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Henninger, J.

Publications and source records attributed to Henninger, J..

8 recordsLinked to original sources

Multimodal reference brain atlas of adult Danionella cerebrum

Mechanistic accounts of brain function require a common coordinate system in which structural, molecular and functional data can be integrated and compared across individuals. The teleost genus Danionella is unique among vertebrates in retaining lifelong transparency, allowing non-invasive, cellular-resolution functional imaging across the entire adult brain. A reference atlas in this model would therefore provide a strong foundation for causal and comparative circuit studies. Here we present an integrated anatomical, molecular and functional reference brain for adult Danionella cerebrum as a standardised atlas resource. Using a transgenic nuclear fluorescence marker, whole-mount tissue clearing and high-resolution two-photon microscopy, we generated an average reference brain from 21 adult fish to create a common coordinate system. Whole-mount in situ hybridisation for 29 neuronal markers, complemented by tract annotation from structural imaging and tracer injections, enabled us to segment 203 neuroanatomical regions. We found pronounced sex differences in telencephalic, cerebellar and hindbrain nuclei, revealing sexually dimorphic organisation across multiple brain regions. All data and segmentations are made openly accessible, providing a community resource for studies of circuit function, molecular makeup and sexual dimorphism in an optically accessible adult vertebrate brain.

neuroscience↗

Brain-wide hierarchical and sexually dimorphic tuning for social vocalizations

Vocal repertoires consist of a limited number of call types, even though their sounds can vary continuously in form. Where in the brain receivers partition this variation into discrete types is contested: different accounts place the emergence of categories in the cortex/pallium or already in the midbrain. Because recordings have been limited to isolated regions, it remains unknown whether this partitioning is confined to a single region at all, occurs in parallel across many, or is built up along the pathway. Here we present the first whole-brain, cellular-resolution analysis of how conspecific vocalizations are categorized in a vertebrate, using the glassfish Danionella cerebrum. We find that categorization is neither pallial nor localized. It begins at the first central auditory nuclei, much earlier than previously thought, where a continuous morph between social and non-social sounds evokes an abrupt switch in population activity. The midbrain then sharpens these representations, and the thalamus filters for species-typical pulse rates while splitting call duration into two discrete populations. Only downstream of this shared code do the sexes diverge in forebrain social nuclei. Call type partitioning is thus distributed and hierarchically assembled, rather than read out at any one stage.

neuroscience↗

Advances in non-invasive tracking of wave-type electric fish in natural and laboratory settings

Recent technological advances greatly improved the possibility to study freely behaving animals in natural conditions. However, many systems still rely on animal-mounted devices, which can already bias behavioral observations. Alternatively, animal behaviors can be detected and tracked in recordings of stationary sensors, e.g. video cameras. While these approaches circumvent the influence of animal-mounted devices, identification of individuals is much more challenging. We take advantage of the individual-specific electric fields electric fish generate by discharging their electric organ (EOD) to record and track their movement and communication behaviors without interfering with the animals themselves. EODs of complete groups of fish can be recorded with electrode arrays submerged in the water and then be tracked for individual fish. Here, we present an improved algorithm for tracking electric signals of wave-type electric fish with unprecedented accuracy. Our algorithm benefits from combining and refining previous approaches of tracking individual specific EOD frequencies (EODf) and spatial electric field properties. In this process, the similarity of signal pairs in extended data windows determines their tracking order, making the algorithm more robust against detection losses and intersections. We quantify the performance of the algorithm and show its application for a data set recorded with a 64-electrode array in a stream in the Llanos, Colombia, where we managed, for the first time, to track Apteronotus leptorhynchus over many days. These technological advances make electric fish a unique model system for a detailed analysis of social and communication behaviors, with strong implications for our research on sensory coding.

animal behavior and cognition↗

Brain-wide imaging of an adult vertebrate with image transfer oblique plane microscopy

Optical imaging is a powerful tool to visualise and measure neuronal activity. However, due to the size and opacity of vertebrate brains it has until now been impossible to simultaneously image neuronal circuits at cellular resolution across the entire adult brain. This is true even for the smallest known vertebrate brain in the teleost Danionella, which is still too large for existing volumetric imaging approaches. Here we introduce image transfer oblique plane microscopy, which uses a new optical refocusing solution via a custom fibre-optical faceplate, enabling a large field-of-view of up to 4 mm3 at a volume rate of 1 Hz. We demonstrate the power of this method with the first brain-wide recording of neuronal activity in an adult vertebrate.

neuroscience↗

Evolutionary divergence of locomotion in two related vertebrate species

Locomotion exists in diverse forms in nature and is adapted to the environmental constraints of each species1. However, little is known about how closely related species with similar neuronal circuitry can evolve different navigational strategies to explore their environments. We established a powerful approach in comparative neuroethology to investigate evolution of neuronal circuits in vertebrates by comparing divergent swimming pattern of two closely related larval fish species, Danionella translucida (DT) and Danio rerio or zebrafish (ZF)2,3. During swimming, we demonstrate that DT utilizes lower half tail-beat frequency and amplitude to generate a slower and continuous swimming pattern when compared to the burst-and-glide swimming pattern in ZF. We found a high degree of conservation in the brain anatomy between the two species. However, we revealed that the activity of a higher motor region, referred here as the Mesencephalic Locomotion Maintenance Neurons (MLMN) correlates with the duration of swim events and differs strikingly between DT and ZF. Using holographic stimulation, we show that the activation of the MLMN is sufficient to increase the frequency and duration of swim events in ZF. Moreover, we propose two characteristics, availability of dissolved oxygen and timing of swim bladder inflation, which drive the observed differences in the swim pattern. Our findings uncover the neuronal circuit substrate underlying the evolutionary divergence of navigational strategies and how they are adapted to their respective environmental constraints.

neuroscience↗

Tracking activity patterns of a multispecies community of gymnotiform weakly electric fish in their neotropical habitat

Field studies on freely behaving animals commonly require tagging and often are focused on single species. Weakly electric fish generate a species- and individual-specific electric organ discharge (EOD) and therefore provide a unique opportunity for individual tracking without tagging. We here present and test tracking algorithms based on recordings with submerged electrode arrays. Harmonic structures extracted from power spectra provide fish identity. Localization of fish based on weighted averages of their EOD amplitudes is found to be more robust than fitting a dipole model. We apply these techniques to monitor a community of three species, Apteronotus rostratus, Eigenmannia humboldtii, and Sternopygus dariensis, in their natural habitat in Darien, Panama. We found consistent upstream movements after sunset followed by downstream movements in the second half of the night. Extrapolations of these movements and estimates of fish density obtained from additional transect data suggest that some fish cover at least several hundreds of meters of the stream per night. Most fish, including Eigenmannia, were traversing the electrode array solitarily. From in-situ measurements of the decay of the EOD amplitude with distance of individual animals we estimated that fish can detect conspecifics at distances of up to 2 m. Our recordings also emphasize the complexity of natural electrosensory scenes resulting from the interactions of the EODs of different species. Electrode arrays thus provide an unprecedented window into the so-far hidden nocturnal activities of multispecies communities of weakly electric fish at an unmatched level of detail. Summary statementDetailed movement patterns and complex electrosensory scenes of three species of weakly electric fish were tracked without tagging using a submerged electrode array in a small Neotropical stream.

animal behavior and cognition↗

Simultaneous spike-time locking to multiple frequencies

Phase locking of neural firing is ubiquitously observed in the brain and occurs when neurons fire at a particular phase of a periodic signal. Here we study in detail how spikes of single neurons can simultaneously lock to multiple distinct frequencies at the example of p-type electroreceptor afferents in the electrosensory system of the Gymnotiform weakly electric fish Apteronotus leptorhynchus. We identify key elements for multiple frequency locking, study its determining factors and limits, and provide concise mathematical models reproducing our main findings. Our findings provide another example how rate and temporal codes can coexist and complement each other in single neurons, and demonstrate that sensory coding in p-type electroreceptor afferents provides a much richer representation of the sensory environment than commonly assumed. Since the underlying mechanisms are not specific to the electrosensory system, our results could provide the basis for studying multiple-frequency locking in other systems.

neuroscience↗

Court and spark in the wild: communication at the limits of sensation

Sensory systems evolve in the ecological niches each species is occupying. Accordingly, the tuning of sensory neurons is expected to be adapted to the statistics of natural stimuli. For an unbiased quantification of sensory scenes we tracked natural communication behavior of the weakly electric fish Apteronotus rostratus in their Neotropical rainforest habitat with high spatio-temporal resolution over several days. In the context of courtship and aggression we observed large quantities of electrocommunication signals. Echo responses and acknowledgment signals clearly demonstrated the behavioral relevance of these signals. The known tuning properties of peripheral electrosensory neurons suggest, however, that they are barely activated by these obviously relevant signals. Frequencies of courtship signals are clearly mismatched with the frequency tuning of neuronal population activity. Our results emphasize the importance of quantifying sensory scenes derived from freely behaving animals in their natural habitats for understanding the evolution and function of neural systems.

neuroscience↗