Biology subjects

Benda, J.

Publications and source records attributed to Benda, J..

13 recordsLinked to original sources

bioRxiv2026

Modelling individual ampullary afferents in two species of gymnotiform fish using simulation-based inference

Ampullary electroreceptors are widespread across aquatic vertebrates. The purpose of sensing exogeneous electric fields is conserved across species but the implementations differ and the encoding mechanisms remain incompletely understood. We compared baseline and stimulus-driven response properties of ampullary electroreceptor afferents in the weakly electric fish Apteronotus leptorhynchus and Eigenmannia virescens. We find that their activity is very well captured by an extended leaky integrate-and-fire model that generalizes across both species. The model shares similarities to a previous model of the tuberous electroreceptor afferents but further incorporates a low-pass pre-filtering and additional noise sources to reproduce the observed spectral response characteristics. The low-pass is essential to shape stimulus encoding in the high-frequency range. Accurate prediction of low-frequency stimulus encoding further requires two distinct noise sources: stimulus-independent white current noise and activity-dependent noise in the adaptation current, which is shaped by the adaptation time constant to yield pink noise dynamics. Using simulation-based inference, we trained a neural network to map model parameters to neuronal response features. This approach enables the generation of heterogeneous, biologically plausible model populations that may serve as a realistic input layer for studying neuronal processing on the next level. With this, we provide a unified and mechanistic model of ampullary electroreceptor encoding in these species and possibly beyond. The proposed model is another step towards a full model of the electrosensory periphery in these animals. Author summaryThe ability to sense exogenous electric fields, i.e. passive electroreception, is widespread among aquatic animals. It plays a central role in prey detection and, in some species, also contributes to communication. To understand higher-order brain function, we also need to grasp the sensory periphery and ideally have models that provide naturalistic peripheral responses. Using simulation-based inference (SBI), we here develop a mechanistic model of passive electroreception that is valid for at least two species of electric fish. Through detailed analyses, we identify model components, such as a source of pink noise, that are essential for matching the models spectral response properties to those of the recorded cells. The main results of this work are the model itself and the trained inference network (here called the SBI network), which can now be used to create artificial but biologically plausible populations of sensory neurons that may serve as a realistic input layer for studying higher-order neuronal processing. Our work complements the existing models of the active electric sense and is a big step towards a full model of the electrosensory periphery in these animals.

neuroscience↗

bioRxiv2025

Dissolved inorganic carbon driven dynamics of calcite shell formation in 12 strains of the freshwater algae Phacotus lenticularis (Chlorophyta)

This article explores the close relationship between dissolved inorganic carbonate ion concentration (DIC) and the calcification state of Phacotus lenticularis, a globally abundant freshwater phytoplankton that is responsible for a significant part of modern lake carbonate production during bloom formation. We cultured 12 freshly isolated P. lenticularis strains under an ecologically relevant range of DIC (0.2 to 12 mmol l-1 total scale) for 14 days. From this experiment we gained information on responses in shell formation and growth that highlight strong lower boundaries in morphometric calcite shell variables with regards to DIC. All P. lenticularis strains showed reduced shell thickness by up to 60 % and dissolved calcite crystals structures at declining DIC < 4 mmol l-1. Increasing DIC > 4 mmol l-1 had no significant effect on shell thickness and crystal length in the culture experiments. We found a significant preadaptation of all 12 strains to ambient DIC concentrations measured in their lake of origin, but no dependence of growth rates up to a lethal DIC of > 10 mmol l-1. The simulation experiments illustrate the close relationship between shell function and dissolved inorganic carbonate ion concentration in lakes and highlight the need of continued research of important roles in biogenic carbon transformation and storage in a future world.

ecology↗

bioRxiv2024

Tracking spatial patterns and nocturnal arousal in an undisturbed natural population of the pulse-type weakly electric fish Gymnotus omarorum

Assessing animals locomotor and activity-rest patterns in natural populations is challenging. It requires individual identification and behavioral tracking in sometimes complex and inaccessible environments. Weakly electric fish are advantageous models for remote monitoring due to their continuous emission of electric signals (EODs). Gymnotus omarorum is a South American freshwater pulse-type weakly electric fish. Previous manual recordings of restrained individuals in the wild showed a spatial distribution compatible with territoriality and a nocturnal increase in EOD rate interpreted as arousal. This interdisciplinary study presents the development of low-cost amplifiers for remote EOD recordings and the refinement of tracking algorithms that provide individual recognition of Gymnotus omarorum in the wild. We describe natural daily spacing patterns of undisturbed individuals that are compatible with territoriality, although heterogeneous across sampling sites, and confirm that all resident fish showed a robust nocturnal increase of EOD rate likely associated with daily variations of water temperature. HIGHLIGHTSO_LISuccessful remote individual tracking of wild pulse type weakly electric fish C_LIO_LIG. omarorum spacing patterns are compatible with known nocturnality and territoriality C_LIO_LIResidents keep their diurnal resting sites and move within small areas during the night C_LIO_LIThe robust nocturnal electric arousal of residents is linked to water temperature peak C_LI

animal behavior and cognition↗

bioRxiv2024

Weakly nonlinear responses at low intrinsic noise levels in two types of electrosensory primary afferents

Spiking thresholds in neurons or rectification at synapses are essential for neuronal computations rendering neuronal processing inherently nonlinear. Nevertheless, linear response theory has been instrumental for understanding, for example, the impact of noise or neuronal synchrony on signal transmission, or the emergence of oscillatory activity, but is valid only at low stimulus amplitudes or large levels of intrinsic noise. At higher signal-to-noise ratios, however, nonlinear response components become relevant. Theoretical results for leaky integrate-and-fire neurons in the weakly nonlinear regime suggest strong responses at the sum of two input frequencies if one of these frequencies or their sum match the neurons baseline firing rate. We here analyze nonlinear responses in two types of primary electroreceptor afferents, the P-units of the active and the ampullary cells of the passive electrosensory system of the wave-type electric fish Apteronotus leptorhynchus of either sex. In our combined experimental and modeling approach we identify these predicted nonlinear responses in those 31 out of 172 P-units that are characterized by low intrinsic noise. In contrast, the majority (22 out of 30) ampullary cells show nonlinear responses. Our results provide experimental evidence for nonlinear responses of spike generators in the weakly nonlinear regime. We conclude that such nonlinear responses occur in any sensory neuron that operates in similar regimes particularly at near-threshold stimulus conditions. Significance statementThe generation of action potentials involves a strong threshold nonlinearity. Nevertheless, the encoding of stimuli with small amplitudes by neurons with sufficient intrinsic noise can be well described as a linear system. As the stimulus amplitude is increased, new spectral components start to appear in the so called weakly nonlinear regime. Theory predicts nonlinear interactions whenever one or the sum of two stimulus frequencies matches the neurons baseline firing rate. Indeed, we find these interactions in a large set of electrophysiological recordings from primary electroreceptive afferents of a weakly electric fish. The non-linear response components could boost sensory responses to weak signals emitted, for example, by distant conspecifics.

neuroscience↗

bioRxiv2024

Bursts boost nonlinear encoding in electroreceptor afferents

Nonlinear mechanisms are at the heart of neuronal information processing, for example to fire an action potential, the membrane voltage must exceed a threshold nonlinearity. Even though, linear encoding schemes are commonly used and often successfully describe large parts of sensory encoding nonlinear mechanisms such as thresholds and saturations are well known to be crucial to encode behaviorally relevant features in the stimulus space not captured by linear methods. Here we analyze the role of bursts in p-type electroreceptor afferents (P-units) in the weakly electric fish Apteronotus leptorhynchus. It is long known that subpopulations of these cells fire bursts of action potentials while others do not. Previous research suggests, that the non-bursting cells are better at encoding the stimulus time-course while bursting neurons are better suited to encode special features in the stimulus. We here show, based on the analysis of experimental data and modeling, that bursts affect the linear as well as the nonlinear encoding. Theoretical work predicts that in simple leaky-integrate-and-fire model neurons, two periodic stimuli interact nonlinearly when the sum of the two frequencies matches the neurons baseline firing rate as quantified by the second-order susceptibility. Indeed, such nonlinear responses have been found in non-bursting P-units when stimulated by two beats simultaneously but only in those cells, that exhibit very low levels of intrinsic noise. In this study, we found that bursts strongly enhance these nonlinear responses which may play a critical role in the detection of weak intruder signals in the presence of a strong female signal, i.e. an electrosensory cocktail party.

neuroscience↗

bioRxiv2023

Loss or Gain of Function? Neuronal Firing Effects of Ion Channel Mutations Depend on Cell Type

Clinically relevant mutations to voltage-gated ion channels, called channelopathies, alter ion channel function, properties of ionic current and neuronal firing. The effects of ion channel mutations are routinely assessed and characterized as loss of function (LOF) or gain of function (GOF) at the level of ionic currents. Emerging personalized medicine approaches based on LOF/GOF characterization have limited therapeutic success. Potential reasons are that the translation from this binary characterization to neuronal firing especially when considering different neuronal cell types is currently not well understood. Here we investigate the impact of neuronal cell type on the firing outcome of ion channel mutations with simulations of a diverse collection of neuron models. We systematically analyzed the effects of changes in ion current properties on firing in different neuronal types. Additionally, we simulated the effects of mutations in the KCNA1 gene encoding the KV1.1 potassium channel subtype associated with episodic ataxia type 1 (EA1). These simulations revealed that the outcome of a given change in ion channel properties on neuronal excitability is cell-type dependent. As a result, cell-type specific effects are vital to a full understanding of the effects of channelopathies on neuronal excitability and present an opportunity to further the efficacy and precision of personalized medicine approaches. Significance StatementAlthough the genetic nature of ion channel mutations as well as their effects on the biophysical properties of an ion channel are routinely assessed experimentally, determination of their role in altering neuronal firing is more difficult. In particular, cell-type dependency of ion channel mutations on firing has been observed experimentally, and should be accounted for. In this context, computational modelling bridges this gap and demonstrates that the cell type in which a mutation occurs is an important determinant in the effects of neuronal firing. As a result, classification of ion channel mutations as loss or gain of function is useful to describe the ionic current but should not be blindly extend to classification at the level of neuronal firing.

neuroscience↗

bioRxiv2022

Beat encoding at mistuned octaves within single sensory neurons

Beats are periodic amplitude modulations resulting from the superposition of two spectrally close periodic signals, where the difference between the two signal frequencies defines the frequency of the beat. Such amplitude modulations are known to be well encoded in corresponding firing rate modulations in auditory fibers as well as in electrosensory afferents. In a field study we showed the behavioral relevance of beat-like amplitude modulations exceeding spectrally close interactions in electric fish. Thus, we here study the encoding of beat-like waveforms over a wide range of difference frequencies in the electrosensory system of Apteronotus leptorhynchus. Contrary to expectations from the previously measured beat tuning, the activity of p-type electroreceptor afferents follows a repetitive pattern with slow modulations of their firing rate reoccurring around multiples of the frequency of the carrier signal. Mathematical reasoning supported by simulations of modified integrate-and-fire models reveals that neither Hilbert transform, squaring, harmonics of the carrier, half-wave rectification, nor the threshold-non-linearity of a spike generator are sufficient to extract slow beating signal envelopes around the octave of the carrier. Rather, a threshold operation smoothed out by exponentiation with a power of three is needed prior to spike generation to explain the repetitive occurrence of slow signal envelopes and electroreceptor responses. Our insights suggest the synapses of inner hair cells as candidate mechanisms underlying the perception of beats at mistuned octaves that has been described by Georg Simon Ohm, Hermann Helmholtz, and others already in the 19th century.

neuroscience↗

bioRxiv2022

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↗

bioRxiv2021

Dravet variant SCN1AA1783V impairs interneuron firing predominantly by altered channel activation

Dravet syndrome (DS) is a developmental epileptic encephalopathy mainly caused by functional NaV1.1 haploinsufficiency in interneurons (IN). Recently, a new conditional mouse model expressing the recurrent human p.A1783V missense variant has become available. Here we provide an electrophysiological characterization of this variant in tsA201 cells, revealing both altered voltage-dependence of activation and slow inactivation without reduced sodium peak current density. Simulating IN excitability in a Hodgkin-Huxley one-compartment model suggested surprisingly similar firing deficits for Scn1aA1783V and full haploinsufficiency as caused by heterozygous truncation variants. Impaired NaVA1783V channel activation was predicted to have a significantly larger impact on channel function than altered slow inactivation and is therefore proposed as the main mechanism underlying IN dysfunction. The computational model was validated in cortical organotypic slice cultures derived from conditional Scn1aA1783V mice. Pan-neuronal activation of the p.A1783V variant in vitro confirmed the predicted IN firing deficit while demonstrating normal excitability of pyramidal neurons. Taken together these data demonstrate that despite maintained physiological peak currents density LOF gating properties may match effects of full haploinsufficiency on neuronal level, thereby causing DS. HighlightsNaV1.1A1783V alters voltage-dependence of activation and slow inactivation while not affecting fast inactivation. Depolarizing and hyperpolarizing shifts of activation and slow inactivation curves result in combined channel loss of function (LOF). Simulations of NaV1.1A1783V interneuronal properties indicate reduced action potential firing rates comparable to full SCN1A haploinsufficiency, which is often found in Dravet syndrome. In silico modelling identifies impaired channel activation as the predominant mechanism of channel LOF. Panneuronal induction of Scn1a+/A1783V in a cortical slice culture model confirms restriction of loss of function and its restriction to interneurons.

neuroscience↗

bioRxiv2021

Electric fish use electrocommunication signals to fine tune relative dominance and access to resources

Animals across species compete for limited resources. While in some species competition behavior is solely based on own abilities, others assess their opponents to facilitate these interactions. Using cues and communication signals, contestants gather information about their opponent, adjust their behavior accordingly, and can thereby avoid high costs of escalating fights. We tracked electrocommunication signals, in particular "rises", and agonistic behaviors of the gymnotiform electric fish Apteronotus leptorhynchus in staged competition experiments. A larger body size relative to the opponent was the sole significant predictor for winners. Sex and the frequency of the continuously emitted electric field were only mildly influencing competition outcome. In males, correlations of body-size and winning were stronger than in females and, especially when losing against females, communication and agonistic interactions were enhanced, hinting towards males being more motivated to compete. Fish that lost competitions emitted the majority of rises in dependence on the competitors relative size and sex. The emission of rises was costly since it provoked ritualized biting or chasing behaviors by the other fish. Despite winners being accurately predictable based on rise numbers already after the initial 25 minutes, losers continued to emit rises. The number of rises emitted by losers and the duration of chasing behaviors depended in similar ways on physical attributes of contestants. The detailed evaluation of these correlations hint towards A. leptorhynchus adjusting their competition behavior according to mutual assessment, where rises could signal a losers motivation to continue assessment through ritualized fighting.

animal behavior and cognition↗

bioRxiv2019

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↗

bioRxiv2017

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↗

bioRxiv2017

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↗