Animal-Robot Interactions: Electrocommunication, Sensory Ecology, and Group Dynamics in a Mormyrid Weakly Electric Fish

Mormyrid weakly electric fish possess a specialized electrosensory system. During the process of active electrolocation, these animals perceive self-generated electric organ dis-charges (EOD) and are thereby able to detect objects in their nearby environment. The EOD is a short, biphasic pulse, which is simultaneously used to communicate with conspe-cifics. There are two principles according to which information exchange occurs during electrocommunication. The waveform of the EOD constitutes a relatively stable identity marker that signals species, gender, and status of an individual. In contrast, the temporal sequence of inter-discharge intervals (IDI) is highly variable and encodes context-specific information. Modifications of IDI-duration not only alter the instantaneous discharge fre-quency but also enable the generation of specific signaling patterns and interactive dis-charge sequences. One such interactive discharge behavior is the so-called echo response, during which a fish responds with a constant latency of only a few milliseconds to the EOD of a conspecific. Animals can synchronize their signaling sequences by mutually generating echoes to each other's signals over a coherent period. Although active electrolocation and electrocommunication are mediated by different types of electroreceptor organs and neural pathways, an unambiguous assignment of electromotor behavior to only one of the two functions is often problematic. In this thesis, the significance of IDI-based signaling sequences during motor and electro-motor interactions of the mormyrid fish Mormyrus rume proboscirostris were investigated. To this end, different electrical playback sequences of species-specific EODs were generated via mobile fish dummies, and the motor and electromotor responses of live fish were analyzed. In Part One of this thesis, electrocommunication strategies of the fish were analyzed, and particularly the functions of double pulses, discharge regularizations, and echo responses were examined in an adaptive context. Double pulses were classified as an aggressive mo-tivation signal, whereas regularizations may have a communicative function during the early stages of the sequential assessment of a potential opponent. In this context, discharge synchronization by means of echo responses may enable a mutual assessment for the net benefit of both contestants. Because echo responses occur in various behavioral contexts, and artificial echoes of the dummy evoked increased echoing by the fish, it was hypothesized that the echo response serves a more general purpose by enabling mutual allocation of social attention between two fish. In Part Two of this thesis, a biomimetic robotic fish was designed to investigate the senso-ry basis on which fish followed the dummy. It was shown that electrical playback signals induced following-behavior in live fish, whereas biomimetic motility patterns had no ef-fect. By subsequently reducing the mobile dummy to only the electric signaling sequence from the perspective of the fish, it could be shown that passive perception of electrical communication signals is also involved in mediating the spatial coordination of social in-teractions. This passive perception is likely mediated by the same electroreceptor organs that are used during electrocommunication. The EOD can therefore be considered to be an essential social stimulus that makes it possible to integrate a dummy into a group of weak-ly electric fish as an artificial conspecific. The influence of an interactively signaling mobile dummy fish on small groups of up to four individuals was investigated in Part Three of this thesis. Typical schooling behavior was a rare occurrence in this context. However, EOD-synchronizations through mutual echo responses between two fish, or between a fish and the interactive dummy, were fre-quently observed during social interactions in small groups. Motor interactions during synchronization episodes supported the hypothesis that mormyrids may use discharge synchronizations between individuals to allocate social attention, and the echo response may thus adopt a particularly useful function during communication in groups.Schwach elektrische Fisch aus der Familie der Mormyriden verfügen über ein spezialisier-tes elektrosensorisches Sinnessystem. In einem Prozess, der als aktive Elektroortung be-zeichnet wird, sind diese Tiere in der Lage, selbstgenerierte elektrische Organentladungen (EOD) wahrzunehmen, und dadurch Objekte in ihrer unmittelbaren Nähe zu detektieren. Das EOD ist ein kurzer bipolarer Puls, der gleichzeitig auch zur Kommunikation mit Artge-nossen dient. Informationsaustausch während der Elektrokommunikation basiert auf zwei verschiedenen Prinzipien: Die Wellenform des EOD stellt einen relativ konstanten Identi-tätsmarker dar, der beispielsweise Art, Geschlecht und Status eines Individuums signali-siert. Die zeitliche Abfolge der Intervalle zwischen den EODs ist hingegen höchst variabel und kodiert kontextspezifische Information. Durch Modifikation der Intervalldauer ändert sich nicht nur die Entladungsfrequenz, sondern es können auch spezifische Signalmuster und interaktive Entladungssequenzen generiert werden. Ein interaktives Entladungsver-halten stellt beispielsweise die Echoantwort dar, bei der ein Fisch mit einer konstanten Latenz von wenigen Millisekunden auf das EOD eines Artgenossen reagiert. Zwei Tiere können ihre Entladungssequenzen synchronisieren, indem sie ihre Signale über einen kohärenten Zeitraum gegenseitig mit Echos beantworten. Obwohl aktive Elektroortung und Elektrokommunikation über unterschiedliche Rezeptororgansysteme und neuronale Pfade vermittelt werden, ist eine eindeutige Zuordnung der elektromotorischen Verhal-tensäußerungen der Fische zu nur einer der beiden Funktionen oft problematisch. In der vorliegenden Arbeit wurde die Bedeutung intervallbasierter EOD-Sequenzen für motorische und elektromotorische Interaktionen des Mormyriden Mormyrus rume proboscirostris erforscht. Hierzu wurden verschiedene elektrische Playbacksequenzen artspezifischer EODs generiert und durch mobile Fischattrappen wiedergegeben. Die mo-torischen und elektromotorischen Verhaltensreaktionen der Fische wurden analysiert. Im ersten Teil der Arbeit wurden Elektrokommunikationsstrategien der Fische analysiert und die adaptive Funktion insbesondere von Doppelpulsen, Entladungsregularisierungen und Echoantworten untersucht. Doppelpulse wurden als aggressives Motivationssignal kategorisiert, wohingegen die Kommunikationsfunktion von Regularisierungen im gegen-seitigen Einschätzen zu Beginn einer kompetitiven Begegnung zu liegen scheint. Entla-dungssynchronisation durch gegenseitige Echoantworten kann dabei eine Einschätzung des Gegenübers zum Vorteil beider Parteien erleichtern. Da Echoantworten in verschiede-nen Verhaltenssituationen auftreten und artifizielle Echoantworten der Attrappe vermehrt zu Echos vonseiten der Fische führten, wurde postuliert, dass die Echoantwort eine generellere Funktion bei der Fokussierung gegenseitiger sozialer Aufmerksamkeit über-nehmen kann. Im zweiten Teil der Arbeit wurde ein biomimetischer Fischroboter konstruiert, um zu untersuchen, auf welcher sensorischen Grundlage die Fische der Attrappe folgen. Es konnte gezeigt werden, dass elektrische Playbacksignale, nicht aber biomimetische Bewe-gungsmuster, Folgeverhalten der Fische induzieren. In einem weiteren Schritt konnte durch die Reduktion der Attrappe auf die elektrischen Signalsequenzen aus der Perspektive der Versuchsfische gezeigt werden, dass passive Wahrnehmung elektrischer Kommu-nikationssignale auch bei der räumlichen Koordination sozialer Interaktionen von Bedeu-tung ist. Dies wird mutmaßlich über die gleichen Rezeptororgane vermittelt, die auch für die Elektrokommunikation verantwortlich sind. Das EOD kann daher als ein soziales Signal betrachtet werden, das es ermöglicht, eine Attrappe als künstlichen Artgenossen in eine Gruppe schwach elektrischer Fische zu integrieren. Der Einfluss einer elektrisch interaktiven mobilen Fischattrappe auf kleine Gruppen von bis zu vier Individuen wurde im dritten Teil der Arbeit getestet. Typisches Schwarmver-halten konnte in diesem Zusammenhang nur selten beobachtet werden. In kleinen Gruppen kam es während sozialer Interaktionen jedoch häufig zu EOD-Synchronisationen durch Echoantworten zwischen zwei Fischen, oder zwischen einem Fisch und der interaktiven Attrappe. Motorische Verhaltensinteraktionen im Zeitraum dieser Synchronisationen stützen die Hypothese, dass Mormyriden durch elektrische Entladungssynchronisation soziale Aufmerksamkeit zwischen Individuen herstellen können, und die Echoantwort somit besonders in Gruppen eine nützliche Kommunikationsfunktion übernehmen kann

Object Localization in Fluids based on a Bioinspired Electroreceptor System

Wolf-Homeyer S. Object Localization in Fluids based on a Bioinspired Electroreceptor System. Bielefeld: Universität Bielefeld; 2019.Weakly electric fish use self-generated electric fields for communication, active electrolocation and navigation. Additionally to visual sense, this ability enables them to detect objects and food even in dark or turbid waters. Specialized muscle cells in the tail region actively generate an electric field in the surrounding fluid, shaped like a dipole between tail and head. This dipole field may be distorted depending on environmental parameters such as the presence of objects of different geometry or material properties in the animal's vicinity. Electroreceptors, distributed all over the fish' skin allow to perceive distortions of the field, caused by objects. Furthermore, fish execute stereotyped scanning behaviors to obtain additional sensory information of detected objects. The development of innovative sensor systems for short-range exploration in fluids is still in its infancy. Also, the use of electric fields in bio-inspired technologies is still at an early stage. Based on the biological model of weakly electric fish, the question has already been examined if an array of electrodes can be used for a contactless object detection and localization and finally for navigation in fluids (Solberg et al. 2008). This examination is performed by analyses of electric field modulations, based on so-called EEVs. An EEV (Ensemble of Electrosensory Viewpoints) is a scalar field representation of the influence of an object on the electric field in the form of potential differences measured between two electrodes for every possible object location. The first part of this thesis explores the characteristics of the electric dipole field and the resulting EEV by means of numerical simulations to determine the influence of an object placed in the emitted field. It will also be investigated how many receptors are required and which arrangement is to be preferred to uniquely identify the positions of spherical objects in the vicinity of the sensor system. For this, a receptor system composed of a simple biomimetic abstraction of an emitter dipole and an orthogonally arranged pair of sensor electrodes is used. Inspired by the scanning movements of the fish, a fixed, minimal scanning strategy, composed of active receptor system movements is developed. The active electrolocation strategy introduced here is based on the superposition of extracted EEV contour-rings in order to find intersections of these contours. The second part of this work focuses on the development of an *application* for active electrolocation which is based on a minimal set of scanning movements as a precursor for the partitioning of the later search area in which sensor-emitter movements take place. In this application, EEVs are also used as major components of two localization algorithms. In order to find points within the search space which are part of several contour-rings, intersection points have to found. Due to numerical inaccuracies intersection points may degrade to contour-segments which lie very close to each other but do not touch. For this case, a nearness metric is used to identify such points. However, in this part of the work the EEVs are based on a simplified analytical representation, which renders the corresponding algorithms suitable for embedded computer systems. In the third part of this thesis, a fitted histogram representation of EEVs is used to compare a large number of different movement sequences to select the optimal composition from this variety. For this, the general shape of an EEV has to be considered, which plays a major role in estimating the best sequence

Mathematical models of depth perception in weakly electric fish

Weakly electric fish use electrolocation - the detection of electric fields - to sense their environment. The task of electrolocation involves the decoding of the third dimension - depth - from a two-dimensional electric image. In this work we present three advances in the area of depth-perception. First, we develop a model for electrolocation based on a single parameter, namely the width of the electric image. In contrast to previous suggested algorithms, our algorithm would only require a single narrow tuned topographic map to accurately estimate distance. This model is used to study the effects of electromagnetic noise and the presence of stochastic resonance. Second, considering the problem of depth perception from the perspective of information constraints, we ask how much information is necessary for location disambiguation? That is, what is the minimum amount of information that fish would need to localize an object? This inverse problem approach gives us insight into biological electrolocation and provides a guide for future experimental work. Our final contribution is to provide a mathematical foundation for two of the most accepted depth perception models currently in use

Study of sequential information processing in electroreception through modelling and closed-loop stimulation techniques

Tesis Doctoral inédita leída en la Universidad Autónoma de Madrid, Escuela Politécnica Superior, Departamento de Ingenieria Informática. Fecha de Lectura: 20-01-202

Engineering derivatives from biological systems for advanced aerospace applications

The present study consisted of a literature survey, a survey of researchers, and a workshop on bionics. These tasks produced an extensive annotated bibliography of bionics research (282 citations), a directory of bionics researchers, and a workshop report on specific bionics research topics applicable to space technology. These deliverables are included as Appendix A, Appendix B, and Section 5.0, respectively. To provide organization to this highly interdisciplinary field and to serve as a guide for interested researchers, we have also prepared a taxonomy or classification of the various subelements of natural engineering systems. Finally, we have synthesized the results of the various components of this study into a discussion of the most promising opportunities for accelerated research, seeking solutions which apply engineering principles from natural systems to advanced aerospace problems. A discussion of opportunities within the areas of materials, structures, sensors, information processing, robotics, autonomous systems, life support systems, and aeronautics is given. Following the conclusions are six discipline summaries that highlight the potential benefits of research in these areas for NASA's space technology programs

Models of Causal Inference in the Elasmobranch Electrosensory System: How Sharks Find Food

We develop a theory of how the functional design of the electrosensory system in sharks reflects the inevitability of noise in high-precision measurements, and how the Central Nervous System may have developed an efficient solution to the problem of inferring parameters of stimulus sources, such as their location, via Bayesian neural computation. We use Finite Element Method to examine how the electrical properties of shark tissues and the geometrical configuration of both the shark body and the electrosensory array, act to focus weak electric fields in the aquatic environment, so that the majority of the voltage drop is signalled across the electrosensory cells. We analyse snapshots of two ethologically relevant stimuli: localized prey-like dipole electric sources, and uniform electric fields resembling motion-induced and other fields encountered in the ocean. We demonstrated that self movement (or self state) not only affects the measured field, by perturbing the self field, but also affects the external field. Electrosensory cells provide input to central brain regions via primary afferent nerves. Inspection of elasmobranch electrosensory afferent spike trains and inter-spike interval distributions indicates that they typically have fairly regular spontaneous inter-spike intervals with skewed Gaussian-like variability. However, because electrosensory afferent neurons converge onto secondary neurons, we consider the convergent input a "super afferent" with the pulse train received by a target neuron approaching a Poisson process with shorter mean intervals as the number of independent convergent spike trains increases. We implement a spiking neural particle filter which takes simulated electrosensory "super afferent" spike trains and can successfully infer the fixed Poisson parameter, or the equivalent real world state, distance to a source. The circuit obtained by converting the mathematical model to a network structure bears a striking resemblance to the cerebellar-like hindbrain circuits of the dorsal octavolateral nucleus. The elasmobranchs’ ability to sense electric fields down to a limit imposed by thermodynamics seems extraordinary. However we predict that the theories presented here generalize to other sensory systems, particularly the other octavolateralis senses which share cerebellar-like circuitry, suggesting that the cerebellum itself also plays a role in dynamic state estimation

MECHANOSENSORY FEEDBACK FOR FLIGHT CONTROL AND PREY CAPTURE IN THE ECHOLOCATING BAT

Throughout the animal kingdom, organisms have evolved neural systems that process biologically relevant stimuli to guide a wide range of species-specific behaviors. Bats, comprising 25% of mammalian species, rely on diverse sensory modalities to carry out tasks such as foraging, obstacle avoidance and social communication. While it is well known that many bat species use echolocation to find food and steer around obstacles, they also depend on other senses. For instance, some bats predominantly use vision to navigate, and others use olfaction to find food sources. In addition, bats rely on airflow sensors to stabilize their flight, primarily through signals carried by microscopic hairs embedded in their wings and tail membranes. Studies have shown that bats performing an obstacle avoidance task show changes in their flight behavior when dorsal wing hairs are removed. Additionally, electrophysiological studies have shown that wing hairs are involved in airflow sensing, but little is known about the contribution of sensory hairs on the ventral surfaces of the wing and tail membranes to their flight control and other complex behaviors, such as prey handling. Chapter 1 of my dissertation presents a general introduction to bat echolocation, flight kinematics, and airflow sensing for flight control. In Chapter 2, I review sensory hairs across the animal kingdom, from invertebrates to vertebrates. I discuss the role of sensory hairs for functions ranging from detection to locomotion and propose the use and benefit of mechanosensors in biologically-inspired technology. In Chapter 3, I devised an experiment to evaluate changes in capture success, as well changes in flight kinematics and adaptive sonar behavior, before and after depilation of sensory hairs in order to ascertain if these sensory hairs have a functional role in both airflow sensing for flight control and tactile sensing for prey handling. In Chapter 4, I designed an experiment aimed at determining if firing patterns of S1 neurons change with airflow speed and angle of attack and if wing hair depilation affects S1 responses to whole wing stimulation. To answer these questions, I record neural activity in S1 of sedated big brown bats while the entire contralateral wing is systematically exposed to naturalistic airflow in a wind tunnel. Finally, in Chapter 5, I address open questions that remain, present experiments aimed at filling these gaps, and consider key points important for future work

25th annual computational neuroscience meeting: CNS-2016

The same neuron may play different functional roles in the neural circuits to which it belongs. For example, neurons in the Tritonia pedal ganglia may participate in variable phases of the swim motor rhythms [1]. While such neuronal functional variability is likely to play a major role the delivery of the functionality of neural systems, it is difficult to study it in most nervous systems. We work on the pyloric rhythm network of the crustacean stomatogastric ganglion (STG) [2]. Typically network models of the STG treat neurons of the same functional type as a single model neuron (e.g. PD neurons), assuming the same conductance parameters for these neurons and implying their synchronous firing [3, 4]. However, simultaneous recording of PD neurons shows differences between the timings of spikes of these neurons. This may indicate functional variability of these neurons. Here we modelled separately the two PD neurons of the STG in a multi-neuron model of the pyloric network. Our neuron models comply with known correlations between conductance parameters of ionic currents. Our results reproduce the experimental finding of increasing spike time distance between spikes originating from the two model PD neurons during their synchronised burst phase. The PD neuron with the larger calcium conductance generates its spikes before the other PD neuron. Larger potassium conductance values in the follower neuron imply longer delays between spikes, see Fig. 17.Neuromodulators change the conductance parameters of neurons and maintain the ratios of these parameters [5]. Our results show that such changes may shift the individual contribution of two PD neurons to the PD-phase of the pyloric rhythm altering their functionality within this rhythm. Our work paves the way towards an accessible experimental and computational framework for the analysis of the mechanisms and impact of functional variability of neurons within the neural circuits to which they belong

25th Annual Computational Neuroscience Meeting: CNS-2016

Abstracts of the 25th Annual Computational Neuroscience Meeting: CNS-2016 Seogwipo City, Jeju-do, South Korea. 2–7 July 201