement spécifique est
observé.
Ils montrent que ces mécanismes sont
avantageux dans des environnements complexes, en
permettant à un observateur d'utiliser
les informations relatives à son propre
comportement pour interpréter celui des
autres. Cependant, sans inhibition des circuits
neuronaux recrutés, l'observateur
effectuerait l'action en aval correspondante
plutôt que de produire la réponse
sociale appropriée. Ils identifient des
compromis évolutifs qui pourraient
empêcher cette inhibition, menant à
la contagion émotionnelle en tant que
conséquence de la lecture de
l'intentionnalité.
L'interaction de ce modèle avec la
réalité est complexe. Ils montrent
que l'empathie a probablement
évolué suivant un schéma
où les stratégies de
mimétisme ont des avantages indirects
pour la vue sociale et que ces derniers ont
autorisé l'émergence de la
capacité à décoder
l'intentionnalité. Ce modèle donne
une explication à la contagion
émotionnelle observés au sein
d'une famille ou d'un groupe.
Introduction
Learning enables organisms to adapt flexibly
to their environment without waiting for natural
selection to take its long and arduous route.
However, the more complex the environment, the
slower the adaptive gain from either learning or
evolution. One of the most complex and relevant
environments that organisms encounter is the
social milieu. Here individuals are presented
with a multitude of other individuals, each with
a complex adaptive responses. Predicting these
"black boxes", a process called mind-reading1,
is hard. Thus accurate social predictions would
require a long adaptive process, requiring
accurate information about each perceived
stimulus and the possible responses. Luckily a
shortcut is available: the organism holds an
almost identical copy of the "black box" - its
own decision making apparatus or neural
circuitry, which can be used to extrapolate
inferences concerning others' behavior.
Information acquired over evolutionary time and
information acquired through individual learning
can thus be used to speed up adaptation to
social encounters.
Since the discovery of mirror neurons, a
large number of neurophysiological studies have
shown that similar brain regions are activated
when observing and when performing a specific
action, or perceiving a given emotional or
sensory stimulus. These mirroring phenomena
supported the view that an observer can decipher
an actor's actions and states through at least a
partial simulation of those same neural circuits
and internal states elicited as an actor, in
what de Waal termed "perception-action
mechanisms" PAMs. Neuroscientists proposed that
these brain regions, activated both as observers
or as actors, possibly underlie "shared
representations" of the perceived stimuli and
actions. For an observer, a potential advantage
of activating the as-actor neural configuration
is to have access to information about one's own
sensory and motor programs. In the social
context this information might help to interpret
social cues and infer an observed actor's
actions or intentions12, allowing to solve the
complex "black box" problem. We adopt here the
term "simulation" to indicate any mind-reading
strategy that relies on self-information
experienced as an actor, rather than information
acquired via observation of others.
Simulative strategies face possible
disadvantages and computational obstacles: the
secondary activation of as-actor neural circuits
during observation has to be discriminated
precisely from primary activations of the same
circuits when performing the corresponding
action oneself. Otherwise, the partial
activation of neural configuration which are
usually used in the as-actor context may prime
the corresponding autonomic and somatic
responses, and unless properly inhibited would
then evoke in the observer the responses of an
actor. We define these events in which a
simulative observer performs the same action as
an observed actor as accidental coordination. A
pathological lack of inhibition results in
compulsive imitation, as in echopraxia and
echolalia, the involuntary repetition of others'
actions or language, respectively. In specific
situations, accidental coordination can be
advantageous. However in the context of
mind-reading and social interactions,
individuals are often characterized by different
states or competing motivations, thus for an
observer it is generally not advantageous to
copy blindly the action of an observed actor.
The potential cost of accidental coordination is
two-folded: first, it hinders the observer from
performing the most appropriate response to an
actor's behavior; second, it might imply further
specific costs: for instance, contagious
distress can interfere with an optimal decision
making, and potentially lead to costly actions,
such as alarm calls or aggressive behavior. A
well documented example, in which the first
inherent cost is apparent, is motor
interference, in which the observation of a
movement impairs the performance of an
incongruent movement in the observer. For this
reason, the inhibition of accidental
coordination is likely shaped by natural
selection, and of primary importance in
mind-reading and mirroring processes.
We suggest that the two mechanisms could be
phylogenetically related. Simulative strategies,
by recruiting the as-actor network, provide a
simple proximate mechanism to synchronize the
actions of an observer to the internal and
motivational states of a recipient individual.
Our model shows that the recruitment of the
as-actor network and coordination increase when
cooperation is promoted by assortment. Thus
simulative strategies, evolved initially for
mind-reading, could be have been later coopted
for empathy and cooperation. A potential
criticism is that a coordination of internal
states and emotional responses is not
sufficient, and may even hinder, cooperation.
For example, it has been observed that
contagious distress might undermine helping
behavior. However, we showed that coordination
can evolve even when it is not the best possible
cooperative response: coordination offers an
evolutionary compromise, by synchronizing the
internal state of an observer with that of an
actor, and reducing the degrees of freedom for
possible responses. For example, the perception
of distress in the offspring elicits alertness
in parents. From this rudimentary form of
state-matching empathy, the activation of shared
representations of pain or distress could have
evolved to elicit prosocial responses,
concurrently with the role of oxytocin in
reducing avoidance responses triggered by
distress. This is supported by the evidence that
the activation of stress-related responses in
the observer often accompanies empathy and
cooperation.
It has been proposed that parental care
played a key role for the evolution of empathy.
Our model is consistent with this hypothesis,
since parental care would provide both a
selective pressure for cooperation and the
understanding of the needs of the offspring.
However, mind-reading benefits are not
restricted to parental care, and in the spectrum
of social complexity, parent-offspring
interactions are relatively simple: because of
their limited interaction with the environment,
the behavior of offspring is mostly evolved as
opposed to learned. Accordingly, instances of
parental care exist throughout the animal world
even in the absence of apparent empathy (e.g.
eggs brooding, ritualized parental cares). Thus,
even though we cannot rule out that in mammals
parental care provided the sufficient complexity
to render simulative strategies adaptive, we
suggest that simulative strategies might have
evolved for mind-reading in a more general
social context. Only later, might kin selection
have coopted them for cooperation, or emotional
contagion when coordination is advantageous.
These conclusions are supported by
neurophysiological evidence, showing that the
recruitment of the as-actor network extends
beyond the cooperative context; and behavioral
studies, showing that contagion in
non-cooperative context (e.g. contagious
yawning, facial mimicry) is stronger with kin
and unrelated but socially close individuals,
with whom empathy and helping behavior (e.g.
consolation) are stronger.
Future perspectives
Our model suggests potential directions for
new empirical studies, that would allow to test
some of its predictions. For example, we predict
that simulative strategies are more advantageous
in unpredictable environments. While empirical
evidence seems to support the presence of
empathy especially in primates and other
mammals, a better characterization of the
species in which empathy is present would
improve this picture. In addition, more studies
are needed both at the intra-specific and
inter-specific level to assess whether
perspective-taking skills correlate with
emotional contagion and empathy driven
cooperation. Do species or individuals who
simulate more also show more empathy driven
cooperation?
We also showed that specific features of
cognitive processes involved in mind-reading
would be necessary and favour the evolution of
accidental coordination. Thus, more studies
would help to clarify when these conditions
apply. For instance, we showed that accidental
coordination is favored when inhibitory
mechanisms incur the risk of false positives -
inhibiting off-target actions. Thus, studies
investigating the specificity of inhibitory
mechanisms would be precious to clarify the role
of the B-vs-C trade-off. Furthermore, more
studies would be beneficial in assessing the
role and the extent to what as-actor network
circuits are necessary for inferences, for
example in the case of mirror neurons.
Concluding, the characterization of inhibition
mechanisms and their specificity at the
neurophysiological level will certainly help to
understand whether and to what extent accidental
coordination contributes to prosocial behavior
in different species.
Conclusions
Our model explores a simple assumption, that
experience as actor can be useful to predict and
interpret others' actions, and shows that this
has relevant implications and side-effects.
First, we show that strategies relying on this
source information can evolve under many
circumstances. Second, we show that a side
effect of the evolution of such strategies is
that an observers could fail to inhibit the
observed behavior coordinating with the state
and actions of the observed actors. These two
phenomena provide us with a simple unified
perspective on biological phenomena as different
as mirror neurons, motor interference,
contagious yawning, contagious distress and
empathy, and their higher stronger effects with
kin. Many other biological pathological and non
pathological behaviors could possibly be
connected. For example, the comorbidity of
alexythymia and autism had already been
interpreted as the inability to understand
others as a consequence of the impaired
awareness of one's own feelings. The fact that
information and neural circuits acquired as an
actor are used to interpret others' actions is
also apparent for sensory stimuli in the
activation of the somatosensory cortex; for
stimuli of different nature in phenomena like
mirror touch synesthesia; and possibly even for
collective inferences and abstract concepts and
for inanimate or inter-specific entities (e.g.
anthropocentrism). Furthermore, the role of
inhibition of the activation of the as-actor
network to interpret others' actions is apparent
in pathologies like echopraxia and echolalia. As
an actor's cognition is embodied, even an
observer's cognition is required to be embodied,
despite the risk of accidental coordination10.
Concluding, the importance of information
acquired as an actor, either learned or evolved,
is pivotal to understand social cognition and
its evolution.
