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Scientific Understanding of Consciousness |
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Neural Basis of Contagious Itch
Science 10 Mar 2017: Vol. 355, Issue 6329, pp. 1072-1076 Molecular and neural basis of contagious itch behavior in mice Yao-Qing Yu, et.al, Center for the Study of Itch, Washington University School of Medicine, St. Louis, MO 63110, USA. Department of Anesthesiology, Washington University School of Medicine, St. Louis, MO 63110, USA. Institute for Biomedical Sciences of Pain, Tangdu Hospital, Fourth Military Medical University, Xi’an, Shaanxi 710038, China. Department of Psychiatry, Washington University School of Medicine, St. Louis, MO 63110, USA. Department of Developmental Biology, Washington University School of Medicine, St. Louis, MO 63110, USA. [paraphrase] Socially contagious itch is ubiquitous in human society, but whether it exists in rodents is unclear. Using a behavioral paradigm that does not entail prior training or reward, we found that mice scratched after observing a conspecific scratching. Molecular mapping showed increased neuronal activity in the suprachiasmatic nucleus (SCN) of the hypothalamus of mice that displayed contagious scratching. Ablation of gastrin-releasing peptide receptor (GRPR) or GRPR neurons in the SCN abolished contagious scratching behavior, which was recapitulated by chemogenetic inhibition of SCN GRP neurons. Activation of SCN GRP/GRPR neurons evoked scratching behavior. These data demonstrate that GRP-GRPR signaling is necessary and sufficient for transmitting contagious itch information in the SCN. The findings may have implications for our understanding of neural circuits that control socially contagious behaviors. Socially contagious behaviors such as contagious itching/scratching and yawning are prevalent in humans and in highly social animals. However, such behaviors have only been sporadically mentioned in the context of imitation and/or social learning. The lack of experimental paradigms that permit recreation of socially contagious behaviors in a naturalistic environment without prior training or reward has hindered studies of such behaviors at the molecular and circuit levels. To test whether scratching is contagious in mice, we used mice with excessive spontaneous scratching because of chronic itch as the demonstrators and naïve mice with no prior contact to mice with chronic itch in an adjacent home cage as the observers. Mice that did not scratch excessively were used as control demonstrators. Both observer groups showed similar numbers of looks, defined as a pause and look toward the demonstrator (18.3 ± 2 versus 23.1 ± 2.6 looks, P = 0.17). Control observers displayed almost no coincidental look-and-scratch behavior. In contrast, mice displayed significantly increased scratching within 5 s after look behavior, defined as imitative scratching, upon observation of demonstrators scratching (4.5 ± 0.8 versus 0.2 ± 0.2 look-and-scratches, P < 0.001). We found that itch is contagious in mice. Our results identify a previously unknown function of SCN by revealing its critical role in contagious itch transmission. Using cell type–specific inhibition and activation, we discovered that SCN GRP/GRPR neurons are key conduits for receiving, integrating, and transmitting visually induced itch information. GRP depletion after the contagious itch test supported the idea that GRP is released from GRPergic fibers to activate GRPR neurons. Exogenous GRP-induced scratching behavior is completely abolished in Grpr KO mice. This underscores the specificity and sufficiency of GRP-GRPR signaling in mediating contagious itch behavior within intra-SCN circuits. SCN GRPR neurons may functionally be heterogeneous. Alternatively, SCN GRPR neurons could possess a dual function: one for photic modulation and another for itch. Spinal and SCN GRPR neural circuits represent the two parallel pathways for transmission of itch, induced by cutaneous and visual stimuli, respectively. Whether they may converge on the same sensorimotor system to compute stereotyped scratching is not yet known. Scratching behavior in mice was induced by mere observation of a conspecific scratching in a video; this finding provides evidence that contagious itch is not a form of empathy, which in mice appears to be restricted to familiars. Visual cue–induced scratching action could be mimicked by artificially stimulating SCN GRPR neurons, which suggests that an automatic activation of a cascade of neural circuits for itch, rather than a manifestation in a higher cognitive/affective capacity required for empathy, gives rise to contagious itch. The discovery of SCN GRPR circuits for itch permits in-depth dissection of the input and output circuitry for itch transmission; previous studies have suggested that GRP neurons receive non–image-forming photic information. It will be important to probe how visual input that encodes scratching action activates SCN GRP neurons and how GRPR neurons compute the output information. Given that myriad neural circuits are likely modulated upon viewing the scratching motion, further research is necessary to elucidate the discrete neural circuits subserving visual transmission of scratching motion and/or motor control. It will also be of interest to determine whether SCN subcircuits may mediate other types of socially contagious behaviors, such as yawning or empathy for pain. [end of paraphrase]
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