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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.
