Evolutionary adaptations for the temporal processing of natural sounds by the anuran peripheral auditory system

Abstract

Sensory systems function most efficiently when processing natural stimuli, such as vocalizations, and it is thought that this reflects evolutionary adaptation. Among the best-described examples of evolutionary adaptation in the auditory system are the frequent matches between spectral tuning in both the peripheral and central auditory systems of anurans (frogs and toads) and the frequency spectra of conspecific calls. Tuning to the temporal properties of conspecific calls is less well established, and in anurans has so far been documented only in the central auditory system. Using auditoryevoked potentials, we asked whether there are species-specific or sex-specific adaptations of the auditory systems of gray treefrogs (Hyla chrysoscelis) and green treefrogs (H. cinerea) to the temporal modulations present in conspecific calls. Modulation rate transfer functions (MRTFs) constructed from auditory steady-state responses revealed that each species was more sensitive than the other to the modulation rates typical of conspecific advertisement calls. In addition, auditory brainstem responses (ABRs) to paired clicks indicated relatively better temporal resolution in green treefrogs, which could represent an adaptation to the faster modulation rates present in the calls of this species. MRTFs and recovery of ABRs to paired clicks were generally similar between the sexes, and we found no evidence that males were more sensitive than females to the temporal modulation patterns characteristic of the aggressive calls used in male-male competition. Together, our results suggest that efficient processing of the temporal properties of behaviorally relevant sounds begins at potentially very early stages of the anuran auditory system that include the periphery.

Frequency-channel dependent selectivity for temporal call characteristics in gray treefrogs, Hyla versicolor

“…Nonetheless, previous studies (e.g. Schrode and Bee, 2015) and our own results indicate that some temporal processing takes place before information from the two frequency channels is integrated in the central nervous system. Our finding of differences in behavioral selectivity for temporal characteristics based on frequency channel raises important questions about how different components of the auditory system partition the processing of complex signal characteristics, and how this information is ultimately integrated.…”

“…Temporal call characteristics are also important for species recognition, discrimination between different call types and determining the attractiveness of potential mates (Brenowitz and Rose, 1999;Gerhardt, 2008;Sullivan and Leek, 1987;Wells and Bard, 1987). Highly tuned temporal filters are well described in the auditory midbrain and higher processing centers in the brain (Rose and Gooler, 2007) but the possibility of temporal processing in the auditory periphery has received less attention (Schrode and Bee, 2015). Nonetheless, there is reason to expect differences between the two frequency channels of the auditory periphery in the processing of the pattern of amplitude modulation (AM) because of general trade-offs in auditory systems between frequency and time resolution (Gabor, 1946).…”

“…Recordings in the auditory midbrain revealed neurons that are highly selective for conspecific AM patterns (Diekamp and Gerhardt, 1995;Hanson et al, 2015;Rose et al, 1985Rose et al, , 2015. Less is known about the temporal selectivity of lower levels of the auditory system, but a study of auditory-evoked potentials in the closely related H. chrysoscelis demonstrated that the auditory periphery is also involved in temporal processing (Schrode and Bee, 2015).…”

The effects of call-like masking diminish after nightly exposure to conspecific choruses in green treefrogs (Hyla cinerea)

“…Briefly, we measured auditory evoked potentials from each animal on day 0. Auditory evoked potentials are closely correlated with single unit and behavioral estimates of hearing in treefrogs Schrode and Bee, 2015;Schrode et al, 2014). After auditory testing, animals were placed in custom-built sound isolation chambers where they received nightly sound exposure (stimuli described below) to either a simulated treefrog chorus (4 frogs: 2 males and 2 females) or random tones (5 frogs: 2 males and 3 females) for 10 consecutive days (days 1-11).…”

“…The relationship between the temporal properties of calls and auditory temporal resolution has recently been investigated in green treefrogs and Cope's gray treefrogs using auditory evoked potentials (Schrode and Bee, 2015). Green treefrog calls have faster modulations than Cope's gray treefrog calls.…”