Biology subjects

Hechavarria, J. C.

Publications and source records attributed to Hechavarria, J. C..

At least 19 recordsLinked to original sources

bioRxiv2026

Bats use Dip Echolocation to overcome rhythmic noise

Active sensing systems are known to adapt the structure of sensory signals. Whether they can improve perception by controlling when sensory information is acquired remains unclear. We show that echolocating fruit bats exposed to rhythmic noise preferentially emit calls during recurring low-noise periods, a behaviour we term "dip echolocation". Dip echolocation occurred in laboratory and wild bats and represents an active-sensing analogue of dip listening in humans. A normative model showed that temporal positioning of calls emerges from a trade-off between sensory information and energetic cost, alongside concurrent adaptations of call structure. Pharmacological inactivation of the frontal auditory field disrupted precise temporal control, implicating a role for frontal cortical circuits in adaptive vocal timing. These findings identify adaptive vocal timing as an active-sensing strategy for overcoming acoustic interference.

animal behavior and cognition↗

bioRxiv2026

Vocal production differentially affects fast- and broad-spiking neurons in auditory cortex

Vocalization, foundational for information exchange in animals, is supported by vocalization-modulated neurons that occur across species and brain areas. These neurons are typically studied in an undifferentiated manner, despite the heterogeneous nature of the cortical circuitry regarding cell types. Overlooking this diversity risks producing incomplete models of cortical function. Here, we address this challenge by studying large-scale, cell-type specific auditory cortical activity during vocalization in the bat Carollia perspicillata, a vocal specialist. We discovered that vocalisation-related modulatory effects in the auditory cortex, a critical attribute of the underlying circuit, differ starkly between putative inhibitory and pyramidal neurons. During calling, novel cell assemblies and temporal spiking patterns emerge wherein inhibitory cells play a pivotal role. Further, vocalization-specific neural decorrelations affect inhibitory cells most strongly. Together, these results demonstrate that vocalization-related neuronal activity is cell-type specific at the single- and multi-cellular levels of cortical organisation and highlight the importance of inhibitory neurons for auditory cortical dynamics during vocal production.

neuroscience↗

bioRxiv2025

Neurons in the bat auditory cortex encode class and complexity of future vocalizations

Vocal production is a complex behavior across the animal kingdom that relies on coordinated motor and auditory networks. However, the contribution of sensory areas in vocal control remains poorly understood. Here, we investigated vocalization-related activity in a major auditory processing area in the mammalian brain, the auditory cortex. We recorded neuronal spike rates in an audio-vocal specialist, the bat Carollia perspicillata, which emits vocalizations to echolocate and for social communication. We found distinct spike patterns encoding echolocation and communication calls several hundred milliseconds before vocal onset. Neuronal activity not only contained information about the vocalization category, but also reflected temporal complexity, specifically the syllable amount in a communication sequence. These vocalization-specific firing patterns were dependent on the neurons frequency receptive field. Our results indicate that single neurons in the auditory cortex not only process acoustic information but also encode the class and temporal structure of future vocal output.

neuroscience↗

bioRxiv2025

Inhibition of the neurodevelopmental disorder-associated 16p11.2 gene QPRT leads to altered cell type distribution in human stem cell-derived cerebral organoids

The 16p11.2 gene QPRT, encoding a key enzyme of the kynurenine pathway, has been linked to neurodevelopmental disorders including autism spectrum disorder (ASD). To investigate its role in early human brain development, we inhibited QPRT in stem cell-derived cerebral organoids. QPRT inhibition resulted in reduced organoid size, driven by premature neural differentiation resulting in depleted progenitor populations. Single-cell transcriptomics revealed an excitation/inhibition imbalance, with reduced excitatory and increased inhibitory neuron populations. We observed metabolic stress signatures, including pseudo-hypoxia, oxidative stress, and mitochondrial dysfunction, likely linked to NAD+ depletion and QUIN accumulation following QPRT inhibition. Notably, downregulation of LHX2 and PRDX1 may underlie impaired neural patterning and excitotoxic vulnerability. In addition, we report astrocytic and radial glia dysfunctions, indicating broad effects across multiple cell types. Disease gene enrichment analyses showed significant overlap with ASD-associated genes, especially during early differentiation. These findings suggest the loss or reduction of QPRT to shift neural development and neuronal homeostasis towards an imbalance in excitatory and inhibitory neuronal populations, a mechanism previously associated with neurodevelopmental disorders.

cell biology↗

bioRxiv2025

Responses to oddball communication sequences in the bat frontal and auditory cortices

Stimulus-specific adaptation (SSA) is a ubiquitous phenomenon in the animal kingdom across sensory modalities, but this type of neural response has rarely been studied using natural sounds in the auditory brain. Here, we leveraged the well-documented acoustic repertoire of the bat species Carollia perspicillata to study adaptation in the bat brain using natural communication sounds. We searched for SSA in single neuron spiking activity measured in two brain areas simultaneously: the auditory cortex and the frontal auditory field. The stimuli consisted of natural distress syllables, a form of vocalization produced by bats under duress. Bat distress vocalizations signal different degrees of urgency based on their amplitude modulation pattern, without large differences in their spectral structure. These distress vocalizations make an ideal test case for exploring the limits of neural deviance detection when considering naturalistic soundscapes with low stimulus contrast. The results show limited evidence for stimulus-specific adaptation in response to natural sound sequences in the majority of neurons studied. Many neurons did show a prominent effect related to context-dependent changes, caused by the type of sounds that occurred most frequently within each oddball sequence. Context-dependent responses were strongest in frontal neurons. Decoding analysis showed the existence of neural populations in both frontal and auditory cortices, which could distinguish between deviants and standards occurring within the same sequence, without large changes in evoked spike counts. Taken together, our results highlight the diversity of neural mechanisms complementing classical stimulus-specific adaptation when encoding natural vocalizations that do not differ markedly in their spectral composition.

neuroscience↗

bioRxiv2025

Do it yourself: Creating 3D brain-surface models and custom-made brain matrices for guided sectioning using photogrammetry and three-dimensional printing technology

Neuroethologists study many non-model animals. The development of techniques for precise and standardized histological brain analysis is key for understanding neural mechanisms across species. Here we present a novel cost-effective approach combining photogrammetry and three-dimensional printing technology to generate 3D brain surface models and produce species-specific brain matrices for precise and reproducible trimming, blocking, and sectioning of brain tissue. Using this strategy, we generated the first 3D brain surface model and brain matrix for Sebas short-tailed fruit bat Carollia perspicillata, CP. We generated the 3D brain surface model with the open-source 3D graphics suite Blender and its inexpensive photogrammetry plug-in Snapmesh. High-quality photographs of two male CP brains were used for the 3D-reconstruction, resulting in a 3D surface model. Photogrammetry thus offers a viable, cheap alternative to techniques otherwise requiring access to costly 3D- or CT-scanners. The brain matrix was then modeled using Blender, and printed using a 3D printer. Our brain matrix facilitates and standardizes trimming or blocking of brains, providing consistent access to brain regions of CP in the sagittal and coronal planes. Using this workflow, brain surface models and brain matrices can be produced from brains without tissue loss. Our approach provides an affordable, and tissue-preserving alternative for the generation of 3D brain surface models and brain matrices and will benefit researchers globally, especially those with limited funding, no access to scanners or working with particularly valuable specimen.

neuroscience↗

bioRxiv2024

Comparative single-cell analyses reveal evolutionary repurposing of a conserved gene program in bat wing development

Bats are the only mammals capable of self-powered flight, an evolutionary innovation based on the transformation of forelimbs into wings. The bat wing is characterized by an extreme elongation of the second to fifth digits and a wing membrane called chiropatagium connecting them. Here we investigated the developmental and cellular origin of this structure by comparing bat and mouse limbs using omics tools and single-cell analyses. Despite the substantial morphological differences between the species, we observed an overall conservation of cell populations and gene expression patterns including interdigital apoptosis. Single-cell analyses of micro-dissected embryonic chiropatagium identified a specific fibroblast population, independent of apoptosis-associated interdigital cells, as the origin of this tissue. These distal cells express a conserved gene program including the transcription factors MEIS2 and TBX3, which are commonly known to specify and pattern the early proximal limb. Transgenic ectopic expression of MEIS2 and TBX3 in mouse distal limb cells resulted in the activation of genes expressed during wing development and phenotypic changes related to wing morphology, such as the fusion of digits. Our results elucidate fundamental molecular mechanisms of bat wing development and illustrate how drastic morphological changes can be achieved through repurposing of existing developmental programs during evolution.

evolutionary biology↗

bioRxiv2024

Echo-locate: Cerebellar activity predicts vocalization in fruit bats

Echolocating bats exhibit remarkable auditory behaviors, enabled by adaptations within and outside their auditory system. Yet, research in echolocating bats has focused mostly on brain areas that belong to the classic ascending auditory pathway. This study provides direct evidence linking the cerebellum, an evolutionarily ancient and non-classic auditory structure, to vocalization and hearing. We report that in the fruit-eating bat Carollia perspicillata, external sounds can evoke cerebellar responses with latencies below 20 ms. Such fast responses are indicative of early inputs to the bat cerebellum. In vocalizing bats, distinct spike train patterns allow the prediction with over 85% accuracy of the sound they are about to produce, or have just produced, i.e., communication calls or echolocation pulses. Taken together, our findings provide evidence of specializations for vocalization and hearing in the cerebellum of an auditory specialist. TeaserThe cerebellum of fruit-eating bats responds to sounds and predicts future and past vocalizations

neuroscience↗

bioRxiv2023

Deviance detection in subthalamic neural population responses to natural stimuli in 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 multiple species, from subthalamic areas to auditory cortex. While cortical deviance detection has been well characterised by a range of studies covering neural activity at population level (mismatch negativity, MMN) as well as at cellular level (stimulus-specific adaptation, SSA), subcortical deviance detection has been studied mainly on cellular level in the form of SSA. 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 hearing specialist: the bat Carollia perspicillata. Our present approach uses behaviourally relevant vocalisation stimuli that are closer to the animals natural soundscape than artificial stimuli used in previous studies that focussed on subcortical areas. 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 behavioural 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 at population level, the bat brain can detect different types of deviants already in the brainstem. This shows that subthalamic brain structures exhibit more advanced forms of deviance detection than previously known.

neuroscience↗

bioRxiv2023

Oscillatory waveform shape and temporal spike correlations differ across bat frontal and auditory cortex

Neural oscillations are associated with diverse computations in the mammalian brain. The waveform shape of oscillatory activity measured in cortex relates to local physiology, and can be informative about aberrant or dynamically changing states. However, how waveform shape differs across distant yet functionally and anatomically related cortical regions is largely unknown. In this study, we capitalize on simultaneous recordings of local field potentials (LFPs) in the auditory and frontal cortices of awake, male Carollia perspicillata bats to examine, on a cycle-by-cycle basis, waveform shape differences across cortical regions. We find that waveform shape differs markedly in the fronto-auditory circuit even for temporally correlated rhythmic activity in comparable frequency ranges (i.e. in the delta and gamma bands) during spontaneous activity. In addition, we report consistent differences between areas in the variability of waveform shape across individual cycles. A conceptual model predicts higher spike-spike and spike-LFP correlations in regions with more asymmetric shape, a phenomenon that was observed in the data: spike-spike and spike-LFP correlations were higher in frontal cortex. The model suggests a relationship between waveform shape differences and differences in spike correlations across cortical areas. Altogether, these results indicate that oscillatory activity in frontal and auditory cortex possess distinct dynamics related to the anatomical and functional diversity of the fronto-auditory circuit. Significance statementThe brain activity of many animals displays intricate oscillations, which are usually characterized in terms of their frequency and amplitude. Here, we study oscillations from the bat frontal and auditory cortices on a cycle-by-cycle basis, additionally focusing on their characteristic waveform shape. The study reveals clear differences across regions in waveform shape and oscillatory regularity, even when the frequency of the oscillations is similar. A conceptual model predicts that more asymmetric waveforms result from stronger correlations between neural spikes and electrical field activity. Such predictions were supported by the data. The findings shed light onto the unique properties of different cortical areas, providing key insights into the distinctive physiology and functional diversity within the fronto-auditory circuit.

neuroscience↗

bioRxiv2023

Flexible control of vocal timing in bats enables escape from acoustic interference

In natural environments, background noise can degrade the integrity of acoustic signals, posing a problem for animals that rely on their vocalizations for communication and navigation. A simple behavioral strategy to combat acoustic interference would be to restrict call emissions to periods of low-amplitude or no noise. Using audio playback and computational tools for the automated detection of over 2.5 million vocalizations from groups of freely vocalizing bats, we show that bats (Carollia perspicillata) can dynamically adapt the timing of their calls to avoid acoustic jamming in both predictably and unpredictably patterned noise. This study demonstrates that bats spontaneously seek out temporal windows of opportunity for vocalizing in acoustically crowded environments, providing a mechanism for efficient echolocation and communication in cluttered acoustic landscapes. One Sentence SummaryBats avoid acoustic interference by rapidly adjusting the timing of vocalizations to the temporal pattern of varying noise.

animal behavior and cognition↗

bioRxiv2023

Amplitude modulation pattern of rat distress vocalisations during fear conditioning

In humans, screams have strong amplitude modulations (AM) at 30 to 150 Hz. These AM correspond to the acoustic correlate of perceptual roughness. In bats, distress calls can carry AMs, which elicit heart rate increases in playback experiments. Whether amplitude modulation occurs in fearful vocalisations of other animal species beyond humans and bats remains unknown. Here we analysed the AM pattern of rats 22-kHz ultrasonic vocalisations emitted in a fear conditioning task. We found that the number of vocalisations decreases during the presentation of conditioned stimuli. We also observed that AMs do occur in rat 22-kHz vocalisations. AMs are stronger during the presentation of conditioned stimuli, and during escape behaviour compared to freezing. Our results suggest that the presence of AMs in vocalisations emitted could reflect the animals internal state of fear related to avoidance behaviour.

animal behavior and cognition↗

bioRxiv2022

The auditory cortex of bats has a better signal to noise ratio and lower inter-trial variability in response to stimuli trains than mice

The brains of black 6 mice (Mus musculus) and Sebas short-tailed bats (Carollia perspicillata) weigh roughly the same and share mammalian neocortical laminar architecture. Bats have highly developed sonar calls and social communication and are an excellent neuroethological animal model for auditory research. Mice are olfactory and somatosensory specialists, used frequently in auditory neuroscience for their advantage of standardization and wide genetic toolkit. This study presents an analytical approach to overcome the challenge of inter-species comparison with existing data. In both data sets, we recorded with linear multichannel electrodes down the depth of the primary auditory cortex (A1) while presenting repetitive stimuli trains at ~5 and ~40 Hz to awake bats and mice. We found that while there are similarities between cortical response profiles in both, there was a better signal to noise ratio in bats under these conditions, which allowed for a clearer following response to stimuli trains. Model fit analysis supported this, illustrating that bats had stronger response amplitude suppression to consecutive stimuli. Additionally, continuous wavelet transform revealed that bats had significantly stronger power and phase coherence during stimulus response and mice had stronger power in the background. Better signal to noise ratio and lower intertrial phase variability in bats could represent specialization for faster and more accurate temporal processing at lower metabolic costs. Our findings demonstrate a potentially different general auditory processing principle; investigating such differences may increase our understanding of how the ecological need of a species shapes the development and function of its nervous system.

neuroscience↗

bioRxiv2021

Dynamic cortico-cortical information transfer regimes during vocalization

The mammalian frontal and auditory cortices are important for vocal behaviour. Here, using local field potential recordings, we demonstrate for the first time that the timing and spatial pattern of oscillations in the fronto-auditory cortical network of vocalizing bats (Carollia perspicillata) predict the purpose of vocalization: echolocation or communication. Transfer entropy analyses revealed predominantly top-down (frontal-to-auditory cortex) information flow during spontaneous activity and pre-vocal periods. The dynamics of information flow depended on the behavioural role of the vocalization and on the timing relative to vocal onset. Remarkably, we observed the emergence of predominantly bottom-up (auditory-to-frontal cortex) information transfer patterns specific echolocation production, leading to self-directed acoustic feedback. Electrical stimulation of frontal areas selectively enhanced responses to echolocation 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.

neuroscience↗

bioRxiv2021

Acoustic context modulates natural sound discrimination in auditory cortex through frequency specific adaptation

Vocal communication is essential to coordinate social interactions in mammals and it requires a fine discrimination of communication sounds. Auditory neurons can exhibit selectivity for specific calls, but how it is affected by preceding sounds is still debated. We tackled this using ethologically relevant vocalizations in a highly vocal mammalian species: Sebas short-tailed bat. We show that cortical neurons present several degrees of selectivity for echolocation and distress calls. Embedding vocalizations within natural acoustic streams leads to stimulus-specific suppression of neuronal responses that changes sound selectivity in disparate manners: increases in neurons with poor discriminability in silence and decreases in neurons selective in silent settings. A computational model indicates that the observed effects arise from two forms of adaptation: presynaptic frequency specific adaptation acting in cortical inputs and stimulus unspecific postsynaptic adaptation. These results shed light into how acoustic context modulates natural sound discriminability in the mammalian cortex.

neuroscience↗

bioRxiv2020

Phase-amplitude coupling profiles differ in frontal and auditory cortices

Neural oscillations are at the core of important computations in the mammalian brain. Interactions between oscillatory activities in different frequency bands, such as delta (1-4 Hz), theta (4-8 Hz), or gamma (>30 Hz), are a powerful mechanism for binding fundamentally distinct spatiotemporal scales of neural processing. Phase-amplitude coupling (PAC) is one such plausible and well-described interaction, but much is yet to be uncovered regarding how PAC dynamics contribute to sensory representations. In particular, although PAC appears to have a major role in audition, the characteristics of coupling profiles in sensory and integration (i.e. frontal) cortical areas remain obscure. Here, we address this question by studying PAC dynamics in the frontal-auditory field (FAF; an auditory area in the bat frontal cortex) and the auditory cortex (AC) of the bat Carollia perspicillata. By means of simultaneous electrophysiological recordings in frontal and auditory cortices examining local-field potentials (LFPs), we show that the amplitude of gamma-band activity couples with the phase of low-frequency LFPs in both structures. Our results demonstrate that the coupling in FAF occurs most prominently in delta/high-gamma frequencies (1-4/75-100 Hz), whereas in the AC the coupling is strongest in the theta/low-gamma (2-8/25-55 Hz) range. We argue that distinct PAC profiles may represent different mechanisms for neuronal processing in frontal and auditory cortices, and might complement oscillatory interactions for sensory processing in the frontal-auditory cortex network.

neuroscience↗

bioRxiv2019

Fronto-temporal coupling dynamics during spontaneous activity and auditory processing

Most mammals rely on the extraction of acoustic information from the environment in order to survive. However, the mechanisms that support sound representation in auditory neural networks involving sensory and association brain areas remain underexplored. In this study, we address the functional connectivity between an auditory region in frontal cortex (the frontal auditory field, FAF) and the auditory cortex (AC) in the bat Carollia perspicillata. The AC is a classic sensory area central for the processing of acoustic information. On the other hand, the FAF belongs to the frontal lobe, a brain region involved in the integration of sensory inputs, modulation of cognitive states, and in the coordination of behavioural outputs. The FAF-AC network was examined in terms of oscillatory coherence (local-field potentials, LFPs), and within an information theoretical framework linking FAF and AC spiking activity. We show that in the absence of acoustic stimulation, simultaneously recorded LFPs from FAF and AC are coherent in low frequencies (1-12 Hz). This "default" coupling was strongest in deep AC layers and was unaltered by acoustic stimulation. However, presenting auditory stimuli did trigger the emergence of coherent auditory-evoked gamma-band activity (>25 Hz) between the FAF and AC. In terms of spiking, our results suggest that FAF and AC engage in distinct coding strategies for representing artificial and natural sounds. Taken together, our findings shed light onto the neuronal coding strategies and functional coupling mechanisms that enable sound representation at the network level in the mammalian brain.

neuroscience↗

bioRxiv2019

Enhanced representation of natural sound sequences in the ventral auditory midbrain

SummaryThe auditory midbrain (inferior colliculus, IC) plays an important role in sound processing, acting as hub for acoustic information extraction and for the implementation of fast audio-motor behaviors. IC neurons are topographically organized according to their sound frequency preference: dorsal IC regions encode low frequencies while ventral areas respond best to high frequencies, a type of sensory map defined as tonotopy. Tonotopic maps have been studied extensively using artificial stimuli (pure tones) but our knowledge of how these maps represent information about sequences of natural, spectro-temporally rich sounds is sparse. We studied this question by conducting simultaneous extracellular recordings across IC depths in awake bats (Carollia perspicillata) that listened to sequences of natural communication and echolocation sounds. The hypothesis was that information about these two types of sound streams is represented at different IC depths since they exhibit large differences in spectral composition, i.e. echolocation covers the high frequency portion of the bat soundscape (> 45 kHz), while communication sounds are broadband and carry most power at low frequencies (20-25 kHz). Our results showed that mutual information between neuronal responses and acoustic stimuli, as well as response redundancy in pairs of neurons recorded simultaneously, increase exponentially with IC depth. The latter occurs regardless of the sound type presented to the bats (echolocation or communication). Taken together, our results indicate the existence of mutual information and redundancy maps at the midbrain level whose response cannot be predicted based on the frequency composition of natural sounds and classic neuronal tuning curves.

neuroscience↗