Abtsract: Watching someone scratch
himself can induce feelings of itchiness in the
perceiver. This provides a unique opportunity to
characterize the neural basis of subjective
experiences of itch, independent of changes in
peripheral inputs. In this study, we first
established that the social contagion of itch is
essentially a normative response (experienced by
most people), and that the degree of contagion
is related to trait differences in neuroticism
(i.e., the tendency to experience negative
emotions), but not to empathy. Watching video
clips of someone scratching (relative to control
videos of tapping) activated, as indicated by
functional neuroimaging, many of the neural
regions linked to the physical perception of
itch, including anterior insular, primary
somatosensory, and prefrontal (BA44) and
premotor cortices. Moreover, activity in the
left BA44, BA6, and primary somatosensory cortex
was correlated with subjective ratings of
itchiness, and the responsivity of the left BA44
reflected individual differences in neuroticism.
Our findings highlight the central neural
generation of the subjective experience of
somatosensory perception in the absence of
somatosensory stimulation. We speculate that the
habitual activation of this central "itch
matrix" may give rise to psychogenic itch
disorders.
Ward
J, Burckhardt V, Holle H. Contagious
scratching: shared feelings but not shared body
locations. Front Hum Neurosci. 2013
Itch is to some degree socially contagious.
Subjective feelings of itchiness and observable
increases in scratching can be evoked by
watching someone scratch himself or by listening
to a lecture on dermatologic conditions (1, 2).
Although many aspects of the neurobiology of
itch are now appreciated (3, 4), the standard
definition of itch ("an unpleasant sensation
associated with an urge to scratch") and its
description as a symptom within clinical
disorders remain essentially subjective and
based on self-report. The study of the neural
basis of contagious itch presents a unique
opportunity to explore the neural basis of
subjective itch experience that is dissociated
from the normal peripheral inputs.
Functional neuroimaging investigations of
itch [predominantly functional MRI
(fMRI)] typically use an invasive, localized
administration of histamine to induce itch
(5-8). This approach has revealed the engagement
of a network of regions (the so-called "itch
matrix") that includes the anterior insula,
cingulate cortex, primary somatosensory cortex,
premotor cortex, prefrontal cortex, thalamus,
and cerebellum. Within this network, there is
functional specialization that reflects the
multifaceted nature of itch (i.e., its sensory,
motor, and affective attributes), with the
proposal that anterior insula and cingulate
cortex may code the affective components of itch
(4). Of note, these regions are also linked to
the processing of (and awareness of)
interoceptive bodily signals, including pain,
cardiovascular activity, and hunger (9, 10).
These internal signals are motivationally
salient, and thus their representation may
correspondingly engender an urge for action
(11)&emdash;that is, scratching in the case of
itch.
The planning of scratching movements is
linked to premotor activity, whereas the
intention to scratch (or not) is linked to
engagement of the prefrontal cortex (12),
consistent with this area's recognized role in
willed actions (13). Primary and secondary
somatosensory cortices have been proposed to
support the sensory (i.e., spatial, temporal,
and intensity) aspects of the experience (4);
however, activity within almost all parts of the
itch matrix is correlated with subjective
ratings of itch intensity (5, 6, 14), suggesting
interdependence of the sensory, motor, and
affective components of itch. Previous fMRI
studies were constrained by the methodological
limitation that the experience of
histamine-induced itch emerges rather slowly,
taking approximately 1 min to reach peak
intensity after onset of infusion (5), followed
by a slow decay.
This time course means that little of the
moment-to-moment fluctuation in subjective
itchiness can be related to evoked changes in
brain activity, constraining analytic power. We
show that visual induction of itch does not
suffer from this limitation. Although no
previous study has examined the neural
correlates of visually induced itch, several
researchers have suggested that the "mirror
neuron system" may be essential for contagious
itching (2, 4).Mirror neurons, first reported in
the macaque brain, respond to both a
self-executed action and the sight of an action
performed by another person (15). In macaques,
mirror neuron-containing regions include the
premotor and inferior frontal cortices and
inferior parietal lobe (16). Neurons with
similar properties have been observed in the
human brain as well (17). In humans, this system
may extend beyond action perception to
perception of feeling states. For instance, Carr
et al. (18) suggested that viewing a facial
expression activates emotion-related parts of
the brain via the motor-based mirror system, and
that this could be the neural basis of empathy
(19). There is compelling evidence linking
empathy with some forms of emotional or
behavioral "contagion" (20, 21), although
contagious itch has not been considered in any
previous studies. However, some studies did not
implicate actionbased mirror systems as the
interface between perception and feeling (22,
23), but suggested instead that feeling states
can be shared without obligatory motor
simulation.
Discussion
The first important finding of the present
study is that on a behavioral level, social
contagion of itch is a normative response (i.e.,
experienced by most people). When participants
were free to scratch, most (64%) did so at least
once. This puts itch on a par with other types
of socially contagious behavior, including
laughter (47%; ref. 27) and yawning (40-60%;
refs. 21, 28). Furthermore, participants who
experienced stronger feelings of itchiness
during the experiment also tended to
spontaneously scratch themselves more often when
free to do so, indicating a correspondence
between self-report and observable behavior. Our
findings characterize the central neural
substrates mediating the social contagion of
itch by identifying regions that support the
subjective experience of itch. Importantly,
observing itch activated the same set of brain
regions associated with feelings of itch induced
by an irritant, such as histamine (5-7). This
shared network includes the anterior insula,
premotor cortex, primary somatosensory cortex,
and prefrontal cortex. One region not activated
in our study but typically activated by chemical
induction of itch is the midcingulate cortex,
although not all studies of itch have reported
activity here (14, 29). The magnitude of
activation across this "itch matrix" reflects
the main effect of viewing itch-related videos
(relative to non-itch control stimuli), and
tends to correlate with the subjective intensity
of itchiness reported for these stimuli.
There is good evidence that the anterior
insula is a core node in the network for shared
pain (reviewed in ref. 23), and our results
demonstrate that itch may be shared in the
anterior insula as well. Furthermore, the
response in the right anterior insula was
sustained throughout the duration of the
stimulus, in contrast to most other regions,
which displayed a strong response in the early
phase only. The (right) anterior insula is part
of a tightly connected neural network engaged in
interoceptive awareness (30), that is,
representation of motivationally salient
subjective feelings related to the body's
internal state, including C-fiber-mediated
sensations such as itch, tickle, and visceral
pain (31). These insular bodily representations
may subserve at least two functions relevant to
contagious itch. First, the anterior insula may
act as a comparator in a predictive coding model
of interoception, according to which subjective
feeling states arise from top-down predictions
of interoceptive signals (32). Second, these
predictive representations may allow simulation
of how a specific stimulus feels to others (33).
Combining these views, anterior insula activity
thus may be related to sharing the unpleasant
bodily sensations that accompany itch.
Several of the brain regions linked to
contagious itch are implicated in the simulation
of actions (mirror systems), including the
premotor cortex (BA6) and adjacent BA44 (34,
35). The primary somatosensory cortex (BA2) is
also commonly activated during action
observation (34), but also plausibly could code
the sensory aspects of itch. In all three of
these regions, activity was greatest in the
earlier half of the stimulus presentation. This
is more consistent with involvement of these
regions in the perception of itch than in, say,
the generation of scratching urges. The latter
would be expected to build up over the duration
of the stimulus (although we did not explicitly
measure how the subjective experience unfolds
over time). However, each of these regions
likely has a relatively different functional
contribution that remains to be fully
elucidated. The area of activity in primary
somatosensory cortex lies in the left hemisphere
hand area (36), suggesting that it may code the
sensory effects of scratching (rather than the
location being scratched). Along with a role in
the simulation of actions, the premotor cortex
also responds to somatosensory stimuli (37-39)
and the sight of touch (40-42); thus, in
principle, its role also may be sensory-based
rather than action-based. However, premotor and
somatosensory cortices differ in the degree to
which they are also activated by the control
condition of tapping. The premotor region does
not respond to this control action relative to
fixation, whereas somatosensory cortex does
respond.
This could reflect different motoric demands
that affect primarily the premotor cortex; for
example, scratching requires complex
manipulation of fingers, but tapping is a far
simpler wrist-based action. Itch-related
activity in the left BA44 is correlated with
neuroticism, and neuroticism itself has been
identified as the sole reliable trait predictor
of individual differences in subjective feelings
of itch contagion. This trait is known to
exacerbate certain clinical symptoms, such as
chronic pain (43), and is a predisposing
influence in various psychopathologies (44). The
importance of neuroticism as opposed to empathy
might reflect a key difference between the
social processing of itch versus pain that may
originate in distinct motivational biases toward
social proximity (pain) or distance (itch). The
prefrontal cortex is generally implicated in the
control of cognition and behavior, and in the
present context it may serve a gating
(attention-related) function that modulates the
degree of contagion. Finally, some patients
report persistent itch sensations (often
accompanied by a belief of infestation) but
appear dermatologically normal (45). It is
likely that the same central mechanisms
responsible for itch sensations induced by
observing itch in others (an essentially
normative response) is responsible for itch
induced by self-generated thoughts of itching or
infestation (which may become established as
dominant overvalued representations in a
minority of persons). Individual differences
within this network, also related to personality
traits, may modulate the extent to which this
contagion is triggered by environmental cues
versus occurring spontaneously and habitually
(46, 47). Further research is warranted to
explore the link between contagious itching and
compulsive itching.
