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The Cry Embedded Within the Purr

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The Cry Embedded Within the Purr Magazine R507 Conclusions Data available on-line with this issue). Our understanding of the functions of Correspondence When we conducted playbacks of semaphorins now extends far beyond purrs from 10 cats recorded in both their initial characterisation as axon solicitation and non-solicitation guidance cues, with roles identified The cry embedded contexts to 50 human participants in vascular and cardiac development, at equal amplitude (Supplemental cancer progression, and the immune within the purr Data), they consistently judged the system, whilst their important roles in solicitation purrs to be more urgent the pathology of various diseases and Karen McComb1, Anna M. Taylor1, and less pleasant than the non- 1 injury states are becoming increasingly Christian Wilson , and solicitation purrs (urgency: F1,500 = evident. It is now accepted that Benjamin D. Charlton2 248.26, P < 0.0005; and pleasantness: semaphorins are key regulators of F1,500 = 138.24, P < 0.0005) and when the cytoskeleton and cell adhesion Despite widespread interest in given the choice between pairs of during cell migration, but that they also inter-specific communication, few non-solicitation and solicitation evoke responses such as cell survival, studies have examined the abilities of purrs from the same cats they proliferation and differentiation. companion animals to communicate identified the solicitation purr as the Semaphorins stimulate a complex with humans in what has become more urgent and less pleasant of the signalling network involving a multitude their natural environment — the two (urgency: t49 = 17.11, d.f. = 49, of receptors and signalling molecules, human home [1,2]. Here we report p < 0.0005; pleasantness: t49 = 15.42, which allows for a diverse range of how domestic cats make subtle use p < 0.0005). While participants outcomes, often in a cell- of one of their most characteristic consistently selected the solicitation type-specific manner. Within a given vocalisations — purring — to purrs as more urgent irrespective of cell type, a particular semaphorin solicit food from their human hosts, previous cat experience (owners: t29 = signal can also generate different apparently exploiting sensory biases 18.05, p < 0.0005; non-owners: t19 = responses depending on the presence that humans have for providing care. 8.22, p < 0.0005), individuals that of a variety of modulatory signals, such When humans were played purrs had owned a cat did perform as cyclic nucleotides, adding a further recorded while cats were actively significantly better than non-owners, layer of complexity to the network. seeking food at equal amplitude to suggesting that the ability to Clearly, future questions in this field purrs recorded in non-solicitation identify these purrs can improve have to be directed at analysing the contexts, even individuals with no through learning (F1,45 = 10.71, significance of semaphorin signalling experience of owning cats judged p = 0.002). systems in controlling cellular the ‘solicitation’ purrs to be more We conducted analyses to responses in vivo, which promises urgent and less pleasant. Embedded identify the acoustic cues that both to deepen our understanding of the within the naturally low-pitched purr, distinguished the purr types and diverse and important functions now we found a high frequency voiced predicted the mean urgency and attributed to semaphorins. component, reminiscent of a cry or pleasantness ratings that each of meow, that was crucial in determining the purr stimuli in the independent Further reading urgency and pleasantness ratings. rankings trial had received Bashaw, G.J. (2004). Semaphorin signaling unplugged; a nervy AKAP cAMP(s) out on Moreover, when we re-synthesised (Supplemental Data). While examining plexin. Neuron 42, 363–366. solicitation purrs to remove only the acoustic structure of purrs we Eickholt, B.J. (2008). Functional diversity and the voiced component, paired identified the presence of a frequency mechanisms of action of the semaphorins. Development 135, 2689–2694. presentations revealed that these peak (range 220–520 Hz, mean 380 Holt, C.E., and Dickson, B.J. (2005). Sugar codes for purrs were perceived as being Hz) that was particularly pronounced axons? Neuron 46, 169–172. Larrivee, B., Freitas, C., Suchting, S., Brunet, I., significantly less urgent. We discuss in solicitation purrs and did not match and Eichmann, A. (2009). Guidance of vascular how the structure of solicitation the predicted formant structure of development: lessons from the nervous system. purrs may be exploiting an inherent the call (Figure 1). This peak was Circ. Res. 104, 428–441. Neufeld, G., and Kessler, O. (2008). The mammalian sensitivity to acoustic taken to indicate voicing (activation semaphorins: versatile regulators of tumour cues relevant in the context of of the vocal folds via air movement), progression and tumour angiogenesis. Nat. Rev. Cancer 8, 632–645. nurturing offspring. at a frequency more typical of a cry Pasterkamp R.J. (2007). Semaphorins: Receptor In the domestic cat, many signals or meow [1], occurring alongside and Intracellular Signaling Mechanisms (Berlin: given when interacting with humans the unusual low frequency muscular Springer). Serini, G., Maione, F., and Bussolino, F. (2009). seem to originate from the period of activation of the vocal folds that gives Semaphorins and tumor angiogenesis. dependency on the mother — which the purr its extremely low (~27 Hz) Angiogenesis, epub ahead of print. Tamagnone, L., and Comoglio, P.M. (2004). To move is also the time when social behaviour fundamental frequency [5]. The height or not to move? Semaphorin signalling in cell in this ancestrally asocial species of this spectral peak was the acoustic migration. EMBO Rep. 5, 356–361. is most prevalent [3]. Purring in feature that most consistently defined Tran, T.S., Kolodkin, A.L., and Bharadwaj, R. (2007). Semaphorin regulation of cellular morphology. domestic cats is one such signal, with purr stimuli in the solicitation context, Annu. Rev. Cell Dev. Biol. 23, 263–292. kittens being first observed to purr solicitation purrs having more intense Zhou, Y., Gunput, R.A., and Pasterkamp, R.J. (2008). Semaphorin signaling: progress made whilst suckling from the mother [4]. voiced peaks (Wilcoxon-signed-ranks and promises ahead. Trends Biochem. Sci. 33, Although humans typically interpret test z = –2.67, p = 0.008). Moreover, 161–170. purring as indicating a happy, the height of the voiced peak (VP) was MRC Centre for Developmental Neurobiology, contented cat, some cats also purr at crucial in determining the urgency and King’s College London, London SE1 1UL, UK. feeding time, actively soliciting food pleasantness ratings that participants E-mail: [email protected] from their owners (see Supplemental gave individual stimuli. A multiple Current Biology Vol 19 No 13 R508 Solicitation purr Non-solicitation purr F1 F1 (1090 Hz) (970 Hz) F3 F2 (3620 Hz) (2175 Hz) F4 F2 (5280 Hz) (2130 Hz) F3 (3970 Hz) dBs dBs F4 (5660 Hz) Pronounced voiced Small voiced peak peak (490 Hz, 12.5 dB above falling slope) (330 Hz, 0.3 dB above falling slope) Frequency (Hz) Frequency (Hz) Current Biology Figure 1. Purr spectra illustrating intensity of voiced peak in a solicitation and non-solicitation purr from the same cat (Pepo). For comparison with position of formant peaks and fundamental frequency see Supplemental Data; audio files of these purr types (solicitation and non-solicitation purr) are also supplied as Supplementary material. regression on the mean ratings that dramatically emphasised by cats Waltham Foundation for initial funding, each of the stimuli received identified in the context of food solicitation and Benji Elimelech, Leanne Proops, David VP height and purr rate as the key and humans are highly sensitive Reby, Stuart Semple and Graeme Shannon for invaluable help. predictors of urgency ratings (F 2,17 = to it. The inclusion of this high 15.13, p < 0.005, Adjusted R2 = 0.598; frequency component within the purr VP height: β = 0.619, t = 4.09, p = could serve as a subtle means of References 0.001; purr rate: = 0.706, t = 4.67, exploitation, tapping into an inherent 1. Nicastro N., and Owren, M.J. (2003). β Classification of domestic cat (Felis catus) p < 0.0005), and VP height and purr mammalian sensitivity to such cries vocalisations by naive and experienced harmonicity as the key predictors of and also possibly rendering the call human listeners. J. Comp. Psychol. 117, 44–52. pleasantness (F2,17 = 9.76, p = 0.002, less harmonic and thus more difficult 2. Pongracz, P., Molnar, C., Miklosi, A. (2006). adjusted R2 = 0.480; voiced peak to habituate to [7]. The voiced peak Acoustic parameters of dog barks carry height: = –0.555, t = -3.34, p = that we measured in our study in fact emotional information for humans. Appl. β Anim. Behav. Sci. 100, 228–240. 0.004; harmonicity: β = 0.423, occurs at comparable frequencies 3. Bateson, P., and Turner, D.C., (2000). t = 2.55, p = 0.021). To directly to the fundamental frequency of a Questions about cats. In The Domestic Cat, the Biology of its Behaviour, P. Bateson, and investigate the specific effect of the human infant’s cry (300–600Hz in a D.C. Turner eds. (Cambridge: Cambridge VP, we re-synthesised solicitation healthy infant: [8]). While solicitation University Press), pp. 230–237. purrs to remove this spectral purrs may not have the obvious 4. Moelk, M. (1979). The development of friendly approach behaviour in the cat: a study of component while leaving other urgency of the wails of hungry/ kitten-mother relations and the cognitive acoustic parameters unchanged distressed human infants, their development of the kitten from birth to eight weeks. Adv. Stud. Behav. 10, 163–223. (Supplemental Data). In paired particular acoustic characteristics 5. Frazer-Sissom, D., Rice, D., and Peters, G. presentations, stimuli with the VP are likely to make them very difficult (1991). How cats purr.
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