The behavioral neuroscience of anuran social signal processing

Abstract

Acoustic communication is the major component of social behavior in anuran amphibians (frogs and toads) and has served as a neuroethological model for the nervous system's processing of social signals related to mate choice decisions. The male's advertisement or mating call is its most conspicuous social signal, and the nervous system's analysis of the call is a progressive process. As processing proceeds through neural systems, response properties become more specific to the signal and, in addition, neural activity gradually shifts from representing sensory (auditory periphery and brainstem) to sensorimotor (diencephalon) to motor (forebrain) components of a behavioral response.A comparative analysis of many anuran species shows that the first stage in biasing responses toward conspecific signals over heterospecific signals, and toward particular features of conspecific signals, lies in the tuning of the peripheral auditory system. Biases in processing signals are apparent through the brainstem auditory system, where additional feature detection neurons are added by the time processing reaches the level of the midbrain. Recent work using immediate early gene expression as a marker of neural activity suggests that by the level of the midbrain and forebrain, the differential neural representation of conspecific and heterospecific signals involves both changes in mean activity levels across multiple subnuclei, and in the functional correlations among acoustically active areas. Our data show that in frogs the auditory midbrain appears to play an important role in controlling behavioral responses to acoustic social signals by acting as a regulatory gateway between the stimulus analysis of the brainstem and the behavioral and physiological control centers of the forebrain. We predict that this will hold true for other vertebrate groups such as birds and fish that produce acoustic social signals, and perhaps also in fish where electroreception or vibratory sensing through the lateral line systems plays a role in social signaling, as in all these cases ascending sensory information converges onto midbrain nuclei which relay information to higher brain centers.

Prior experience with conspecific signals enhances auditory midbrain responsiveness to conspecific vocalizations

“…female phonotaxis and male antiphonal calling behavior (Diekamp and Gerhardt, 1995;Gerhardt, 1974;Gerhardt, 1981a;Gerhardt, 1981b;Gerhardt, 1991;Simmons et al, 1993) mate attraction signals -and synthetic stimuli with similar spectral-temporal features are processed selectively or with enhanced responsiveness by neurons in many brain regions [as revealed in electrophysiology studies (Diekamp and Gerhardt, 1995;Eggermont and Epping, 1986;Elliott et al, 2011;Fuzessery and Feng, 1983;Miranda and Wilczynski, 2009a;Miranda and Wilczynski, 2009b;Rose et al, 1985) and immediate early gene studies (Chakraborty et al, 2010;Hoke et al, 2004;Hoke et al, 2008;Lynch and Wilczynski, 2008;Mangiamele and Burmeister, 2011)]. In anuran amphibians, this is particularly apparent in the midbrain (reviewed in Rose and Gooler, 2007;Wilczynski and Ryan, 2010).…”

“…In H. cinerea and other anurans, the importance of communication signals is reflected in specializations in the neural systems processing them. Communication signals -particularly mate-attraction signals -and synthetic stimuli with similar spectral-temporal features are processed selectively or with enhanced sensitivity throughout the auditory system, and particularly in the midbrain (Feng et al, 1990;Leary et al, 2008;Rose and Gooler, 2007;Wilczynski and Ryan, 2010). There is good evidence to suggest that exposure to conspecific chorus sounds can influence the hormonal state of the green treefrog and other frogs (Burmeister and Wilczynski, 2000;Burmeister and Wilczynski, 2001;Lynch and Wilczynski, 2006;Wilczynski and Lynch, 2011); however, it is not clear how this exposure to conspecific choruses might alter the neural processing of male calls in the auditory system.…”

“…The torus is a midbrain auditory processing area that is equivalent to the inferior colliculus of mammals and has previously been shown to respond selectively to stimulation with conspecific calls in other frog species (Burmeister et al, 2008;Hoke et al, 2004;Hoke et al, 2008;Leary et al, 2008). The torus is also a critical part of the auditory system for connecting sensory processing with both motor and endocrine areas of the forebrain (Hoke et al, 2008;Hoke et al, 2010;Wilczynski and Ryan, 2010). We hypothesized that ecologically relevant exposure to mate signals would increase expression of the activity-dependent immediate early gene egr-1 in the torus in response to mate attraction signals.…”

The Influence of Genome and Cell Size on Brain Morphology in Amphibians

“…The bulk of auditory afferents terminates in the principal nucleus with projections that mainly terminate at the mesencephalic level. In contrast, magnocellular neurons and especially laminar nucleus neurons do not only project to other auditory centers, but also to premotor and motor centers in the brainstem and medulla oblongata, thus forming an audiomotor interface (Walkowiak and Luksch 1994;Luksch and Walkowiak 1998;Wilczynski and Ryan 2010). Single-unit (Hermes et al 1982), as well as multiunit studies (Mohneke 1983;Schneichel and Schneider 1988) revealed a topic representation of tones in the torus.…”

A miniature microdrive for recording auditory evoked potentials from awake anurans

“…However, several investigators have assumed that each species-specific property is relevant to the conspecific animal (see review by Wilczynski and Ryan 2010). Therefore, the sound stimuli used in this study have been chosen to be simple and complex tone bursts, which have carrier frequencies similar to those extracted from the mating call of the toad Bufo regularis.…”