Neuroethology of auditory systems: contributions in memory of Albert S. Feng

This special issue is organized into three major parts according to the organisms studied: frogs, mammals (excluding bats), and bats. In the following, we summarize the core messages conveyed by the authors of each of the individual contributions and place their papers in a broader context of the neuroethology of auditory systems and of the work of Al Feng.

Frogs

In “Are frog calls relatively difficult to locate by mammalian predators?,” Jones and Ratnam (2023) suggest that there are several features of frog calls that reduce their localizability by mammalian predators. These features include using highly periodic vocalizations, narrowband calls, short-pulsed calls and often calling in dense choruses using various means for controlling synchrony, maintaining chorus tenure, and abruptly switching off calling, all of which serve to confound localization by predators. They illustrate these strategies with call analyses for three different frog species. This work demonstrates that not only do frogs have sophisticated mechanisms for sound localization (many of which were first described by Al Feng), but also employ clever approaches to limit the localizability of their own calls to avoid predation.

In “Female preferences for the spectral content of advertisement calls in Cope’s gray treefrog (Hyla chrysoscelis),” Gupta and Bee (2023) investigate the amplitude dependence of female preferences for the spectral content of male advertisement calls, which have a “bimodal” spectrum with separate low-frequency (1.25 kHz) and high-frequency (2.5 kHz) components. With few exceptions, preferences are largely independent of amplitude across both a 30-dB range of overall signal amplitude suggesting an “essential nonlinearity” (sensu Goldstein 1967), and an 11-dB range in the relative amplitudes of the two spectral components. Their data speak to the difficulty of blind acceptance of the matched filter hypothesis across all species. These findings also give strong impetus for future comparative neuroethological studies of spectral processing, an approach pioneered and promoted by Al Feng throughout his career.

In “Behind the mask(ing): How frogs cope with noise,” Lee et al. (2023) review the literature on release from auditory masking with a focus on frog auditory communication in noisy environments, such as during chorusing. They address many of the mechanisms to which Al Feng’s work made a major contribution, such as matched filtering, dip listening, using temporal patterns of sound such as co-modulation or spatial separation to facilitate extracting an acoustic signal from a noisy environment. They then look forward, proposing additional mechanisms and approaches to test these mechanisms.

In “Male antiphonal calls and phonotaxis evoked by female courtship calls in the large odorous frog (Odorrana graminea),” Shen et al. (2023) examine the acoustic behaviors of males from the species Odorrana graminea, a close relative of well-studied concave-eared torrent frog (Odorrana tormota). This work, done with Al Feng’s longtime collaborator Peter Narins, showed that Odorrana graminea, like the sympatric Odorrana tormota, display bidirectional courtship-related acoustic communication between males and females. These data suggest that similar environmental pressures between these two species may have produced similar acoustic specializations.

In “DPOAEs and tympanal membrane vibrations reveal adaptations of the sexually dimorphic ear of the concave-eared torrent frog, Odorrana tormota,” Cobo-Cuan et al. (2023) continue their studies of the remarkable Chinese frog which has an auditory system that can respond to both audible and ultrasonic frequencies. They measured tympanal vibrations using laser Doppler vibrometry and found that Eustachian tube closing in these frogs increases the sensitivity of the ear to frequencies matching that of the opposite sex. This study also includes Al Feng as a co-author.

In “Diversity of temporal response patterns in midbrain auditory neurons of frogs Batrachyla and its relevance for male vocal responses,” longtime Feng collaborator Mario Penna and colleagues examine responses of neurons in the torus semicircularis (inferior colliculus) of two species of Batrachyla to temporally patterned sounds (Penna et al. 2023). They uncovered a diversity of temporal transfer function response types in these neurons. When coupled with previous work in a different species of Batrachyla, this work suggests that multiple strategies may exist to extract temporal characteristics of sound within this genus.

De Luca et al. (2023) test the reactions of male midwife toads to the randomized playback of a vibrational crescendo stimulus train in their paper entitled: “Effect of natural abiotic soil vibrations, rainfall and wind on anuran calling behavior: A test with captive-bred midwife toads (Alytes obstetricans).” They found that A. obstetricans is highly sensitive to very low frequencies, which could explain their sensitivity to vibrational stimuli. This work corroborates the earlier use of playback of a random crescendo stimulus train (Caorsi et al. 2019) and validates it to be a compelling approach for addressing behavioral questions.

In their article entitled “Neuroethology of sound localization in anurans,” Gerhardt et al. (2023) review the literature on behavioral and neurophysiological studies of sound localization by frogs and toads. It becomes immediately obvious that Al Feng’s contributions to this field are seminal. Moreover, his classical neuroethological approach to understanding the mechanisms underlying this critical behavior in the amphibia has yielded great insights into the neural processes underlying both the encoding of sound direction and binaural processing in these animals.

Mammals (excluding bats)

In their paper “Descending projections to the auditory midbrain: Evolutionary considerations,” (Macias and Llano 2023) compare the structure and function of the mammalian inferior colliculus with the analogous structure in the frog—the torus semicircularis. They reflect on whether thalamotectal projections in mammals and amphibians are homologous and whether they interact with evolutionarily more newly derived projections from the cerebral cortex. They also consider the behavioral significance of these descending pathways, given the anurans’ ability to navigate complex acoustic landscapes without the benefit of a corticocollicular projection.

William P. Shofner's contribution to this special issue is titled “Cochlear tuning and the peripheral representation of harmonic sound in mammals.” In this article, he compares the spectral and temporal representations of stochastic, complex sounds which underlie the perception of pitch strength in humans and chinchillas (Shofner 2023). Specifically, the pitch strengths of these stochastic sounds differ between humans and chinchillas. Shofner’s studies with auditory filterbank models and comparisons between summary correlograms and excitation patterns with corresponding behavioral data on pitch strength suggest that the dominant cue for pitch strength in humans is spectral (i.e., harmonic) structure, whereas the dominant cue for chinchillas is temporal (i.e., envelope) structure.

Extending auditory processing work to humans, in “Long-term changes in cortical representation through perceptual learning of spectrally degraded speech,” Murai and Riquimaroux (2023) examined neural changes in response to acoustic perceptual training. They found that as humans learned to improve the accuracy of their perception of noise-vocoded speech, responses in the left posterior superior temporal sulcus showed parallel changes. These data point to the posterior temporal sulcus as a candidate region to facilitate the learning of noise-degraded speech sounds in humans.

Bats

In “Oscillatory discharges in the auditory midbrain of the big brown bat contribute to coding of echo delay,” Simmons and Simmons (2023) examine a potential mechanism for delay tuning in the bat inferior colliculus. They report that big brown bat inferior colliculus neurons respond with oscillatory discharges at a broad range of latencies in response to pulse-echo pairs. Oscillations to pulse and echo extensively overlap, creating interference patterns that can be used for pulse-echo delay encoding. This work extends Al Feng’s early pioneering work that first showed the presence of pulse-echo delay-tuned neurons and his later work on neural oscillations in the inferior colliculus (Feng et al. 1978).

In “Transmitter and receiver of the low frequency horseshoe bat Rhinolophus paradoxolophus are functionally matched for fluttering target detection,” Schoeppler et al. (2023) show that Rhinolophus paradoxolophus, which emits a pulse that is an octave lower than expected for its body size, demonstrates the same Doppler-shift compensation to allow echoes to remain within its foveal frequencies, similar to other species that hunt fluttering insects.

In “Echo feedback mediates noise-induced vocal modifications in flying bats,” Luo et al. (2023) examined noise-induced vocal modifications (NIVMs) in flying bats. The authors exposed freely-flying bats to broadcast noise while recording their sonar calls. They found that unlike non-echolocating animals, NIVMs in bats rely on echo feedback rather than vocal feedback.

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