Processing of acoustic motion in the auditory cortex of the rufous horseshoe bat, Rhinolophus rouxi

This study investigated the representation of acoustic motion in different fields of auditory cortex of the rufous horseshoe bat, Rhinolophus rouxi. Motion in horizontal direction (azimuth) was simulated using successive stimuli with dynamically changing interaural intensity differences presented via earphones. The mechanisms underlying a specific sensitivity of neurons to the direction of motion were investigated using microiontophoretic application of γ-aminobutyric acid (GABA) and the GABAA receptor antagonist bicuculline methiodide (BMI). In the first part of the study, responses of a total of 152 neurons were recorded. Seventy-one percent of sampled neurons were motion-direction sensitive. Two types of responses could be distinguished. Thirty-four percent of neurons showed a directional preference exhibiting stronger responses to one direction of motion. Fifty-seven percent of neurons responded with a shift of spatial receptive field position depending on the direction of motion. Both effects could occur in the same neuron depending on the parameters of apparent motion. Most neurons with contralateral receptive fields exhibited directional preference only with motion entering the receptive field from the opposite direction (i.e. the ipsilateral part of the azimuth). Receptive field shifts were opposite to the direction of motion. Specific combinations of spatio-temporal parameters determined the motion-direction-sensitive responses. Velocity was not encoded as a specific parameter. Temporal parameters of motion and azimuthal position of the moving sound source were differentially encoded by neurons in different fields of auditory cortex. Neurons with a directional preference in the dorsal fields can encode motion with short interpulse intervals, whereas direction preferring neurons in the primary field can best encode motion with medium interpulse intervals. Furthermore, neurons with a directional preference in the dorsal fields are specialized for encoding motion in the midfield of azimuth, whereas direction preferring neurons in the primary field can encode motion in lateral positions. In the second part of the study, responses were recorded from additional 69 neurons. Microiontophoretic application of BMI influenced the motion-direction sensitivity of 53 % of neurons. In 21 % of neurons the motion-direction sensitivity was decreased by BMI by decreasing either directional preference or receptive field shift. In neurons with a directional preference, BMI increased the spike number for the preferred direction in about the same amount as for the non-preferred direction. Thus, inhibition was not direction specific. In contrast, BMI increased motion-direction sensitivity by either increasing directional preference or magnitude of receptive field shifts in 22 % of neurons. An additional 10 % of neurons changed their response from a receptive field shift to a directional preference under BMI. In these 32 % of neurons, the observed effects could often be better explained by adaptation of excitation than by inhibition. The results suggest, that motion information is differentially processed in different fields of the auditory cortex of the rufous horseshoe bat. Thus, functionally organized pathways for the processing of different parameters of auditory motion seem to exist. The fact that cortex specific GABAergic inhibition contributes to motion-direction sensitivity in at least a part of cortical neurons is supportive for the notion that the auditory cortex plays an important role in further processing the neural responses to apparent motion brought up from lower levels of the auditory pathway.In der vorliegenden Arbeit wurde die neuronale Repräsentation von akustischer Bewegungsinformation in verschiedenen Feldern des Hörkortex der Hufeisennasen- Fledermaus Rhinolophus rouxi untersucht. Bewegungen einer Schallquelle in der Horizontalebene wurden durch aufeinanderfolgende Stimuli mit sich dynamisch verändernden interauralen Intensitätsdifferenzen simuliert. Die Stimuli wurden über Ohrhörer dargeboten. Die Mechanismen die der Bewegungsrichtungsselektivität von Neuronen zu Grunde liegen, wurden mit Hilfe von mikroiontophoretischer Applikation von γ-Amino-buttersäure (GABA) und dem GABAA-Rezeptor Antagonisten Bicucullinmethiodid (BMI) untersucht. Im ersten Teil der Arbeit wurden Ableitungen von insgesamt 152 Neuronen erhalten. 71 % der Zellen waren bewegungsrichtungssensitiv. Dabei konnten zwei verschiedene Typen unterschieden werden: Bei 34 % aller Neurone zeigte sich eine Richtungsabhängigkeit in der Antwortamplitude. Die Zellen antworteten bevorzugt auf nur eine Bewegungsrichtung. Bei Zellen mit einem contralateralen rezeptiven Feld war dies eine Bewegung von der entgegengesetzten Seite (d.h. der ipsilateralen Seite) in das rezeptive Feld hinein. 57 % aller Neurone zeigten als richtungsabhängige Antwort eine Verschiebung der räumlichen Position des rezeptiven Feldes. Die Verschiebung war der Bewegungsrichtung entgegengesetzt. Beide Effekte konnten zusammen bei einer Nervenzelle beobachtet werden. Welcher der beiden Effekte auftrat, hing von den Parametern der Bewegung ab. Bestimmte Kombinationen von räumlichen und zeitlichen Bewegungsparametern bestimmten die Art der neuronalen richtungsabhängigen Antworten, die Bewegungsgeschwindigkeit wurde nicht als spezifische Größe in der Antwort kodiert. Zeitliche Parameter und die Position der Bewegung einer Schallquelle in der Horizontalebene wurden in verschiedenen Feldern des Hörkortex spezifisch verarbeitet. Neurone in den dorsalen Feldern zeigten ihre größte Richtungspräferenz bei Bewegungen mit kurzen Interpulsintervallen, wohingegen Zellen im primären Feld mittlere Interpulsintervalle bevorzugten. Weiterhin zeigten Neurone mit Richtungspräferenz in den dorsalen Feldern ihre maximale Antwort in mittleren Bereichen der Horizontalebene, während Zellen im primären Feld stärker auf seitliche Bereiche abgestimmt waren. Im zweiten Teil der vorliegenden Arbeit wurden die neuronalen Antworten von 69 weiteren Zellen abgeleitet. Die mikroiontophoretische Applikation von BMI beeinflußte das bewegungsrichtungssensitive Antwortverhalten von 53 % der Neurone. Bei 21 % der Zellen verringerte BMI die Bewegungsrichtungssensitivität. Es wurde entweder die Stärke der Richtungspräferenz oder die Größe der Verschiebung der räumlichen rezeptiven Felder verkleinert. Bei Zellen mit Richtungspräferenz erhöhte BMI die Antwortstärke für beide Bewegungsrichtungen in ungefähr dem gleichen Ausmaß. Es lag also keine richtungsspezifische Hemmung vor. Im Gegensatz dazu vergrößerte BMI bei 22 % der Neurone die Bewegungsrichtungssensitivität, entweder durch Vergrößerung der Richtungspräferenz oder durch Vergrößerung der Verschiebung der rezeptiven Felder. Weitere 10 % der Neurone veränderten ihre Antworteigenschaften durch BMI. Zeigten diese Zellen ohne BMI eine Verschiebung der räumlichen rezeptiven Felder, so konnte der Antworttyp mit BMI besser als Richtungspräferenz beschrieben werden. Bei diesen 32 % der Neurone konnten die beobachteten Effekte von BMI eher mit Adaptationsvorgängen erklärt werden, als durch den spezifischen Einfluß von GABAerger Hemmung. Die Ergebnisse lassen den Schluß zu, daß akustische Bewegungsinformation spezifisch in verschiedenen Feldern des Hörkortex von Rhinolophus rouxi verarbeitet wird. Es scheinen funktionell organisierte Verarbeitungswege für die verschiedenen Parameter akustischer Bewegungsinformation zu existieren. Die Tatsache, daß kortexspezifische Inhibition zumindest bei einem Teil der Neurone zur Bewegungsrichtungssensitivität beiträgt, unterstützt die Annahme, daß der Hörkortex eine wichtige Rolle bei der weiteren Verarbeitung der neuronalen Antworten auf bewegte Schallreize aus anderen Stationen der Hörbahn spielt

A novel approach identifies the first transcriptome networks in bats: a new genetic model for vocal communication

Background: Bats are able to employ an astonishingly complex vocal repertoire for navigating their environment and conveying social information. A handful of species also show evidence for vocal learning, an extremely rare ability shared only with humans and few other animals. However, despite their potential for the study of vocal communication, bats remain severely understudied at a molecular level. To address this fundamental gap we performed the first transcriptome profiling and genetic interrogation of molecular networks in the brain of a highly vocal bat species, Phyllostomus discolor. Results: Gene network analysis typically needs large sample sizes for correct clustering, this can be prohibitive where samples are limited, such as in this study. To overcome this, we developed a novel bioinformatics methodology for identifying robust co-expression gene networks using few samples (N=6). Using this approach, we identified tissue-specific functional gene networks from the bat PAG, a brain region fundamental for mammalian vocalisation. The most highly connected network identified represented a cluster of genes involved in glutamatergic synaptic transmission. Glutamatergic receptors play a significant role in vocalisation from the PAG, suggesting that this gene network may be mechanistically important for vocal-motor control in mammals. Conclusion: We have developed an innovative approach to cluster co-expressing gene networks and show that it is highly effective in detecting robust functional gene networks with limited sample sizes. Moreover, this work represents the first gene network analysis performed in a bat brain and establishes bats as a novel, tractable model system for understanding the genetics of vocal mammalian communication

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

Open Access funding enabled and organized by Projekt DEAL. This work was supported by the Human Frontier Science Program (Grant RGP0058 to UF).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.Publisher PDFPeer reviewe

Object-Oriented Echo Perception and Cortical Representation in Echolocating Bats

Echolocating bats can identify three-dimensional objects exclusively through the analysis of acoustic echoes of their ultrasonic emissions. However, objects of the same structure can differ in size, and the auditory system must achieve a size-invariant, normalized object representation for reliable object recognition. This study describes both the behavioral classification and the cortical neural representation of echoes of complex virtual objects that vary in object size. In a phantom-target playback experiment, it is shown that the bat Phyllostomus discolor spontaneously classifies most scaled versions of objects according to trained standards. This psychophysical performance is reflected in the electrophysiological responses of a population of cortical units that showed an object-size invariant response (14/109 units, 13%). These units respond preferentially to echoes from objects in which echo duration (encoding object depth) and echo amplitude (encoding object surface area) co-varies in a meaningful manner. These results indicate that at the level of the bat's auditory cortex, an object-oriented rather than a stimulus-parameter–oriented representation of echoes is achieved

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

Funding: UK Research and Innovation (Grant Number(s): MR/T021985/1; Grant recipient(s): Sonja Vernes). Max-Planck-Gesellschaft (Grant Number(s): Max Planck Research Group ; Grant recipient(s): Sonja Vernes). Human Frontier Science Program (Grant Number(s): RGP0058/2016, RGP0058/2016; Grant recipient(s): Uwe Firzlaff, Sonja Vernes).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.Publisher PDFPeer reviewe

Dominant Glint Based Prey Localization in Horseshoe Bats: A Possible Strategy for Noise Rejection

Rhinolophidae or Horseshoe bats emit long and narrowband calls. Fluttering insect prey generates echoes in which amplitude and frequency shifts are present, i.e. glints. These glints are reliable cues about the presence of prey and also encode certain properties of the prey. In this paper, we propose that these glints, i.e. the dominant glints, are also reliable signals upon which to base prey localization. In contrast to the spectral cues used by many other bats, the localization cues in Rhinolophidae are most likely provided by self-induced amplitude modulations generated by pinnae movement. Amplitude variations in the echo not introduced by the moving pinnae can be considered as noise interfering with the localization process. The amplitude of the dominant glints is very stable. Therefore, these parts of the echoes contain very little noise. However, using only the dominant glints potentially comes at a cost. Depending on the flutter rate of the insect, a limited number of dominant glints will be present in each echo giving the bat a limited number of sample points on which to base localization. We evaluate the feasibility of a strategy under which Rhinolophidae use only dominant glints. We use a computational model of the echolocation task faced by Rhinolophidae. Our model includes the spatial filtering of the echoes by the morphology of the sonar apparatus of Rhinolophus rouxii as well as the amplitude modulations introduced by pinnae movements. Using this model, we evaluate whether the dominant glints provide Rhinolophidae with enough information to perform localization. Our simulations show that Rhinolophidae can use dominant glints in the echoes as carriers for self-induced amplitude modulations serving as localization cues. In particular, it is shown that the reduction in noise achieved by using only the dominant glints outweighs the information loss that occurs by sampling the echo

The auditory cortex of the bat Phyllostomus discolor: Localization and organization of basic response properties

<p>Abstract</p> <p>Background</p> <p>The mammalian auditory cortex can be subdivided into various fields characterized by neurophysiological and neuroarchitectural properties and by connections with different nuclei of the thalamus. Besides the primary auditory cortex, echolocating bats have cortical fields for the processing of temporal and spectral features of the echolocation pulses. This paper reports on location, neuroarchitecture and basic functional organization of the auditory cortex of the microchiropteran bat <it>Phyllostomus discolor </it>(family: Phyllostomidae).</p> <p>Results</p> <p>The auditory cortical area of <it>P. discolor </it>is located at parieto-temporal portions of the neocortex. It covers a rostro-caudal range of about 4800 μm and a medio-lateral distance of about 7000 μm on the flattened cortical surface.</p> <p>The auditory cortices of ten adult <it>P. discolor </it>were electrophysiologically mapped in detail. Responses of 849 units (single neurons and neuronal clusters up to three neurons) to pure tone stimulation were recorded extracellularly. Cortical units were characterized and classified depending on their response properties such as best frequency, auditory threshold, first spike latency, response duration, width and shape of the frequency response area and binaural interactions.</p> <p>Based on neurophysiological and neuroanatomical criteria, the auditory cortex of <it>P. discolor </it>could be subdivided into anterior and posterior ventral fields and anterior and posterior dorsal fields. The representation of response properties within the different auditory cortical fields was analyzed in detail. The two ventral fields were distinguished by their tonotopic organization with opposing frequency gradients. The dorsal cortical fields were not tonotopically organized but contained neurons that were responsive to high frequencies only.</p> <p>Conclusion</p> <p>The auditory cortex of <it>P. discolor </it>resembles the auditory cortex of other phyllostomid bats in size and basic functional organization. The tonotopically organized posterior ventral field might represent the primary auditory cortex and the tonotopically organized anterior ventral field seems to be similar to the anterior auditory field of other mammals. As most energy of the echolocation pulse of <it>P. discolor </it>is contained in the high-frequency range, the non-tonotopically organized high-frequency dorsal region seems to be particularly important for echolocation.</p