The Behavioral Neuroscience of Anuran Social Signal Processing

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.