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Resolving a ticklish problem

What is the neural correlate of ticklishness? When Ishiyama and Brecht tickled rats, the animals produced noises and other joyful responses. During the tickling, the authors observed nerve cell activity in deep layers of the somatosensory cortex corresponding to the animals' trunks. Furthermore, microstimulation of this brain region evoked the same behavior. Just as in humans, mood could modulate this neuronal activity. Anxiety-inducing situations suppressed the cells' firing, and the animal could no longer be tickled.
Science, this issue p. 757

Abstract

Rats emit ultrasonic vocalizations in response to tickling by humans. Tickling is rewarding through dopaminergic mechanisms, but the function and neural correlates of ticklishness are unknown. We confirmed that tickling of rats evoked vocalizations, approach, and unsolicited jumps (Freudensprünge). Recordings in the trunk region of the rat somatosensory cortex showed intense tickling-evoked activity in most neurons, whereas a minority of cells were suppressed by tickling. Tickling responses predicted nontactile neural responses to play behaviors, which suggests a neuronal link between tickling and play. Anxiogenic conditions suppressed tickling-evoked vocalizations and trunk cortex activity. Deep-layer trunk cortex neurons discharged during vocalizations, and deep-layer microstimulation evoked vocalizations. Our findings provide evidence for deep-layer trunk cortex activity as a neural correlate of ticklishness.
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References and Notes

1
Hall G. S., Alliń A., The psychology of tickling, laughing, and the comic. Am. J. Psychol. 9, 1–41 (1897).
2
Aristotle, On the Parts of Animals, W. Ogle, trans. (K. Paul, Trench & Co., London, 1882).
3
Harris C. R., The mystery of ticklish laughter. Am. Sci. 87, 344–351 (1999).
4
C. Darwin, The Expressions of the Emotions in Man and Animals (John Murray, London, 1872).
5
E. Hecker, Die Physiologie und Psychologie des Lachens und des Komischen (Ferd. Dümmlers Verlags, Berlin, 1873).
6
Harris C. R., Christenfeld N., Humour, tickle, and the Darwin-Hecker hypothesis. Cogn. Emotion 11, 103–110 (1997).
7
J. Panksepp, J. Burgdorf, in Toward a Science of Consciousness III, S. R. Hameroff, D. Chalmers, A. W. Kaszniak, Eds. (MIT Press, 1999), pp. 231–244.
8
Panksepp J., Burgdorf J., “Laughing” rats and the evolutionary antecedents of human joy? Physiol. Behav. 79, 533–547 (2003).
9
Blakemore S. J., Wolpert D. M., Frith C. D., Central cancellation of self-produced tickle sensation. Nat. Neurosci. 1, 635–640 (1998).
10
Wattendorf E., Westermann B., Fiedler K., Kaza E., Lotze M., Celio M. R., Exploration of the neural correlates of ticklish laughter by functional magnetic resonance imaging. Cereb. Cortex 23, 1280–1289 (2013).
11
Knutson B., Burgdorf J., Panksepp J., Ultrasonic vocalizations as indices of affective states in rats. Psychol. Bull. 128, 961–977 (2002).
12
Hori M., Shimoju R., Tokunaga R., Ohkubo M., Miyabe S., Ohnishi J., Murakami K., Kurosawa M., Tickling increases dopamine release in the nucleus accumbens and 50 kHz ultrasonic vocalizations in adolescent rats. Neuroreport 24, 241–245 (2013).
13
Burgdorf J., Wood P. L., Kroes R. A., Moskal J. R., Panksepp J., Neurobiology of 50-kHz ultrasonic vocalizations in rats: Electrode mapping, lesion, and pharmacology studies. Behav. Brain Res. 182, 274–283 (2007).
14
Newberry R. C., Wood-Gush D. G. M., Hall J. W., Playful behaviour of piglets. Behav. Processes 17, 205–216 (1988).
15
Sachs B. D., Harris V. S., Sex-differences and developmental-changes in selected juvenile activities (play) of domestic lambs. Anim. Behav. 26, 678–684 (1978).
16
Bekoff M., Social play and play-soliciting by infant canids. Am. Zool. 14, 323–340 (1974).
17
Schwarting R. K. W., Jegan N., Wöhr M., Situational factors, conditions and individual variables which can determine ultrasonic vocalizations in male adult Wistar rats. Behav. Brain Res. 182, 208–222 (2007).
18
Rao R. P., Mielke F., Bobrov E., Brecht M., Vocalization-whisking coordination and multisensory integration of social signals in rat auditory cortex. eLife 3, e03185 (2014).
19
Wright J. M., Gourdon J. C., Clarke P. B., Identification of multiple call categories within the rich repertoire of adult rat 50-kHz ultrasonic vocalizations: Effects of amphetamine and social context. Psychopharmacology 211, 1–13 (2010).
20
Burgdorf J., Kroes R. A., Moskal J. R., Pfaus J. G., Brudzynski S. M., Panksepp J., Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: Behavioral concomitants, relationship to reward, and self-administration of playback. J. Comp. Psychol. 122, 357–367 (2008).
21
Zotterman Y., Touch, pain and tickling: An electro-physiological investigation on cutaneous sensory nerves. J. Physiol. 95, 1–28 (1939).
22
Vrontou S., Wong A. M., Rau K. K., Koerber H. R., Anderson D. J., Genetic identification of C fibres that detect massage-like stroking of hairy skin in vivo. Nature 493, 669–673 (2013).
23
Newman B., O’Grady M. A., Ryan C. S., Hemmes N. S., Pavlovian conditioning of the tickle response of human subjects: Temporal and delay conditioning. Percept. Mot. Skills 77, 779–785 (1993).
24
Fried I., Wilson C. L., MacDonald K. A., Behnke E. J., Electric current stimulates laughter. Nature 391, 650 (1998).
25
Fernández-Baca Vaca G., Lüders H. O., Basha M. M., Miller J. P., Mirth and laughter elicited during brain stimulation. Epileptic Disord. 13, 435–440 (2011).
26
Caruana F., Avanzini P., Gozzo F., Francione S., Cardinale F., Rizzolatti G., Mirth and laughter elicited by electrical stimulation of the human anterior cingulate cortex. Cortex 71, 323–331 (2015).
27
Caruana F., Gozzo F., Pelliccia V., Cossu M., Avanzini P., Smile and laughter elicited by electrical stimulation of the frontal operculum. Neuropsychologia 89, 364–370 (2016).
28
Panksepp J., Normansell L., Cox J. F., Siviy S. M., Effects of neonatal decortication on the social play of juvenile rats. Physiol. Behav. 56, 429–443 (1994).
29
Gazzola V., Spezio M. L., Etzel J. A., Castelli F., Adolphs R., Keysers C., Primary somatosensory cortex discriminates affective significance in social touch. Proc. Natl. Acad. Sci. U.S.A. 109, E1657–E1666 (2012).
30
Bobrov E., Wolfe J., Rao R. P., Brecht M., The representation of social facial touch in rat barrel cortex. Curr. Biol. 24, 109–115 (2014).
31
Lenschow C., Brecht M., Barrel cortex membrane potential dynamics in social touch. Neuron 85, 718–725 (2015).
32
Lausberg H., Sloetjes H., Coding gestural behavior with the NEUROGES—ELAN system. Behav. Res. Methods 41, 841–849 (2009).
33
Chapin J. K., Lin C. S., Mapping the body representation in the SI cortex of anesthetized and awake rats. J. Comp. Neurol. 229, 199–213 (1984).
34
Seelke A. M. H., Dooley J. C., Krubitzer L. A., The emergence of somatotopic maps of the body in S1 in rats: The correspondence between functional and anatomical organization. PLOS ONE 7, e32322 (2012).

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Science
Volume 354Issue 631311 November 2016
Pages: 757 - 760

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Received: 7 July 2016
Accepted: 21 September 2016

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S. Ishiyama
Bernstein Center for Computational Neuroscience Berlin, Institut für Biologie, Humboldt-Universität zu Berlin, 10115 Berlin, Germany.
Bernstein Center for Computational Neuroscience Berlin, Institut für Biologie, Humboldt-Universität zu Berlin, 10115 Berlin, Germany.
NeuroCure Cluster of Excellence, Humboldt-Universität zu Berlin, Berlin, Germany.

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*Corresponding author. Email: [email protected]

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Science
Volume 354|Issue 6313
11 November 2016
Submission history
Received:7 July 2016
Accepted:21 September 2016
Published in print:11 November 2016
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