Sound source perception in anuran amphibians
Highlights
► Sound source perception in animal communication is not well understood. ► Frogs solve a biological analogue of the ‘cocktail party problem’ to communicate. ► This article reviews studies of how they do so using a limited number of acoustic cues. ► The focus is on mechanisms of masking release and auditory grouping.
Introduction
Humans and other animals often communicate acoustically in large social aggregations. Familiar examples might include a cocktail party, a songbird dawn chorus, or a group of singing insects. An important problem in the study of animal communication and sensory neurobiology concerns how a receiver's sense of hearing enables them to perceive acoustic signals as distinct sounds in these noisy and acoustically cluttered environments [1, 2]. Sound pressure waves produced by multiple active sources add together to form a single, composite sound pressure waveform that impinges on the receiver's ears (Figure 1). Listeners must parse this complex sensory input to make sense of the surrounding acoustic scene, and this ability involves overcoming two related challenges. One of these challenges is auditory masking. Signalers cannot be perceived as distinct sound sources unless receivers can segregate signals from the ambient background noise. The second challenge involves perceptually binding the spectral and temporal sound elements composing an acoustic signal to create a coherent auditory percept of the signal that can be assigned to the correct source. For humans, these two challenges form the basis of the so-called ‘cocktail party problem,’ which refers to the difficulty we experience listening to speech in noisy social settings (Figure 1) [3•].
Compared with our well-developed understanding of sound source perception in humans [4, 5, 6, 7, 8•], we know less about how non-human animals perform similar tasks in the general context of hearing and in the more specific context of acoustic communication [1, 2, 9]. This taxonomic disparity in knowledge about sound source perception represents an exciting research opportunity for neuroethologists. The sense of hearing had multiple evolutionary origins [10], and key features of auditory processing within some lineages arose multiple times (e.g. tympanic hearing in terrestrial vertebrates) [11, 12••]. From an evolutionary perspective, comparative neuroethological studies of diverse animal groups are necessary to understand how evolution might have solved common problems in sound source perception in different lineages [12••]. Here, I review studies of sound source perception in anuran amphibians, a group of vertebrates for which acoustic communication is the most important form of socio-sexual communication.
Section snippets
The frog's cocktail party problem
Anurans are notable for the loud vocalizations males produce to attract females and to defend calling sites against rival males [13, 14]. Frog vocalizations commonly reach peak sound pressure levels (SPLs) of 90 dB to 110 dB (re 20 μPa; measured at 1 m) [15]. In many species, communication takes place in large breeding choruses comprising hundreds of males, usually of multiple species, gathered at a suitable breeding site (e.g. a pond). Ambient chorus noise is intense [16], and has been reported
Segregating signals from masking noise
In humans, exploiting spatial separation between speech signals and noise represents one important way we ameliorate auditory masking under cocktail-party-like listening conditions [20]. Frogs appear to do so as well. Schwartz and Gerhardt [21] showed that female green treefrogs, Hyla cinerea, responded to male calls at signal-to-noise ratios (SNRs) that were about 3 dB lower when there was spatial separation between signals and noise, although spatial separation did not improve discrimination
Auditory grouping
Frog calls and other animal acoustic signals commonly consist of spectrally rich sounds arranged in sequences of temporally discrete elements, such as pulses or notes. Auditory grouping, therefore, requires both ‘simultaneous integration’ (i.e. grouping concurrent harmonics or formants) and ‘sequential integration’ (i.e. grouping temporally separated elements through time) [4]. Rigorous psychoacoustic studies of human subjects suggest the general rule that sound elements sharing features in
Auditory induction
In acoustically and structurally complex environments, sounds of interest may often be masked by brief, intermittent loud sounds (e.g. a cough, a clap of thunder, a door shutting). Humans [51], nonhuman primates [52], and songbirds [53] possess the remarkable ability to reconstruct percepts of sounds masked by (or even replaced by) brief bursts of noise. Known as ‘auditory induction’ [51], this ability is responsible for ‘phonemic restoration’ in humans and underlies the so-called ‘continuity
Conclusions
Research on sound source perception in anurans represents an exciting frontier in the neuroethological study of acoustic communication in these animals. As the behavioral studies reviewed here make clear, there are some fascinating parallels and notable differences in sound source perception between frogs and other animals, as well as among different species of frogs. Demonstrated similarities and differences within and among taxa create the solid foundation necessary for comparative
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgments
I thank Michael Dickinson, Christophe Micheyl, Cynthia Moss, Katrina Schrode, and Alejandro Vélez for helpful feedback on the manuscript, Robert Schlauch, morgueFile user sound_man73, and the morgueFile Free License for use of the frog images in Figure 1, Alex Baugh for the túngara frog call depicted in Figure 3, Folkert Seeba for help generating Figure 4, and the National Institute on Deafness and Other Communication Disorders (R03DC008396 and R01DC009582) and the National Science Foundation (
References (56)
Auditory scene analysis in animal communication
Adv Study Behav
(2002)The cocktail party problem
Curr Biol
(2009)How the brain separates sounds
Trends Cogn Sci
(2004)- et al.
Auditory Perception of Sound Sources
(2008) Sound source perception and stream segregation in nonhuman vetebrate animals
- et al.
Acoustic Communication in Insects and Anurans: Common Problems and Diverse Solutions
(2002) - et al.
GABA is involved in spatial unmasking in the frog auditory midbrain
J Neurosci
(2003) - et al.
Signal recognition by frogs in the presence of temporally fluctuating chorus-shaped noise
Behav Ecol Sociobiol
(2010) - et al.
Perception of mistuned harmonics in complex sounds by the bullfrog (Rana catesbeiana)
J Comp Psychol
(2000) Selectivity for harmonic structure in complex sounds by the green treefrog (Hyla cinerea)
J Comp Physiol A
(1988)