2382
INTRODUCTION
Background noise is always present in natural environments, and
this noise is usually viewed as detrimental to signal detection. Many
sources of air movement are present in the natural environment of
crickets. Atmospheric air current, singing by males, displacements
of other crickets and insects, as well as self-movement (including
the movements of the cerci themselves) all produce airflows that
are most likely sensed by the animal (Edwards and Palka, 1974;
Kämper and Dambach, 1981). All these air currents can furthermore
be modulated by the structural properties of the environment. Despite
the presence of this very complex and variable background noise,
behavioral studies have shown that crickets are able to detect and
recognize extremely weak air movements generated by an attacking
predator (Dangles et al., 2007). Crickets perceive air movements
using hundreds of filiform mechanosensory hairs located on the
cerci. Axons from these mechanosensory receptors project into the
terminal abdominal ganglion (TAG) and connect to local and
projecting interneurons. The projecting interneurons leave the TAG
via the pair of abdominal connectives and connect to neurons in
higher centers, which mediate escape and other behaviors (Edwards
and Palka, 1974; Camhi, 1984; Ritzmann, 1984; Insausti et al.,
2011). The axons of some projecting cercal interneurons are very
large relative to other projecting axons in the abdominal connectives,
allowing a quick transmission of the information and thus a quick
escape response. The ability of the cercal system to detect
approaching predators under noisy conditions has not been studied
extensively at the neuronal level, and the few studies that have been
published were based on measurements obtained exclusively in the
laboratory using white noise stimuli (Plummer and Camhi, 1981;
Levin and Miller, 1996; Clague et al., 1997). However, as shown
recently in another electrophysiological study, the responses of the
cercal interneurons to white-noise stimuli, which were used in many
previous studies, are qualitatively and quantitatively different than
responses elicited by air currents crafted to resemble those generated
by natural predators (Mulder-Rosi et al., 2010). Hence, interpretation
of those earlier studies on the effects of noise on interneuron
responsiveness and on the response to predator attack may be
problematic, and a neuroethologically relevant study of the
perception of an approaching predator would require the use of
realistic stimuli. Furthermore, experiments conducted in the field
under more naturalistic noise conditions could shed light on the true
operation of the cercal system.
Over the last few years, the wood cricket Nemobius sylvestris
(Bosc 1792) has been the subject of studies focusing on its ecology
(Dangles et al., 2006a), its escape behavior (Dupuy et al., 2011),
the neuroanatomy of the cercal sensory system (Insausti et al., 2008;
Insausti et al., 2011), the anatomy of cerci (Dangles et al., 2005),
mathematical modeling of the movement of mechanoreceptive hairs
(Magal et al., 2006) and air movements around hairs on cerci
(Steinmann et al., 2006). Nemobius sylvestris crickets live in the
litter of forests, an easily accessible environment for field
experiments. The main predator of this cricket species in the region
where these studies were carried out is the wolf spider Pardosa sp.
(Dangles et al., 2006a). The aerodynamics of the running spider
SUMMARY
The ability of the insect cercal system to detect approaching predators has been studied extensively in the laboratory and in the
field. Some previous studies have assessed the extent to which sensory noise affects the operational characteristics of the cercal
system, but these studies have only been carried out in laboratory settings using white noise stimuli of unrealistic nature. Using
a piston mimicking the natural airflow of an approaching predator, we recorded the neural activity through the abdominal
connectives from the terminal abdominal ganglion of freely moving wood crickets (Nemobius sylvestris) in a semi-field situation.
A cluster analysis of spike amplitudes revealed six clusters, or ʻunitsʼ, corresponding to six different subsets of cercal
interneurons. No spontaneous activity was recorded for the units of larger amplitude, reinforcing the idea they correspond to the
largest giant interneurons. Many of the cercal units are already activated by background noise, sometimes only weakly, and the
approach of a predator is signaled by an increase in their activity, in particular for the larger-amplitude units. A scaling law
predicts that the cumulative number of spikes is a function of the velocity of the flow perceived at the rear of the cricket, including
a multiplicative factor that increases linearly with piston velocity. We discuss the implications of this finding in terms of how the
cricket might infer the imminence and nature of a predatory attack.
Supplementary material available online at http://jeb.biologists.org/cgi/content/full/215/14/2382/DC1
Key words: semi-field experiment, escape behavior, giant interneuron, terminal abdominal ganglion, TAG, electrophysiology, Nemobius sylvestris.
Received 29 October 2011; Accepted 19 March 2012
The Journal of Experimental Biology 215, 2382-2389
© 2012. Published by The Company of Biologists Ltd
doi:10.1242/jeb.067405
RESEARCH ARTICLE
Responses of cricket cercal interneurons to realistic naturalistic stimuli in the field
Fabienne Dupuy
1
, Thomas Steinmann
1
, Dominique Pierre
1
, Jean-Philippe Christidès
1
, Graham Cummins
2
,
Claudio Lazzari
1
, John Miller
2
and Jérôme Casas
1,
*
1
Institut de Recherche sur la Biologie de lʼInsecte, UMR 7261 CNRS–Université François Rabelais, Av Monge, Parc Grandmont,
Tours 37200, France and
2
Center for Computational Biology, Montana State University, Bozeman, MT, USA
*Author for correspondence (casas@univ-tours.fr)
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