Rats responded to air tickling (a hand with tickling motion) with USVs, suggesting an anticipation of tickling. One could argue whether the response to witnessed tickling is merely an anticipatory response to the hand, rather than playfulness contagion. We consider that the observers’ response to witnessed tickling is not a response just to the hand because the observers responded also to demonstrators’ spontaneous behaviors such as jump and USVs when the experimenter’s hand was not in the demonstrator compartment ( Figures 1 J and 1K). Because air tickling was administered shortly after direct tickling ( Figure 1 B), the rats were already vocalizing prior to air tickling, which would overestimate the effect of air tickling ( Figure 1 E). In contrast, the demonstrator was tickled a long time after direct tickling, and even after playback of tickling, which would have led to an underestimation of the response to witnessed tickling when compared with air tickling.
We found that the observer rat showed little behavioral response to audio and/or visual playback of tickling footage ( Figures 1 F–1H) but more to the live demonstrator rat being tickled suggesting vicarious playfulness. It is remarkable that playfulness contagion is not merely carried by the sound and vision, but it requires the presence of a live demonstrator. In fact, we occasionally noticed that the observers were sleeping during playback. Yet, it remains to be tested how differently playback and live demonstration of play lead to an increase in play behavior in observer animals. Our experimental setup ( Figure 1 A) had a partition with metal mesh at the bottom so that the rats could smell each other. The striking difference in the behavioral responses to witnessing live vs. audio/visual playback tickling may suggest an important role of olfactory components in playfulness contagion.
We verified our previous resultsthat rats show a neuronal and behavioral response to tickling. Playful rats showed interest in the conspecifics being tickled. Fifty-kHz USVs are reliable measures of positive emotions in ratsand Freudensprünge are described as a behavior that is seen in joyful ratsand other species including piglets,dogs,foxes,and guinea pigs.We found such playful behaviors in the observer rat witnessing the demonstrator rat being tickled, demonstrator jump, and demonstrator USVs, pointing to an emotional contagion of playfulness. This kind of playfulness contagion has been observed also in other species, such as ravensand keas.Contagion of laughter has been suggested in humansand chimpanzees.Several studies on rats showed an increase in play by introduction of a more playful individualand tickling-induced emotional contagion from a tickled rat to their cage mate.Devocalized pairs of rats show reduced play frequency.Artificially deafened but not blinded ratsplay less than their conspecifics.
Are 50-khz calls used as play signals in the playful interactions of rats? III. The effects of devocalization on play with unfamiliar partners as juveniles and as adults.
Cortical response to witnessed tickling and anticipatory response
28 Ishiyama S.
Brecht M. Neural correlates of ticklishness in the rat somatosensory cortex. 29 Ishiyama S.
Kaufmann L.V.
Brecht M. Behavioral and cortical correlates of self-suppression, anticipation, and ambivalence in rat tickling. 46 Pezzulo G.
Hoffmann J.
Falcone R. Anticipation and anticipatory behavior. , 47 Maldonato M.
Dell’Orco S. Mirror neurons and the predictive mind. , 48 Gallese V.
Goldman A. Mirror neurons and the simulation theory of mind-reading. , 49 Gallese V. Mirror neurons, embodied simulation, and the neural basis of social identification. 50 Anderson D.J.
Adolphs R. A framework for studying emotions across species. Next, we found that trunk somatosensory neurons responded to both direct and witnessed tickling ( Figure 2 ), suggesting that somatosensory cortex represents playfulness contagion, or possibly “tickling mirror-like” neurons. Moreover, this neuronal response was associated with positive emotional behavior ( Figure 1 I). Many units that responded to direct tickling were also excited by air tickling ( Figures 2 H, 2J, and S4 ), however. Responses to air tickling and witnessed tickling were considerably smaller than response to direct tickling ( Figure S3 ). Accordingly, it seems also possible that these units responded rather to the expectancy of being tickled than the observed tickling act itself, and we think this possibility cannot be fully excluded. In fact, individual neurons that were strongly activated during witnessing tickling certainly gave the impression of true “mirroring”. The most likely expectancy-driven responses seen in control conditions (air tickling) leave us unable to decide whether at the population level our responses represent true mirroring or play expectancy. Previous studies also found that somatosensory neurons fire in response to expected tickling during hand chaseand slow hand approach.We note that few mirroring studies used the type of strong control conditions that we applied (air tickling) and that further work may help to differentiate mirroring and (play-)expectancy. Yet, there is precedent to the idea that the mirror neuron system implements anticipatory and simulative capabilities, i.e. an internal simulation and anticipation of the consequences of an action.Anderson & Adolphsemphasized that persistence is a characteristic feature of emotional processing in comparison with other sensory processings. Activity of trunk somatosensory neurons, particularly the direct-tickle respondents ( Figure 2 ), increased during direct tickling, decreased but remained elevated from the baseline during break, and increased by witnessing tickling. This persistence and revoking in the activity without a tactile stimulus could be better explained as emotional processing, rather than tactile processing. Previous experience of being tickled might also play a role in tickle contagion. Thus, experiments using tickle-naïve observer rats would be of interest to test whether ticklishness is innate or acquired. We conclude that somatosensory cortical neurons show strong visual responses that are driven by a mirroring or play-expectancy mechanism and that contribute to tickle contagion.
51 Brecht M. The body model theory of somatosensory cortex. 29 Ishiyama S.
Kaufmann L.V.
Brecht M. Behavioral and cortical correlates of self-suppression, anticipation, and ambivalence in rat tickling. 28 Ishiyama S.
Brecht M. Neural correlates of ticklishness in the rat somatosensory cortex. We found that the correlation between the direct and the witnessed tickling response was stronger in deep layers compared to superficial layers ( Figure 4 ). Traditionally, the somatosensory cortex is seen as a sensory map with layer 4 being a sensory relay center, but recently we proposed a broader capability of the somatosensory system as a body model that is not only receiving and relaying sensory inputs but serves as a representation of the body and body simulation.We previously showed that discharge of layer 4 trunk somatosensory neurons is sharply aligned to the onset of tickling, whereas layer 5 plays a role in anticipation of tickling i.e. activation prior to tickling onset.Layer 5 neurons also show strong responses during tickling, and microstimulation of deep layers evokes USVs.The role of deep layers of the trunk somatosensory cortex in tickling and witnessing tickling could indicate that the deep layers are more related to emotional states. Interestingly, laminar pattern of correlation of direct tickling and air tickling response ( Figure S5 ) as well as correlation of witnessed tickling and air tickling ( Figure S6 ) was different from that of direct and witnessed tickling, which might suggest different mechanisms underlying direct, air, and witnessed tickling responses.
28 Ishiyama S.
Brecht M. Neural correlates of ticklishness in the rat somatosensory cortex. 52 Berz A.C.
Wöhr M.
Schwarting R.K.W. Response calls evoked by playback of natural 50-kHz ultrasonic vocalizations in rats. 53 Wöhr M.
Schwarting R.K.W. Ultrasonic communication in rats: can playback of 50-kHz calls induce approach behavior?. 54 Sadananda M.
Wöhr M.
Schwarting R.K.W. Playback of 22-kHz and 50-kHz ultrasonic vocalizations induces differential c-fos expression in rat brain. In line with a previous report,trunk somatosensory neurons discharged upon vocal emission ( Figure 5 ). The neurons weakly yet significantly responded also to USVs emitted by the demonstrator rats during break phases i.e. out of tickling. Playback of 50-kHz USVs is reported to induce response calls,social approach,and increased c-fos expression in the frontal cortex and the nucleus accumbens.Whereas our audio playback experiment did not induce observer’s response, USVs emitted by the live demonstrator out of tickling led to USV emission ( Figure 1 K) and activation of trunk somatosensory cortex ( Figure 5 ) in the observer animals. These results further support that the behavioral and neuronal response to vicarious tickling is a response not only to the hand but also to the exhilarated emotional state of the demonstrator rats. Yet, our conclusion is limited to the observation of the somatosensory cortex. We do not know to what extent the trunk somatosensory cortex has a role in emotional contagion, given that many other brain regions play a more prominent role in emotions than the somatosensory cortex. Thus, further work including investigation of other brain areas is needed to understand this interesting behavior.
55 Kohler E.
Keysers C.
Umiltà M.A.
Fogassi L.
Gallese V.
Rizzolatti G. Hearing sounds, understanding actions: action representation in mirror neurons. , 56 Keysers C.
Kohler E.
Umiltà M.A.
Nanetti L.
Fogassi L.
Gallese V. Audiovisual mirror neurons and action recognition. 57 Gazzola V.
Aziz-Zadeh L.
Keysers C. Empathy and the somatotopic auditory mirror system in humans. 58 Gharaei S.
Honnuraiah S.
Arabzadeh E.
Stuart G.J. Superior colliculus modulates cortical coding of somatosensory information. 59 Burn C.C. What is it like to be a rat? Rat sensory perception and its implications for experimental design and rat welfare. Trunk somatosensory neurons showed little if not no response to the audio and/or visual playback of conspecific tickling ( Figure S4 ). There are actually many accounts of modality-specific mirror neurons. At least two studies found auditory mirror neurons in macaques,and neuroimaging in humans led to the proposition of a somatotopic auditory mirror system. Most of this proposed system, however, appears to be multimodal.Recently, a study revealed modulation of the barrel cortex by the superior colliculus in mice.Regarding the rat ecology as nocturnal and rats as not very visual animals that are prey for a number of hunters and rely more on their hearing and olfaction,more cells might respond to auditory stimuli, or these responses could be stronger than responses to other sensory inputs. Anatomical tracing experiments could potentially reveal more about multisensory integration in the somatosensory cortex.
60 Vielle C.
Montanari C.
Pelloux Y.
BAUNEZ C. Evidence for a vocal signature in the rat and its reinforcing effects. 61 Gonzalez-Liencres C.
Juckel G.
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Friebe A.
Brüne M. Emotional contagion in mice: the role of familiarity. , 62 Rogers-Carter M.M.
Djerdjaj A.
Culp A.R.
Elbaz J.A.
Christianson J.P. Familiarity modulates social approach toward stressed conspecifics in female rats. , 63 Cox S.S.
Reichel C.M. Rats display empathic behavior independent of the opportunity for social interaction. , 64 Langford D.J.
Crager S.E.
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Smith S.B.
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Levitin D.J.
Mogil J.S. Social modulation of pain as evidence for empathy in mice. A recent study demonstrated that rats distinguish a USV emitter, and they self-administer preferentially playback of 50-kHz USVs emitted by a stranger rat over those emitted by their cage mate.We used playback footage of a rat that was a stranger to the observers, whereas the live demonstrators were familiar to the observers. Using live demonstration of a stranger rat, therefore, might have been a more rewarding stimulus to the observer rats. It is to be noted, however, that familiarity with the demonstrator is crucial in empathetic behavior of the observer in rodents, at least for negative experiences.
21 Carrillo M.
Han Y.
Migliorati F.
Liu M.
Gazzola V.
Keysers C. Emotional mirror neurons in the rat's anterior cingulate cortex. 65 Andraka K.
Kondrakiewicz K.
Rojek-Sito K.
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et al. Distinct circuits in rat central amygdala for defensive behaviors evoked by socially signaled imminent versus remote danger. , 66 Keysers C.
Gazzola V. Emotional contagion: improving survival by preparing for socially sensed threats. 22 Adolphs R.
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Damasio A.R. A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping. , 67 Pitcher D.
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Duchaine B.C. Transcranial magnetic stimulation disrupts the perception and embodiment of facial expressions. 68 Adolphs R. Neural systems for recognizing emotion. , 69 Banissy M.J.
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Scott S.K. Suppressing sensorimotor activity modulates the discrimination of auditory emotions but not speaker identity. 23 Kragel P.A.
LaBar K.S. Somatosensory representations link the perception of emotional expressions and sensory experience. Carrillo et al. showed that there are emotional mirror neurons in the rat anterior cingulate cortex.The central amygdala also appears to be involved in the recognition and emotional contagion of socially signaled danger.It is likely that the response to direct and witnessed tickling that we observed in the somatosensory cortex neurons was strongly influenced by or dependent on the positive emotional valence of the tickling. Interestingly, a number of studies report that the recognition of emotional expression in facesand voicesdepends on the right somatosensory cortex in humans. Furthermore, it has been proposed that the somatosensory cortex plays a role in linking the perception of emotional expressions with subjective sensory experience.