Modeling the sequential pattern variability of the electromotor command system of pulse electric fish

This study was supported by AEI/FEDER grants TIN2017-84452-R, PID2020-114867RB-I00, and PGC2018-095895-B-I0

Peripheral and Central Mechanisms of Temporal Pattern Recognition

Encoding information into the timing patterns of action potentials, or spikes, is a strategy used broadly in neural circuits. This type of coding scheme requires downstream neurons to be sensitive to the temporal patterns of presynaptic inputs. Indeed, neurons with temporal filtering properties have been found in a wide range of sensory pathways. However, how such response properties arise was previously not well understood. The goal of my dissertation research has been to elucidate how temporal filtering by single neurons contributes to the behavioral ability to recognize timing patterns in communication signals. I have addressed this question using mormyrid weakly electric fish, which vary the time intervals between successive electric pulses to communicate. Fish detect these signals with sensory receptors in their skin. In the majority of species, these receptors fire a single spike in response to each electric pulse. Spiking receptors faithfully encode the interpulse intervals in communication signals into interspike intervals, which are then decoded by interval-selective midbrain neurons. Using in vivo intracellular recordings from awake fish during sensory stimulation, I found that short-term depression and temporal summation play important roles in establishing single-neuron interval selectivity. Moreover, the combination of short-term depression and temporal summation in the circuit resulted in greater diversity of interval tuning properties across the population of neurons, which would increase the population’s ability to detect temporally patterned communication signals. Indeed, I found that the responses of single interval-selective neurons were sensitive to subtle variation in the timing patterns of a specific communication display produced by different individuals. A subset of mormyrid species has sensory receptors that produce spontaneously oscillating potentials. How the electrosensory system of these species established sensitivity to temporally patterned communication signals was completely unknown. Using in vivo extracellular recordings, I demonstrated that these receptors encode sensory stimuli into phase resets, which is the first clear instance of information coding by oscillatory phase reset. Furthermore, the ongoing oscillations conferred enhanced sensitivity to fast temporal patterns that are only found in the communication signals of a large group of fish. Behavioral playback experiments provided further support for the hypothesis that oscillating receptors are specialized for detecting communication signals produced by a group of conspecifics, which is a novel role for a sensory receptor. These findings demonstrate that temporal pattern sensitivity, which was previously thought to be a central processing problem, can also arise from peripheral filtering through a novel oscillatory phase reset mechanism

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

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

Social interactions in natural populations of weakly electric fish

Animals and their sensory systems evolved in specific environments and in the context of their particular ethological niches. It is often found that sensory neurons are tuned to the statistics of the natural scenes that they likely to experience. Accordingly, the importance of knowledge of natural stimuli and the problems faced and solved by sensory systems in their natural environments for the understanding of neural processing is increasingly recognized. Weakly electric fish are successful model organisms for studying the neural mechanisms underlying sensory processing in vertebrates. These mostly nocturnal animals evolved an active electric sense employed in navigation, foraging and communication. Nocturnal conditions, murky water, and the tropical environment make their natural habitats challenging study sites. Therefore, most data on their natural behavior and their communication signals have been acquired under restricted lab conditions or remain anecdotal. However, their permanently active electric organ discharges provide an excellent opportunity to monitor the movements and communication of individual unrestrained fish. The central goal of the present thesis has been to establish and to apply a method for the non-invasive quantification of electrocommunication stimuli while animals roam and interact in their natural environment. In Chapter 2, we present an automated tracking system allowing for the reliable and continuous tracking of wave-type electric fish based on the individual-specific frequency of the electric organ discharge. The system extracts frequency modulations of the EOD on short and long time scales, and estimates location and orientation of the tracked fish. We acquired data on natural communication of the ghost knifefish, Apteronotus rostratus, during its reproductive period, by deploying our tracking system in the Panamanian rain forest (Chapter 3). We tracked individuals and characterized dyadic interactions and the corresponding electro-communication scenes. We showed that a specific communication signal, independent of context, was almost exclusively emitted in close proximity to a conspecific. During courtship, the communication of males was precisely locked to that of females. Our data also showed that competing male intruders can be detected and responded to over larger distances of up to 170 cm, even in the presence of a much stronger EOD of a nearby female conspecific. For the observed interactions we extracted frequency differences and estimated effective signal intensities, and related those to the response properties of the P-unit electro-receptors. Surprisingly, we found that in many relevant communication situations the electro-receptors will be driven only weakly by electric communication signals, either because of a frequency mismatch in courtship or because of large interaction distances in agonistic contexts. This study is the first account for the detailed monitoring and characterization of electric fish movement and communication in their natural habitat. To determine the behavioral context of the male-female interaction observed in Panamá, we conducted a long-term breeding experiment in the laboratory with the closely related species A. leptorhynchus (Chapter 4). We used our tracking software to identify male-female communication scenes similar to those observed in the field and demonstrated its relationship to courtship and spawning. Sequence and dynamics of the chirping during courtship closely matched that observed in the field. We found that both the female long chirp signaling spawning and the quick and precisely timed male echo response to female chirps are conserved across species. Applying our tracking system we revealed the properties of natural communication situations. We then demonstrated how our system can be used to further characterize the behaviors observed in the field in a tailor-made long-term laboratory study

Dynamics of sensorimotor behavior in electrolocation and electrocommunication

Pedraja F. Dynamics of sensorimotor behavior in electrolocation and electrocommunication. Bielefeld: Universität Bielefeld; 2019.How are external sensory stimuli perceived, integrated and represented within the central nervous system? How does the nervous system generate appropriate behavioral responses based on this input and how does this behavior affect perception? The above questions have in common that they view sensory input and motor control as two sides of the sensorimotor loop. In this closed-loop system, actions inevitably generate sensory flow that can serve to organize behavior. To look, to smell, to touch, etc. are perceptual acts that depend on the interaction, coordination and interpretation of motor and sensory information through neural mechanisms. Active sensory systems are particularly amenable to the study of the reciprocal relations of motor and sensory components, as parts of closed loop control structures. A notable advantage of these sensory systems is the experimental accessibility of their sensory input, both in terms of its measurement and in terms of detailed modeling reconstructions of the input. In the case of weakly electric fish studied in this thesis, the animals sense and process environmental perturbations of a self-generated electric field. The fact that this field serves as the carrier of sensory information and at the same time is controlled by the animal, enables to precisely determine aspects of sensing that are often hard to obtain or quantify in sensory systems that do not actively generate the carrier: where, when and what an animal samples. Drawing on these benefits, my thesis focuses on the role of motor and electromotor behavior in sensorimotor integration. For this, a biophysical model for the active and passive electroreception was combined with physiological recordings and behavioral approaches. The central topics addressed are: (i) Object detection and sensorimotor learning. The sensory information obtained by the African species Gnathonemus petersii while learning a detection task was computationally reconstructed using boundary element methods (BEM). This revealed that the improved task performance was paralleled by an enhancement of the quality of the sensory information, which was mediated by changes of the electromotor patterns. The versatile manner in which the fish changed the spatial and temporal allocation of otherwise stable motor components not only improved the quality of the sensory input, but also resulted in shifts of the animals' attention towards the object. (ii) Dynamic choice of optimal behavior. Extending on the above results, I next explored how changing the distance of an object to be detected by the fish influenced the electromotor behavior. With increasing complexity (distance), the fish resorted to a new motor strategy. This consisted in first approaching a salient element in the arena, from where the fish then made a perceptually-guided decision. This interpretation is backed up by analyzing the trajectories in the context of attractors, revealing that the focus of attention was altered in a task-dependent manner. (iii) Distance estimation using a non-visual form of motion parallax. In the above experiments it is implicitly assumed that electric fish acquire spatial information like the position and distance of a target. How this is achieved dynamically has been addressed recently. Based on the properties of the electric field geometry, theoretical considerations indicated that relative movements might provide depth information. In a behavioral assay, I show that this novel form of electric parallax exists and is used across phylogenetically distant taxa of weakly electric fish (Apteronotus albifrons, Eigenmania virescens and Gnathonemus petersii). Notably, these species electrically sample the environment in temporally distinct ways (using discrete pulses or quasi-sinusoidal waves), suggesting an ubiquitous role for parallax in electric sensing. (iv) The role of multi-modal integration in socially relevant agonistic behaviour. Extending on the above results, I next addressed if passive as well as active electric sensory information can be used to evaluate more complex features of the environment. For this I turned to social interactions of the South American species Gymnotus omarorum to study if an electrical assessment of a competitor is possible. Based on modeling the sensory consequences of dyadic encounters, I showed that passive as well as active sensory information can drive agonistic interactions. This suggests that aggressive interactions may be triggered by information about contenders obtained through the active and passive electrosensory system. (v) Hierarchy as a social consequence of electric interactions. The above analysis indicated that active as well as passive electrolocation may contribute in a non-reciprocal manner to social interactions. Gymnotus omarorum then was tested in intra- and intersexual dyads in small plain arenas. A sex-independent dominant-subordinate status emerged after highly aggressive contests. Subordinates signaled their submission by retreating and emitting specific (submissive) electric signals. The emergence of a dominant-subordinate status was also observed in a larger arena after longer but milder contests with rare electric signaling of submission with a unique consequence: the persistence of dominance over time with no outcome reversion

Amazon Nights II: Electric Boogaloo-Neural Adaptations for Communication in Three Species of Weakly Electric FIsh

Sensory systems have to extract useful information from environments awash in noise and confounding input. Studying how salient signals are encoded and filtered from these natural backgrounds is a key problem in neuroscience. Communication is a particularly tractable tool for studying this problem, as it is a ubiquitous task that all organisms must accomplish, easily compared across species, and is of significant ethological relevance. In this chapter I describe the current knowledge of what is both known and still unknown about how sensory systems are adapted for the challenges of encoding conspecific signals, particularly in environments complicated by conspecific-generated noise. The second half of this chapter describes why weakly electric fish are particularly suited to investigating how communication can shape the nervous system to accomplish this task

26th Annual Computational Neuroscience Meeting (CNS*2017): Part 3 - Meeting Abstracts - Antwerp, Belgium. 15–20 July 2017

This work was produced as part of the activities of FAPESP Research,\ud Disseminations and Innovation Center for Neuromathematics (grant\ud 2013/07699-0, S. Paulo Research Foundation). NLK is supported by a\ud FAPESP postdoctoral fellowship (grant 2016/03855-5). ACR is partially\ud supported by a CNPq fellowship (grant 306251/2014-0)