Michael Smotherman

Versatility and Stereotypy of Free-Tailed Bat Songs

In mammals, complex songs are uncommon and few studies have examined song composition or the order of elements in songs, particularly with respect to regional and individual variation. In this study we examine how syllables and phrases are ordered and combined, ie “syntax”, of the song of Tadarida brasiliensis, the Brazilian free-tailed bat. Specifically, we test whether phrase and song composition differ among individuals and between two regions, we determine variability across renditions within individuals, and test whether phrases are randomly ordered and combined. We report three major findings. First, song phrases were highly stereotyped across two regions, so much so that some songs from the two colonies were almost indistinguishable. All males produced songs with the same four types of syllables and the same three types of phrases. Second, we found that although song construction was similar across regions, the number of syllables within phrases, and the number and order of phrases in songs varied greatly within and among individuals. Last, we determined that phrase order, although diverse, deviated from random models. We found broad scale phrase-order rules and certain higher order combinations that were highly preferred. We conclude that free-tailed bat songs are composed of highly stereotyped phrases hierarchically organized by a common set of syntactical rules. However, within global species-specific patterns, songs male free-tailed bats dynamically vary syllable number, phrase order, and phrase repetitions across song renditions.

A Mechanism for Vocal-Respiratory Coupling in the Mammalian Parabrachial Nucleus

Mammalian vocalizations require the precise coordination of separate laryngeal and respiratory motor pathways. Precisely how and where in the brain vocal motor patterns interact with respiratory rhythm control is unknown. The parabrachial nucleus (PB) is known to mediate key respiratory reflexes and is also considered a principle component of the mammalian vocal motor pathway, making it a likely site for vocal-respiratory interactions, yet a specific role for the PB in vocalizing has yet to be demonstrated. To investigate the role of the PB in vocal-respiratory coordination, we pharmacologically manipulated synaptic activity in the PB while spontaneously vocalizing horseshoe bats were provoked to emit either short, single syllable or long, multisyllabic vocal motor patterns. Iontophoresis of the GABAA agonist muscimol (MUS) into the lateral PB extended expiratory durations surrounding all vocalizations and increased mean call durations. Alternatively, application of the GABAA antagonist bicuculline methiodide (BIC) shortened expirations and call durations. In addition, BIC eliminated the occurrence of multisyllabic vocalizations. BIC caused a mild increase in quiet breathing rates, whereas MUS tended to slow quiet breathing. The results indicate that GABAA receptor-mediated inhibition in the lateral PB modulates the time course of respiratory phase switching during vocalizing, and is needed for proper coordination of calling and breathing in mammals. We hypothesize that vocal-respiratory rhythm entrainment is achieved at least in part via mechanisms similar to other forms of locomotor-respiratory coupling, namely somatosensory feedback influences on respiratory phase-switching in the lateral PB.

Sensory Feedback Control of Mammalian Vocalizations

Somatosensory and auditory feedback mechanisms are dynamic components of the vocal motor pattern generator in mammals. This review explores how sensory cues arising from central auditory and somatosensory pathways actively guide the production of both simple sounds and complex phrases in mammals. While human speech is a uniquely sophisticated example of mammalian vocal behavior, other mammals can serve as examples of how sensory feedback guides complex vocal patterns. Echolocating bats in particular are unique in their absolute dependence on voice control for survival: these animals must constantly adjust the acoustic and temporal patterns of their orientation sounds to efficiently navigate and forage for insects at high speeds under the cover of darkness. Many species of bats also utter a broad repertoire of communication sounds. The functional neuroanatomy of the bat vocal motor pathway is basically identical to other mammals, but the acute significance of sensory feedback in echolocation has made this a profitable model system for studying general principles of sensorimotor integration with regard to vocalizing. Bats and humans are similar in that they both maintain precise control of many different voice parameters, both exhibit a similar suite of responses to altered auditory feedback, and for both the efficacy of sensory feedback depends upon behavioral context. By comparing similarities and differences in the ways sensory feedback influences voice in humans and bats, we may shed light on the basic architecture of the mammalian vocal motor system and perhaps be able to better distinguish those features of human vocal control that evolved uniquely in support of speech and language.

Evolution of the Amphibian Ear

Most amphibians have within their ears the substrate to hear efficiently underwater, underground, and in air, a talent few if any other vertebrates can lay claim to. They have achieved this by being very conservative in the nature of novel addition s and specialized adaptations to their ears. Indeed, regressive events appear to be just as common as progressive trends in the evolution of the amphibian ear. As a result, the amphibian ear reflects a diverse array of basically simple, presumably reliable mechanisms of auditory transduction; mechanisms that have in essence served as the foundations of the more sophisticated hearing apparati seen in other terrestrial vertebrates. Understanding of the mechanisms of hearing in amphibians can thus offer many insights into the physical and ecological forces that have fueled the evolution of hearing in terrestrial vertebrates.

Context-dependent effects of noise on echolocation pulse characteristics in free-tailed bats

Background noise evokes a similar suite of adaptations in the acoustic structure of communication calls across a diverse range of vertebrates. Echolocating bats may have evolved specialized vocal strategies for echolocating in noise, but also seem to exhibit generic vertebrate responses such as the ubiquitous Lombard response. We wondered how bats balance generic and echolocation-specific vocal responses to noise. To address this question, we first characterized the vocal responses of flying free-tailed bats (Tadarida brasiliensis) to broadband noises varying in amplitude. Secondly, we measured the bats’ responses to band-limited noises that varied in the extent of overlap with their echolocation pulse bandwidth. We hypothesized that the bats’ generic responses to noise would be graded proportionally with noise amplitude, total bandwidth and frequency content, and consequently that more selective responses to band-limited noise such as the jamming avoidance response could be explained by a linear decomposition of the response to broadband noise. Instead, the results showed that both the nature and the magnitude of the vocal responses varied with the acoustic structure of the outgoing pulse as well as non-linearly with noise parameters. We conclude that free-tailed bats utilize separate generic and specialized vocal responses to noise in a context-dependent fashion.

The tiny difference between foraging and communication buzzes uttered by the Mexican free-tailed bat, Tadarida brasiliensis

Echolocating insectivorous bats consummate prey captures using a distinct vocal motor pattern commonly known as the terminal or feeding buzz, which is widely considered a fixed motor pattern executed independently of auditory feedback influences. The Mexican free-tailed bat, Tadarida brasiliensis, offers an opportunity to explore the role of sensory feedback in buzzing because they emit similar buzzes both in flight during foraging and while stationary as communication sounds. Here we compared the spectral and temporal patterns of foraging and communication buzzes to address whether or not auditory feedback may influence buzz patterns. We found that while foraging buzzes uttered in open space were composed of generic FM calls, communication buzzes were composed of an adapted CF–FM call similar to the call type used by T. brasiliensis when navigating in confined spaces. This provides the first evidence that some bats can make significant context-dependent changes in the spectral parameters of calls within their buzz. We also found that inter-pulse intervals, but not call durations, were different within the two buzz types. These observations indicate that though a common pattern generator hierarchically organizes all buzzes, T. brasiliensis retains a significant capacity to adapt the spectral and temporal patterns of elements within its buzzes.

Social context evokes rapid changes in bat song syntax

The capacity to modify vocal syntax to changes in social context is an important component of vocal plasticity and complexity in adult vertebrates, especially in human speech. The ecological significance of this behaviour has been well established in some avian species but not in mammals where complex, multisyllabic vocalizations are rare. The Brazilian free-tailed bat, Tadarida brasiliensis, is a mammal that sings like a bird, producing hierarchically structured songs that vary in the order and number of phrases (i.e. syntax) from one rendition to the next while simultaneously following specific organizational rules. Here, we used playback experiments to examine the function of songs and tested whether song syntax is correlated with social context. Free-tailed bats responded rapidly and robustly to echolocation calls that mimicked a bat flying past the roost but did not respond to conspecific song playbacks. We compared songs that were directed at a passing bat with songs that were produced spontaneously and found that bats produced longer songs with different phrase content and order when singing spontaneously than when singing to bats approaching their roost. Thus, free-tailed bats quickly varied song composition to meet the specific demands of different social functions. These distinct singing behaviours are similar to those of some songbirds, suggesting that bats and birds have converged upon a similar set of production modes that may reflect common neural mechanisms and ecological factors.

Regulation of bat echolocation pulse acoustics by striatal dopamine

SUMMARY The ability to control the bandwidth, amplitude and duration of echolocation pulses is a crucial aspect of echolocation performance but few details are known about the neural mechanisms underlying the control of these voice parameters in any mammal. The basal ganglia (BG) are a suite of forebrain nuclei centrally involved in sensory-motor control and are characterized by their dependence on dopamine. We hypothesized that pharmacological manipulation of brain dopamine levels could reveal how BG circuits might influence the acoustic structure of bat echolocation pulses. A single intraperitoneal injection of a low dose (5 mg kg–1) of the neurotoxin 1-methyl-4-phenylpyridine (MPTP), which selectively targets dopamine-producing cells of the substantia nigra, produced a rapid degradation in pulse acoustic structure and eliminated the bats ability to make compensatory changes in pulse amplitude in response to background noise, i.e. the Lombard response. However, high-performance liquid chromatography (HPLC) measurements of striatal dopamine concentrations revealed that the main effect of MPTP was a fourfold increase rather than the predicted decrease in striatal dopamine levels. After first using autoradiographic methods to confirm the presence and location of D1- and D2-type dopamine receptors in the bat striatum, systemic injections of receptor subtype-specific agonists showed that MPTPs effects on pulse acoustics were mimicked by a D2-type dopamine receptor agonist (Quinpirole) but not by a D1-type dopamine receptor agonist (SKF82958). The results suggest that BG circuits have the capacity to influence echolocation pulse acoustics, particularly via D2-type dopamine receptor-mediated pathways, and may therefore represent an important mechanism for vocal control in bats.

Groups of bats improve sonar efficiency through mutual suppression of pulse emissions

How bats adapt their sonar behavior to accommodate the noisiness of a crowded day roost is a mystery. Some bats change their pulse acoustics to enhance the distinction between theirs and another bats echoes, but additional mechanisms are needed to explain the bat sonar systems exceptional resilience to jamming by conspecifics. Variable pulse repetition rate strategies offer one potential solution to this dynamic problem, but precisely how changes in pulse rate could improve sonar performance in social settings is unclear. Here we show that bats decrease their emission rates as population density increases, following a pattern that reflects a cumulative mutual suppression of each others pulse emissions. Playback of artificially-generated echolocation pulses similarly slowed emission rates, demonstrating that suppression was mediated by hearing the pulses of other bats. Slower emission rates did not support an antiphonal emission strategy but did reduce the relative proportion of emitted pulses that overlapped with another bats emissions, reducing the relative rate of mutual interference. The prevalence of acoustic interferences occurring amongst bats was empirically determined to be a linear function of population density and mean emission rates. Consequently as group size increased, small reductions in emission rates spread across the group partially mitigated the increase in interference rate. Drawing on lessons learned from communications networking theory we show how modest decreases in pulse emission rates can significantly increase the net information throughput of the shared acoustic space, thereby improving sonar efficiency for all individuals in a group. We propose that an automated acoustic suppression of pulse emissions triggered by bats hearing each others emissions dynamically optimizes sonar efficiency for the entire group.

Doppler-shift compensation behavior by Wagner’s mustached bat, Pteronotus personatus

Doppler-shift compensation behavior (DSC) is a highly specialized vocal response displayed by bats that emit pulses with a prominent constant frequency (CF) component and adjust the frequency of their CF component to compensate for flight-speed induced Doppler shifts in the frequency of the returning echoes. DSC has only been observed in one member of the Neotropical Mormoopidae, a family of bats that use pulses with prominent CF components, leading researchers to suspect that DSC is a uniquely derived trait in the single species Pteronotus parnellii. Yet recent phylogenetic data indicate that the lineage of P. parnellii originates from the most basal node in the evolutionary history of the genus Pteronotus. DSC behavior was investigated in another member of this family, Pteronotus personatus, because molecular data indicated that this species stems from the second most basal node in Pteronotus. DSC was tested for by swinging the bats on a pendulum. P. personatus performed DSC as well as P. parnellii under identical conditions. Two other closely related mormoopids, Pteronotus davyi and Mormoops megalophylla, were also tested and neither shifted the peak frequency of their pulses. These results shed light on the evolutionary history of DSC among the mormoopids.