Simple Syllabic Calls Accompany Discrete Behavior Patterns in Captive Pteronotus parnellii: An Illustration of the Motivation-Structure Hypothesis

Mustached bats, Pteronotus parnellii, are highly social and vocal. Individuals of this species roost in tight clusters, and emit an acoustically rich repertoire of calls whose behavioral significance is largely unknown. We recorded their social and vocal behaviors within a colony housed under semi-natural conditions. We also quantified the spatial spread of each bat's roosting location and discovered that this was relatively fixed and roughly confined to an individual's body width. The spatial precision in roosting was accompanied by an equally remarkable match between specific vocalizations and well-timed, discrete, identifiable postures/behaviors, as revealed by logistic regression analysis. The bodily behaviors included crouching, marking, yawning, nipping, flicking, fighting, kissing, inspecting, and fly-bys. Two echolocation-like calls were used to maintain spacing in the colony, two noisy broadband calls were emitted during fights, two tonal calls conveyed fear, and another tonal call signaled appeasement. Overall, the results establish that mustached bats exhibit complex social interactions common to other social mammals. The correspondence of relatively low frequency and noisy, broadband calls with aggression, and of tonal, high frequency calls with fear supports Morton's Motivation-Structure hypothesis, and establishes a link between motivation and the acoustic structure of social calls emitted by mustached bats

Geographic Variation in Social Vocalizations of the Great Himalayan Leaf-Nosed Bat, Hipposideros armiger: Acoustic Overflow Across Population Boundaries

Bat populations employ rich vocal repertoires for social communication in addition to emitting sound pulses for echolocation. Acoustic parameters of echolocation pulses can vary with the context in which they are emitted, and also with the individual and across populations as a whole. The acoustic parameters of social vocalizations, or “calls”, also vary with the individual and context, but not much is known about their variation across populations at different geographic locations. Here, we leveraged the detailed acoustic classification of social vocalizations available for the Great Himalayan leaf-nosed bat, Hipposideros armiger, to examine geographic variation in five commonly emitted simple syllable types. We hypothesized that individuals within geographically dispersed populations communicate using spectrographically similar constructs or “syllable types”. We also examined whether call syllables vary discordantly with the correlation pattern observed for echolocation pulses across those same geographic regions. Furthermore, we postulated that the acoustic boundaries of a syllable type are not uniquely constrained to its variation within a particular population of the same subspecies. To test our hypotheses, we obtained recordings of social calls of H. a. armiger from nine locations within the oriental region. These locations were consolidated into five geographic regions based on previously established region-specific differences in the peak frequency of echolocation pulses. A multivariate cluster analysis established that unlike echolocation pulses, syllable types exhibit a relatively large variance. Analysis of this variance showed significant differences in Least Squares Means estimates, establishing significant population-level differences in the multiparametric means of individual syllable types across geographic regions. Multivariate discriminant analysis confirmed the presence of region-specific centroids for different syllable constructs, but also showed a large overlap of their multiparametric boundaries across geographic regions. We propose that despite differences in the population-specific core construct of a syllable type, bats maximize acoustic variation across individuals within a population irrespective of its overflow and overlap with other populations

DSCF Neurons Within the Primary Auditory Cortex of the Mustached Bat Process Frequency Modulations Present Within Social Calls

Neurons in the Doppler-shifted constant frequency processing (DSCF) area in the primary auditory cortex of mustached bats, Pteronotus parnellii, are multifunctional, responding both to echolocation and communication sounds. Simultaneous presentation of a DSCF neuron's best low and high frequencies (BFlow and BFhigh, respectively) facilitates its response. BFlow corresponds to a frequency in the frequency-modulated (FM) component of the first harmonic in the echolocation pulse, and BFhigh corresponds to the constant frequency (CF) component in the second harmonic of the echo. We systematically varied the slopes, bandwidths, and central frequencies of FMs traversing the BFhigh region to arrive at the “best FM” for single DSCF neurons. We report that nearly half (46%) of DSCF neurons preferred linear FMs to CFs and average response magnitude to FMs was not significantly less (P = 0.08) than that to CFs at BFhigh when each test stimulus was paired with a CF at BFlow. For linear FMs ranging in slope from 0.04 to 4.0 kHz/ms and in bandwidth from 0.44 to 7.88 kHz, the majority of DSCF neurons preferred upward (55%) to downward (21%) FMs. Central frequencies of the best FMs were typically close to but did not always match a neuron's BFhigh. Neurons exhibited combination-sensitivity to “call fragments” (calls that were band-pass filtered in the BFhigh region) paired with their BFlow. Our data show a close match between the modulation direction of a neuron's best FM and that of its preferred call fragment. These response properties show that DSCF neurons extract multiple parameters of FMs and are specialized for processing both FMs for communication and CFs for echolocation

Fear Conditioned Discrimination of Frequency Modulated Sweeps within Species-Specific Calls of Mustached Bats

Social and echolocation vocalizations of bats contain different patterns of frequency modulations. An adult bat’s ability to discriminate between various FM parameters, however, is not well established. Using changes in heart rate (HR) as a quantitative measure of associative learning, we demonstrate that mustached bats (Pteronotus parnellii) can be fear conditioned to linear frequency modulated (FM) sweeps typically centered at their acoustic fovea (,60 kHz). We also show that HR is sensitive to a change in the direction of the conditional frequency modulation keeping all other parameters constant. In addition, a change in either depth or duration co-varied with FM rate is reflected in the change in HR. Finally, HR increases linearly with FM rate incremented by 0.1 kHz/ms from a pure tone to a target rate of 1.0 kHz/ms of the conditional stimulus. Learning is relatively rapid, occurring after a single training session. We also observed that fear conditioning enhances local field potential activity within the basolateral amygdala. Neural response enhancement coinciding with rapid learning and a fine scale cortical representation of FM sweeps shown earlier make FMs prime candidates for discriminating between different call types and possibly communicating socially relevant information within species-specific sounds

Two examples of learning curves using HR recordings.

<p>Lines are smoothed (0.5 s and 1.0 s sliding window in A and B, respectively). Line plot of HR is expressed as percentage change above average pre-stimulus values representing the “learning curve” for first three training sessions in two bats. Each bat acquired a robust and relatively stable response on the third day that was rapidly re-established on day 7 in the first bat (A).</p

Hemispheric and sex differences in mustached bat primary auditory cortex revealed by neural responses to slow frequency modulations

The mustached bat (Pteronotus parnellii) is a mammalian model of cortical hemispheric asymmetry. In this species, complex social vocalizations are processed preferentially in the left Doppler-shifted constant frequency (DSCF) subregion of primary auditory cortex. Like hemispheric specializations for speech and music, this bat brain asymmetry differs between sexes (i.e., males>females) and is linked to spectrotemporal processing based on selectivities to frequency modulations (FMs) with rapid rates (>0.5 kHz/ms). Analyzing responses to the long-duration (>10 ms), slow-rate (<0.5 kHz/ms) FMs to which most DSCF neurons respond may reveal additional neural substrates underlying this asymmetry. Here, we bilaterally recorded responses from 176 DSCF neurons in male and female bats that were elicited by upward and downward FMs fixed at 0.04 kHz/ms and presented at 0–90 dB SPL. In females, we found inter-hemispheric latency differences consistent with applying different temporal windows to precisely integrate spectrotemporal information. In males, we found a substrate for asymmetry less related to spectrotemporal processing than to acoustic energy (i.e., amplitude). These results suggest that in the DSCF area, (1) hemispheric differences in spectrotemporal processing manifest differently between sexes, and (2) cortical asymmetry for social communication is driven by spectrotemporal processing differences and neural selectivities for amplitude