Deviance Detection to Natural Stimuli in Population Responses of the Brainstem of Bats.

Deviance detection describes an increase of neural response strength caused by a stimulus with a low probability of occurrence. This ubiquitous phenomenon has been reported for humans and multiple other species, from subthalamic areas to the auditory cortex. Cortical deviance detection has been well characterized by a range of studies using a variety of different stimuli, from artificial to natural, with and without a behavioral relevance. This allowed the identification of a broad variety of regularity deviations that are detected by the cortex. Moreover, subcortical deviance detection has been studied with simple stimuli that are not meaningful to the subject. Here, we aim to bridge this gap by using noninvasively recorded auditory brainstem responses (ABRs) to investigate deviance detection at population level in the lower stations of the auditory system of a highly vocal species: the bat Carollia perspicillata (of either sex). Our present approach uses behaviorally relevant vocalization stimuli that are similar to the animals' natural soundscape. We show that deviance detection in ABRs is significantly stronger for echolocation pulses than for social communication calls or artificial sounds, indicating that subthalamic deviance detection depends on the behavioral meaning of a stimulus. Additionally, complex physical sound features like frequency- and amplitude modulation affected the strength of deviance detection in the ABR. In summary, our results suggest that the brain can detect different types of deviants already in the brainstem, showing that subthalamic brain structures exhibit more advanced forms of deviance detection than previously known.

A neuron model with unbalanced synaptic weights explains the asymmetric effects of anaesthesia on the auditory cortex.

Substantial progress in the field of neuroscience has been made from anaesthetized preparations. Ketamine is one of the most used drugs in electrophysiology studies, but how ketamine affects neuronal responses is poorly understood. Here, we used in vivo electrophysiology and computational modelling to study how the auditory cortex of bats responds to vocalisations under anaesthesia and in wakefulness. In wakefulness, acoustic context increases neuronal discrimination of natural sounds. Neuron models predicted that ketamine affects the contextual discrimination of sounds regardless of the type of context heard by the animals (echolocation or communication sounds). However, empirical evidence showed that the predicted effect of ketamine occurs only if the acoustic context consists of low-pitched sounds (e.g., communication calls in bats). Using the empirical data, we updated the naïve models to show that differential effects of ketamine on cortical responses can be mediated by unbalanced changes in the firing rate of feedforward inputs to cortex, and changes in the depression of thalamo-cortical synaptic receptors. Combined, our findings obtained in vivo and in silico reveal the effects and mechanisms by which ketamine affects cortical responses to vocalisations.

Echolocation-related reversal of information flow in a cortical vocalization network.

The mammalian frontal and auditory cortices are important for vocal behavior. Here, using local-field potential recordings, we demonstrate that the timing and spatial patterns of oscillations in the fronto-auditory network of vocalizing bats (Carollia perspicillata) predict the purpose of vocalization: echolocation or communication. Transfer entropy analyses revealed predominant top-down (frontal-to-auditory cortex) information flow during spontaneous activity and pre-vocal periods. The dynamics of information flow depend on the behavioral role of the vocalization and on the timing relative to vocal onset. We observed the emergence of predominant bottom-up (auditory-to-frontal) information transfer during the post-vocal period specific to echolocation pulse emission, leading to self-directed acoustic feedback. Electrical stimulation of frontal areas selectively enhanced responses to sounds in auditory cortex. These results reveal unique changes in information flow across sensory and frontal cortices, potentially driven by the purpose of the vocalization in a highly vocal mammalian model.

Correlates of deviance detection in auditory brainstem responses of bats.

Identifying unexpected acoustic inputs, which allows to react appropriately to new situations, is of major importance for animals. Neural deviance detection describes a change of neural response strength to a stimulus solely caused by the stimulus' probability of occurrence. In the present study, we searched for correlates of deviance detection in auditory brainstem responses obtained in anaesthetised bats (Carollia perspicillata). In an oddball paradigm, we used two pure tone stimuli that represented the main frequencies used by the animal during echolocation (60 kHz) and communication (20 kHz). For both stimuli, we could demonstrate significant differences of response strength between deviant and standard response in slow and fast components of the auditory brainstem response. The data suggest the presence of correlates of deviance detection in brain stations below the inferior colliculus (IC), at the level of the cochlea nucleus and lateral lemniscus. Additionally, our results suggest that deviance detection is mainly driven by repetition suppression in the echolocation frequency band, while in the communication band, a deviant-related enhancement of the response plays a more important role. This finding suggests a contextual dependence of the mechanisms underlying subcortical deviance detection. The present study demonstrates the value of auditory brainstem responses for studying deviance detection and suggests that auditory specialists, such as bats, use different frequency-specific strategies to ensure an appropriate sensation of unexpected sounds.

Male Carollia perspicillata bats call more than females in a distressful context.

Distress calls are a vocalization type widespread across the animal kingdom, emitted when the animals are under duress, e.g. when captured by a predator. Here, we report on an observation we came across serendipitously while recording distress calls from the bat species Carollia perspicillata, i.e. the existence of sex difference in the distress calling behaviour of this species. We show that in C. perspicillata bats, males are more likely to produce distress vocalizations than females when hand-held. Male bats call more, their calls are louder, harsher (faster amplitude modulated) and cover lower carrier frequencies than female vocalizations. We discuss our results within a framework of potential hormonal, neurobiological and behavioural differences that could explain our findings, and open multiple paths to continue the study of sex-related differences in vocal behaviour in bats.

Auditory brainstem responses in the bat Carollia perspicillata: threshold calculation and relation to audiograms based on otoacoustic emission measurement.

An objective method to evaluate auditory brainstem-evoked responses (ABR) based on the root-mean-square (rms) amplitude of the measured signal and bootstrapping procedures was used to determine threshold curves (see Lv et al. in Med Eng Phys 29:191-198, 2007; Linnenschmidt and Wiegrebe in Hear Res 373:85-95, 2019). The rms values and their significance for threshold determination depended strongly on the filtering of the signal. Using the minimum threshold values obtained at three different low-frequency filter corner frequencies (30, 100, 300 Hz), ABR threshold curves were calculated. The course of the ABR thresholds was comparable to that of published DPOAE (distortion-product otoacoustic emission) thresholds based on a - 10 dB SPL threshold criterion for the 2f1-f2 emission (Schlenther et al. in J Assoc Res Otolaryngol 15:695-705, 2014, frequency range 10-90 kHz). For frequencies between 20 and 80 kHz, which is the most sensitive part of the bat's audiogram, median thresholds ranged between 10 and 28 dB SPL, and the DPOAE thresholds ranged between 10 and 23 dB SPL. At frequencies below 20 kHz (5-20 kHz) and above 80 kHz (80-120 kHz), ABR thresholds increased by 20 dB/octave and 45 dB/octave, respectively. We conclude that the combination of objective threshold determination and multiple filtering of the signal gives reliable ABR thresholds comparable to cochlear threshold curves.