The pale spear-nosed bat: A neuromolecular and transgenic model for vocal learning.

Vocal learning, the ability to produce modified vocalizations via learning from acoustic signals, is a key trait in the evolution of speech. While extensively studied in songbirds, mammalian models for vocal learning are rare. Bats present a promising study system given their gregarious natures, small size, and the ability of some species to be maintained in captive colonies. We utilize the pale spear-nosed bat (Phyllostomus discolor) and report advances in establishing this species as a tractable model for understanding vocal learning. We have taken an interdisciplinary approach, aiming to provide an integrated understanding across genomics (Part I), neurobiology (Part II), and transgenics (Part III). In Part I, we generated new, high-quality genome annotations of coding genes and noncoding microRNAs to facilitate functional and evolutionary studies. In Part II, we traced connections between auditory-related brain regions and reported neuroimaging to explore the structure of the brain and gene expression patterns to highlight brain regions. In Part III, we created the first successful transgenic bats by manipulating the expression of FoxP2, a speech-related gene. These interdisciplinary approaches are facilitating a mechanistic and evolutionary understanding of mammalian vocal learning and can also contribute to other areas of investigation that utilize P. discolor or bats as study species.

Communication breakdown: Limits of spectro-temporal resolution for the perception of bat communication calls.

During vocal communication, the spectro-temporal structure of vocalizations conveys important contextual information. Bats excel in the use of sounds for echolocation by meticulous encoding of signals in the temporal domain. We therefore hypothesized that for social communication as well, bats would excel at detecting minute distortions in the spectro-temporal structure of calls. To test this hypothesis, we systematically introduced spectro-temporal distortion to communication calls of Phyllostomus discolor bats. We broke down each call into windows of the same length and randomized the phase spectrum inside each window. The overall degree of spectro-temporal distortion in communication calls increased with window length. Modelling the bat auditory periphery revealed that cochlear mechanisms allow discrimination of fast spectro-temporal envelopes. We evaluated model predictions with experimental psychophysical and neurophysiological data. We first assessed bats' performance in discriminating original versions of calls from increasingly distorted versions of the same calls. We further examined cortical responses to determine additional specializations for call discrimination at the cortical level. Psychophysical and cortical responses concurred with model predictions, revealing discrimination thresholds in the range of 8-15 ms randomization-window length. Our data suggest that specialized cortical areas are not necessary to impart psychophysical resilience to temporal distortion in communication calls.

Post-natal development of the envelope following response to amplitude modulated sounds in the bat Phyllostomus discolor.

Bats use a large repertoire of calls for social communication, which are often characterized by temporal amplitude and frequency modulations. As bats are considered to be among the few mammalian species capable of vocal learning, the perception of temporal sound modulations should be crucial for juvenile bats to develop social communication abilities. However, the post-natal development of auditory processing of temporal modulations has not been investigated in bats, so far. Here we use the minimally invasive technique of recording auditory brainstem responses to measure the envelope following response (EFR) to sinusoidally amplitude modulated noise (range of modulation frequencies: 11-130 Hz) in three juveniles (p8-p72) of the bat, Phyllostomus discolor. In two out of three animals, we show that although amplitude modulation processing is basically developed at p8, EFRs maturated further over a period of about two weeks until p33. Maturation of the EFR generally took longer for higher modulation frequencies (87-130 Hz) than for lower modulation frequencies (11-58 Hz).

Processing of fast amplitude modulations in bat auditory cortex matches communication call-specific sound features.

Bats use a large repertoire of calls for social communication. In the bat Phyllostomus discolor, social communication calls are often characterized by sinusoidal amplitude and frequency modulations with modulation frequencies in the range of 100-130 Hz. However, peaks in mammalian auditory cortical modulation transfer functions are typically limited to modulation frequencies below 100 Hz. We investigated the coding of sinusoidally amplitude modulated sounds in auditory cortical neurons in P. discolor by constructing rate and temporal modulation transfer functions. Neuronal responses to playbacks of various communication calls were additionally recorded and compared with the neurons' responses to sinusoidally amplitude-modulated sounds. Cortical neurons in the posterior dorsal field of the auditory cortex were tuned to unusually high modulation frequencies: rate modulation transfer functions often peaked around 130 Hz (median: 87 Hz), and the median of the highest modulation frequency that evoked significant phase-locking was also 130 Hz. Both values are much higher than reported from the auditory cortex of other mammals, with more than 51% of the units preferring modulation frequencies exceeding 100 Hz. Conspicuously, the fast modulations preferred by the neurons match the fast amplitude and frequency modulations of prosocial, and mostly of aggressive, communication calls in P. discolor. We suggest that the preference for fast amplitude modulations in the P. discolor dorsal auditory cortex serves to reliably encode the fast modulations seen in their communication calls. NEW & NOTEWORTHY Neural processing of temporal sound features is crucial for the analysis of communication calls. In bats, these calls are often characterized by fast temporal envelope modulations. Because auditory cortex neurons typically encode only low modulation frequencies, it is unclear how species-specific vocalizations are cortically processed. We show that auditory cortex neurons in the bat Phyllostomus discolor encode fast temporal envelope modulations. This property improves response specificity to communication calls and thus might support species-specific communication.