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The cry embedded within the purr

Authors:
  • Bader College Queen's University

Abstract

Despite widespread interest in inter-specific communication, few studies have examined the abilities of companion animals to communicate with humans in what has become their natural environment — the human home [1 • Nicastro N. • Owren M.J. Classification of domestic cat (Felis catus) vocalisations by naive and experienced human listeners.J. Comp. Psychol. 2003; 117: 44-52 • Crossref • PubMed • Scopus (61) • Google Scholar , 2 • Pongracz P. • Molnar C. • Miklosi A. Acoustic parameters of dog barks carry emotional information for humans.Appl. Anim. Behav. Sci. 2006; 100: 228-240 • Abstract • Full Text • Full Text PDF • Scopus (92) • Google Scholar ]. Here we report how domestic cats make subtle use of one of their most characteristic vocalisations — purring — to solicit food from their human hosts, apparently exploiting sensory biases that humans have for providing care. When humans were played purrs recorded while cats were actively seeking food at equal amplitude to purrs recorded in non-solicitation contexts, even individuals with no experience of owning cats judged the ‘solicitation’ purrs to be more urgent and less pleasant. Embedded within the naturally low-pitched purr, we found a high frequency voiced component, reminiscent of a cry or meow, that was crucial in determining urgency and pleasantness ratings. Moreover, when we re-synthesised solicitation purrs to remove only the voiced component, paired presentations revealed that these purrs were perceived as being significantly less urgent. We discuss how the structure of solicitation purrs may be exploiting an inherent mammalian sensitivity to acoustic cues relevant in the context of nurturing offspring.
Magazine
R507
Conclusions
Our understanding of the functions of
semaphorins now extends far beyond
their initial characterisation as axon
guidance cues, with roles identified
in vascular and cardiac development,
cancer progression, and the immune
system, whilst their important roles in
the pathology of various diseases and
injury states are becoming increasingly
evident. It is now accepted that
semaphorins are key regulators of
the cytoskeleton and cell adhesion
during cell migration, but that they also
evoke responses such as cell survival,
proliferation and differentiation.
Semaphorins stimulate a complex
signalling network involving a multitude
of receptors and signalling molecules,
which allows for a diverse range of
outcomes, often in a cell-
type-specific manner. Within a given
cell type, a particular semaphorin
signal can also generate different
responses depending on the presence
of a variety of modulatory signals, such
as cyclic nucleotides, adding a further
layer of complexity to the network.
Clearly, future questions in this field
have to be directed at analysing the
significance of semaphorin signalling
systems in controlling cellular
responses in vivo, which promises
to deepen our understanding of the
diverse and important functions now
attributed to semaphorins.
Further reading
Bashaw, G.J. (2004). Semaphorin signaling
unplugged; a nervy AKAP cAMP(s) out on
plexin. Neuron 42, 363–366.
Eickholt, B.J. (2008). Functional diversity and
mechanisms of action of the semaphorins.
Development 135, 2689–2694.
Holt, C.E., and Dickson, B.J. (2005). Sugar codes for
axons? Neuron 46, 169–172.
Larrivee, B., Freitas, C., Suchting, S., Brunet, I.,
and Eichmann, A. (2009). Guidance of vascular
development: lessons from the nervous system.
Circ. Res. 104, 428–441.
Neufeld, G., and Kessler, O. (2008). The
semaphorins: versatile regulators of tumour
progression and tumour angiogenesis. Nat. Rev.
Cancer 8, 632–645.
Pasterkamp R.J. (2007). Semaphorins: Receptor
and Intracellular Signaling Mechanisms (Berlin:
Springer).
Serini, G., Maione, F
., and Bussolino, F. (2009).
Semaphorins and tumor angiogenesis.
Angiogenesis, epub ahead of print.
Tamagnone, L., and Comoglio, P.M. (2004). To move
or not to move? Semaphorin signalling in cell
migration. EMBO Rep. 5, 356–361.
Tran, T.S., Kolodkin, A.L., and Bharadwaj, R. (2007).
Semaphorin regulation of cellular morphology.
Annu. Rev. Cell Dev. Biol. 23, 263–292.
Zhou, Y., Gunput, R.A., and Pasterkamp, R.J.
(2008). Semaphorin signaling: progress made
and promises ahead. Trends Biochem. Sci. 33,
161–170.
MRC Centre for Developmental Neurobiology,
King’s College London, London SE1 1UL, UK.
E-mail: Britta.J.Eickholt@kcl.ac.uk
Data available on-line with this issue).
When we conducted playbacks of
purrs from 10 cats recorded in both
solicitation and non-solicitation
contexts to 50 human participants
at equal amplitude (Supplemental
Data), they consistently judged the
solicitation purrs to be more urgent
and less pleasant than the non-
solicitation purrs (urgency: F1,500 =
248.26, P < 0.0005; and pleasantness:
F1,500 = 138.24, P < 0.0005) and when
given the choice between pairs of
non-solicitation and solicitation
purrs from the same cats they
identified the solicitation purr as the
more urgent and less pleasant of the
two (urgency: t49 = 17.11, d.f. = 49,
p < 0.0005; pleasantness: t49 = 15.42,
p < 0.0005). While participants
consistently selected the solicitation
purrs as more urgent irrespective of
previous cat experience (owners: t29 =
18.05, p < 0.0005; non-owners: t19 =
8.22, p < 0.0005), individuals that
had owned a cat did perform
significantly better than non-owners,
suggesting that the ability to
identify these purrs can improve
through learning (F1,45 = 10.71,
p = 0.002).
We conducted analyses to
identify the acoustic cues that both
distinguished the purr types and
predicted the mean urgency and
pleasantness ratings that each of
the purr stimuli in the independent
rankings trial had received
(Supplemental Data). While examining
the acoustic structure of purrs we
identified the presence of a frequency
peak (range 220–520 Hz, mean 380
Hz) that was particularly pronounced
in solicitation purrs and did not match
the predicted formant structure of
the call (Figure 1). This peak was
taken to indicate voicing (activation
of the vocal folds via air movement),
at a frequency more typical of a cry
or meow [1], occurring alongside
the unusual low frequency muscular
activation of the vocal folds that gives
the purr its extremely low (~27 Hz)
fundamental frequency [5]. The height
of this spectral peak was the acoustic
feature that most consistently defined
purr stimuli in the solicitation context,
solicitation purrs having more intense
voiced peaks (Wilcoxon-signed-ranks
test z = –2.67, p = 0.008). Moreover,
the height of the voiced peak (VP) was
crucial in determining the urgency and
pleasantness ratings that participants
gave individual stimuli. A multiple
The cry embedded
within the purr
Karen McComb1, Anna M. Taylor1,
Christian Wilson1, and
Benjamin D. Charlton2
Despite widespread interest in
inter-specific communication, few
studies have examined the abilities of
companion animals to communicate
with humans in what has become
their natural environment — the
human home [1,2]. Here we report
how domestic cats make subtle use
of one of their most characteristic
vocalisations — purring — to
solicit food from their human hosts,
apparently exploiting sensory biases
that humans have for providing care.
When humans were played purrs
recorded while cats were actively
seeking food at equal amplitude to
purrs recorded in non-solicitation
contexts, even individuals with no
experience of owning cats judged
the ‘solicitation’ purrs to be more
urgent and less pleasant. Embedded
within the naturally low-pitched purr,
we found a high frequency voiced
component, reminiscent of a cry or
meow, that was crucial in determining
urgency and pleasantness ratings.
Moreover, when we re-synthesised
solicitation purrs to remove only
the voiced component, paired
presentations revealed that these
purrs were perceived as being
significantly less urgent. We discuss
how the structure of solicitation
purrs may be exploiting an inherent
mammalian sensitivity to acoustic
cues relevant in the context of
nurturing offspring.
In the domestic cat, many signals
given when interacting with humans
seem to originate from the period of
dependency on the mother — which
is also the time when social behaviour
in this ancestrally asocial species
is most prevalent [3]. Purring in
domestic cats is one such signal, with
kittens being first observed to purr
whilst suckling from the mother [4].
Although humans typically interpret
purring as indicating a happy,
contented cat, some cats also purr at
feeding time, actively soliciting food
from their owners (see Supplemental
Correspondence
Current Biology Vol 19 No 13
R508
regression on the mean ratings that
each of the stimuli received identified
VP height and purr rate as the key
predictors of urgency ratings (F 2,17 =
15.13, p < 0.005, Adjusted R2 = 0.598;
VP height: β = 0.619, t = 4.09, p =
0.001; purr rate: β = 0.706, t = 4.67,
p < 0.0005), and VP height and purr
harmonicity as the key predictors of
pleasantness (F2,17 = 9.76, p = 0.002,
adjusted R2 = 0.480; voiced peak
height: β = –0.555, t = -3.34, p =
0.004; harmonicity: β = 0.423,
t = 2.55, p = 0.021). To directly
investigate the specific effect of the
VP, we re-synthesised solicitation
purrs to remove this spectral
component while leaving other
acoustic parameters unchanged
(Supplemental Data). In paired
presentations, stimuli with the VP
removed were consistently judged
by participants as less urgent than
matched stimuli with the voiced
peak present (t49 = 6.39, p < 0.0005).
Interestingly, stimuli with the VP
removed were not judged as more
pleasant in these comparisons (t48 =
-0.65, p = 0.518), perhaps because
their lower harmonicity (unchanged
between the experimental
conditions) played an important
role here.
Parallels have previously been
drawn between the isolation cry of
domestic cats and the human infant
distress cry [6]. Our study indicates
that such a cry, embedded within
the naturally low-pitched purr, is
dramatically emphasised by cats
in the context of food solicitation
and humans are highly sensitive
to it. The inclusion of this high
frequency component within the purr
could serve as a subtle means of
exploitation, tapping into an inherent
mammalian sensitivity to such cries
and also possibly rendering the call
less harmonic and thus more difficult
to habituate to [7]. The voiced peak
that we measured in our study in fact
occurs at comparable frequencies
to the fundamental frequency of a
human infant’s cry (300–600Hz in a
healthy infant: [8]). While solicitation
purrs may not have the obvious
urgency of the wails of hungry/
distressed human infants, their
particular acoustic characteristics
are likely to make them very difficult
to ignore [7–9]. More generally, such
exploitation of sensory biases in
inter-specific communication has the
potential to provide signallers with
an effective means of enhancing the
level of care or cooperation that they
receive.
Supplemental Data
Supplemental data are available at http://
www.cell.com/current-biology/supplemental/
S0960-9822(09)01168-3.
Acknowledgments
We are indebted to Archie, Clyde, Fuzzy,
Hippolythe, Marbles, Max, Mojo, Morgan,
McKee, Pepo, Socks and their long-
suffering owners for participating, the
Waltham Foundation for initial funding,
and Benji Elimelech, Leanne Proops, David
Reby, Stuart Semple and Graeme Shannon
for invaluable help.
References
1. Nicastro N., and Owren, M.J. (2003).
Classification of domestic cat (Felis catus)
vocalisations by naive and experienced
human listeners. J. Comp. Psychol. 117,
44–52.
2. Pongracz, P., Molnar, C., Miklosi, A. (2006).
Acoustic parameters of dog barks carry
emotional information for humans. Appl.
Anim. Behav. Sci. 100, 228–240.
3. Bateson, P., and Turner, D.C., (2000).
Questions about cats. In The Domestic Cat,
the Biology of its Behaviour, P. Bateson, and
D.C. Turner eds. (Cambridge: Cambridge
University Press), pp. 230–237.
4. Moelk, M. (1979). The development of friendly
approach behaviour in the cat: a study of
kitten-mother relations and the cognitive
development of the kitten from birth to eight
weeks. Adv. Stud. Behav. 10, 163–223.
5. Frazer-Sissom, D., Rice, D., and Peters, G.
(1991). How cats purr. J. Zool. 223, 79–90.
6. Buchwald, J.S. & Shipley, C. (1985).
A comparative model of infant cry. In
Infant Crying: Theoretical and Research
Perspectives, E.M. Lester and C.F.Z. Boukydis
eds. (New York: Plenum), pp. 279–305.
7. Fitch, W., Neubauer, J., and Herzel, H. (2002).
Calls out of chaos: The adaptive significance
of non linear phenomena in mammalian vocal
production. Anim. Behav. 63, 407–418.
8. Furlow, F.B. (1996). Human neonatal cry
quality as an honest signal of fitness. Evol.
Hum. Behav. 18, 175–193.
9. Zeifman, D.M. (2001). An ethological analysis
of human infant crying: answering Tinbergen’s
four questions. Dev. Psychobiol. 39, 265–285.
1Centre for Mammal Vocal Communication
Research, Department of Psychology,
School of Life Sciences, University
of Sussex, Brighton BN1 9QH, UK.
2Zoo Atlanta, Atlanta, Georgia,
GA 30315-1440, USA.
E-mail: karenm@sussex.ac.uk
dBs dBs
F1
(1090 Hz) F1
(970 Hz)
F2
(2175 Hz) F2
(2130 Hz)
F3
(3620 Hz)
F3
(3970 Hz)
F4
(5280 Hz)
F4
(5660 Hz)
Frequency (Hz)Frequency (Hz)
Pronounced voiced
peak
(490 Hz, 12.5 dB above falling slope)
Small voiced
peak
(330 Hz, 0.3 dB above falling slope)
Current Biology
Solicitation purr Non-solicitation purr
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.
... Cat purrs recorded during solicitation of a human for food are encoded with a high-frequency component that may be similar to the specific frequency of a human infant's cry and is acoustically different from purrs recorded during non-solicitation events. Humans are able to distinguish the solicitation purrs from non-solicitation purrs, particularly if they are cat owners (McComb et al., 2009). ...
... Experience was found not to influence an individual's ability to correctly classify canine vocalizations (Molnár et al., 2010), and Pongrácz et al. (2005Pongrácz et al. ( , 2006 found that listeners with different levels of experience with dogs only had minor differences in classifying dog barks. These findings differ from others (McComb et al., 2009;Nicastro & Owren, 2003;Prato-Previde et al., 2020), who independently found that people with previous experience with cats are better at classifying the valence of cat vocalizations. However, cat vocalizations are structurally different (in McComb et al., 2009, a purr) and are used in different contexts, therefore they are difficult to compare. ...
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Recent work on human vocal production demonstrates that certain irregular phenomena seen in human pathological voices and baby crying result from nonlinearities in the vocal production system. Equivalent phenomena are quite common in nonhuman mammal vocal repertoires. In particular, bifurcations and chaos are ubiquitous aspects of the normal adult repertoire in many primate species. Here we argue that these phenomena result from properties inherent in the peripheral production mechanism, which allows individuals to generate highly complex and unpredictable vocalizations without requiring equivalently complex neural control mechanisms. We provide examples from the vocal repertoire of rhesus macaques, Macaca mulatta, and other species illustrating the different classes of nonlinear phenomena, and review the concepts from nonlinear dynamics that explicate these calls. Finally, we discuss the evolutionary significance of nonlinear vocal phenomena. We suggest that nonlinear phenomena may subserve individual recognition and the estimation of size or fluctuating asymmetry from vocalizations. Furthermore, neurally ‘cheap’ unpredictability may serve the valuable adaptive function of making chaotic calls difficult to predict and ignore. While noting that nonlinear phenomena are in some cases probably nonadaptive by-products of the physics of the sound-generating mechanism, we suggest that these functional hypotheses provide at least a partial explanation for the ubiquity of nonlinear calls in nonhuman vocal repertoires.
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Language is generally considered to be unique to the human species and, of its various forms, vocal language, or speech, clearly represents one of the most complex behaviors of any species. The linguistic aspect of speech involves a hierarchy of discrete elements that develop meaning as basic phonemic units are combined into syllables and words, and these, in turn, are organized by rules of syntax into meaningful phrases and sentences. The resulting expression is understandable either when produced by the human voice or by a speech synthesizer such as a computer. However, the marked difference in quality and ease of comprehension between natural and synthetic speech is, in large part, a function of a second nonlexical element— the “paralinguistic” or prosodic component of speech. The qualities of pitch, intensity, and duration combine to provide an overall intonation that makes the human voice recognizable and familiar, projects emotional states—happiness, anger, fear—and conveys general intent as, for example, the terminal rising inflection of a yes/no question versus the falling inflection of a declaration.
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This chapter discusses the development of friendly approach behavior in the cat. It mentions that the behavior of housecat kittens and the development of their behavior is organized by the manner in which the kitten obtain its food in the wild at various ages-first, by suckling only, then by snatching the single item of dead prey brought to the litter at a time by the mother against competition from littermates, and finally by capturing and killing live prey in the prey's own territory. The kitten starts out at birth with the ability to drag itself forward a few inches and move its head from side to side, usually crying, until it locates a milk-producing nipple on its mother's body. By the end of the nest stage in the first half of their fifth week, when kittens are able to run about outside their nest in play, kittens are able to respond to touch or voice greeting from their mother, rolling play, or a bit of purring, and to take the initiative in greeting their mother with batting play or a rub. On sixth week, the kitten is able to eat solid food and focus with absorption on small, movable, inanimate objects as food and toys, and it changes from needing to seek a suckling type of frequent and prolonged whole body contact with its mother to needing to direct at her rough attack play of a sort, which enables the kitten to snatch away from its mother the single item of dead prey.
Article
Care soliciting vocalizations are common in the young of many bird and mammal species. As parents are expected to assess individual offspring's potential contributions to parental fitness when partitioning resources between young, I propose that offspring solicitation displays are evolved demonstrations of phenotypic quality with which offspring compete with current and future siblings for access to parental resources. This hypothesis should apply to human neonatal crying as well as offspring solicitation in other species. In this review of the scientific literature, I test three predictions derived from this hypothesis: (1) that crying is relatively more costly for low phenotypic quality infants than infants of higher phenotypic quality; (2) that the acoustic structure of cries correlates with infant condition; and (3) that the aspects of cry structure that trigger parental emotions likely to affect investment behaviors will be those that communicate offspring condition. All predictions were supported. Acoustic characteristics tied to the neurophysiological production of cries (particularly fundamental frequency, or pitch) constitute a reliable signal of infant phenotypic quality. I conclude that in addition to asserting need, an evolved function of the human neonatal cry is to communicate phenotypic quality (and hence, likely contributions to parental fitness) to parents. The study of offspring solicitation vocalizations may contribute importantly to our understanding of animal communication systems, patterns of parental investment, and the etiology of human child abuse.
Article
We measured purring in unrestrained intact pumas, cheetahs and domestic cats. Domestic cats, Felis silvestris f. catus, purr at a frequency of 26·3 ±; 1·95 (S.D.) Hz. The frequency at mid-expiration exceeds that at mid-inspiration by 2·4 ± 1·3 Hz. Purring frequency for individuals does not change with age. Purring can occur simultaneously with other vocalization. Two-channel acoustic measurements confirm that the primary mechanism for sound and vibration production is a centrally driven laryngeal modulation of respiratory flow. The diaphragm and other muscles appear to be unnecessary for purring other than to drive respiration.
Article
The proximate causes, survival value, ontogeny, and evolutionary history of human infant crying are examined. Experiments and field observations involving infant distress vocalizations and begging calls in avian, mammalian, and nonhuman primate species are considered, as are ethnographic records of infant care and responses to crying in nonindustrialized societies. It is argued that human infant crying evolved as a primarily acoustic, graded signal, that it is a fairly reliable, if imperfect, indicator of need for parental care and that its primary function is to promote parental caregiving. Selection pressures that may have shaped the evolution of crying and its potential for corruption through dishonesty also are discussed. © 2001 John Wiley & Sons, Inc. Dev Psychobiol 39: 265–285, 2001
Article
In an earlier study, we found that humans were able to categorize dog barks correctly, which were recorded in various situations. The acoustic parameters, like tonality, pitch and inter-bark time intervals, seemed to have a strong effect on how human listeners described the emotionality of these dog vocalisations. In this study, we investigated if the effect of the acoustic parameters of the dog bark is the same on the human listeners as we would expect it from studies in other mammalian species (for example, low, hoarse sounds indicating aggression; high pitched, tonal sounds indicating subordinance/ fear). People with different experience with dogs were asked to describe the emotional content of several artificially assembled bark sequences on the basis of five emotional states (aggressiveness, fear, despair, playfulness, happiness). The selection of the barks was based on low, medium and high values of tonality and peak frequency. For assembling artificial bark sequences, we used short, middle or long inter-bark intervals. We found that humans with different levels of experience with dogs described the emotional content of the bark sequences quite similarly, and the extent of previous experience with the given breed (Mudi), or with dogs in general, did not cause characteristic differences in the emotionality scores. The scoring of the emotional content of the bark sequences was in accordance with the so-called Morton's structural-acoustic rules. Thus, low pitched barks were described as aggressive, and tonal and high pitched barks were scored as either fearful or desperate, but always without aggressiveness. In general, tonality of the bark sequence had much less effect than the pitch of the sounds. We found also that the inter-bark intervals had a strong effect on the emotionality of dog barks for the human listeners: bark sequences with short inter-bark intervals were scored as aggressive, but bark sequences with longer inter-bark intervals were scored with low values of aggression. High pitched bark sequences with long inter-bark intervals were considered happy and playful, independently from their tonality. These findings show that dog barks function as predicted by the structural-motivational rules developed for acoustic signals in other species, suggesting that dog barks may present a functional system for communication at least in the dog-human relationship. In sum it seems that many types of different emotions can be expressed with the variation of at least three acoustic parameters.
Article
To test for possible functional referentiality in a common domestic cat (Felis catus) vocalization, the authors conducted 2 experiments to examine whether human participants could classify meow sounds recorded from 12 different cats in 5 behavioral contexts. In Experiment 1, participants heard singlecalls, whereas in Experiment 2, bouts of calls were presented. In both cases, classification accuracy was significantly above chance, but modestly so. Accuracy for bouts exceeded that for single calls. Overall, participants performed better in classifying individual calls if they had lived with, interacted with, and had a general affinity for cats. These results provide little evidence of referentiality suggesting instead that meows are nonspecific, somewhat negatively toned stimuli that attract attention from humans. With experience, human listeners can become more proficient at inferring positive-affect states from cat meows.
Questions about cats
  • Bateson
Bateson, P., and Turner, D.C., (2000). Questions about cats. In The Domestic Cat, the Biology of its Behaviour, P. Bateson, and D.C. Turner eds. (Cambridge: Cambridge University Press), pp. 230-237.