Spatial Acuity and Prey Detection in Weakly Electric Fish

It is well-known that weakly electric fish can exhibit extreme temporal acuity at the behavioral level, discriminating time intervals in the submicrosecond range. However, relatively little is known about the spatial acuity of the electrosense. Here we use a recently developed model of the electric field generated by Apteronotus leptorhynchus to study spatial acuity and small signal extraction. We show that the quality of sensory information available on the lateral body surface is highest for objects close to the fish's midbody, suggesting that spatial acuity should be highest at this location. Overall, however, this information is relatively blurry and the electrosense exhibits relatively poor acuity. Despite this apparent limitation, weakly electric fish are able to extract the minute signals generated by small prey, even in the presence of large background signals. In fact, we show that the fish's poor spatial acuity may actually enhance prey detection under some conditions. This occurs because the electric image produced by a spatially dense background is relatively “blurred” or spatially uniform. Hence, the small spatially localized prey signal “pops out” when fish motion is simulated. This shows explicitly how the back-and-forth swimming, characteristic of these fish, can be used to generate motion cues that, as in other animals, assist in the extraction of sensory information when signal-to-noise ratios are low. Our study also reveals the importance of the structure of complex electrosensory backgrounds. Whereas large-object spacing is favorable for discriminating the individual elements of a scene, small spacing can increase the fish's ability to resolve a single target object against this background

Omnidirectional Sensory and Motor Volumes in Electric Fish

Active sensing organisms, such as bats, dolphins, and weakly electric fish, generate a 3-D space for active sensation by emitting self-generated energy into the environment. For a weakly electric fish, we demonstrate that the electrosensory space for prey detection has an unusual, omnidirectional shape. We compare this sensory volume with the animal's motor volume—the volume swept out by the body over selected time intervals and over the time it takes to come to a stop from typical hunting velocities. We find that the motor volume has a similar omnidirectional shape, which can be attributed to the fish's backward-swimming capabilities and body dynamics. We assessed the electrosensory space for prey detection by analyzing simulated changes in spiking activity of primary electrosensory afferents during empirically measured and synthetic prey capture trials. The animal's motor volume was reconstructed from video recordings of body motion during prey capture behavior. Our results suggest that in weakly electric fish, there is a close connection between the shape of the sensory and motor volumes. We consider three general spatial relationships between 3-D sensory and motor volumes in active and passive-sensing animals, and we examine hypotheses about these relationships in the context of the volumes we quantify for weakly electric fish. We propose that the ratio of the sensory volume to the motor volume provides insight into behavioral control strategies across all animals

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

Sense and Sensitivity: Spatial Structure of conspecific signals during social interaction

Organisms rely on sensory systems to gather information about their environment. Localizing the source of a signal is key in guiding the behavior of the animal successfully. Localization mechanisms must cope with the challenges of representing the spatial information of weak, noisy signals. In this dissertation, I investigate the spatial dynamics of natural stimuli and explore how the electrosensory system of weakly electric fish encodes these realistic spatial signals. To do so In Chapter 2, I develop a model that examines the strength of the signal as it reaches the sensory array and simulates the responses of the receptors. The results demonstrate that beyond distances of 20 cm, the signal strength is only a fraction of the self-generated signal, often measuring less than a few percent. Chapter 2 also focuses on modeling a heterogeneous population of receptors to gain insights into the encoding of the spatial signal perceived by the fish. The findings reveal a significant decrease in signal detection beyond 40 cm, with a corresponding decrease in localization accuracy at 30 cm. Additionally, I investigate the impact of receptor density differences between the front and back on both signal detection and resolution accuracy. In Chapter 3, I analyze distinct movement patterns observed during agonistic encounters and their correlation with the estimated range of receptor sensitivity. Furthermore, I uncover that these agonistic interactions follow a classical pattern of cumulative assessment of competitors\u27 abilities. The outcome of this research is a comprehensive understanding of the spatial dynamics of social interactions and how this information is captured by the sensory system. Moreover, the research contributed to the development of a range of tools and models that will play crucial roles in future investigations of sensory processing within this system

Fish Geometry and Electric Organ Discharge Determine Functional Organization of the Electrosensory Epithelium

Active electroreception in Gymnotus omarorum is a sensory modality that perceives the changes that nearby objects cause in a self generated electric field. The field is emitted as repetitive stereotyped pulses that stimulate skin electroreceptors. Differently from mormyriformes electric fish, gymnotiformes have an electric organ distributed along a large portion of the body, which fires sequentially. As a consequence shape and amplitude of both, the electric field generated and the image of objects, change during the electric pulse. To study how G. omarorum constructs a perceptual representation, we developed a computational model that allows the determination of the self-generated field and the electric image. We verify and use the model as a tool to explore image formation in diverse experimental circumstances. We show how the electric images of objects change in shape as a function of time and position, relative to the fish's body. We propose a theoretical framework about the organization of the different perceptive tasks made by electroreception: 1) At the head region, where the electrosensory mosaic presents an electric fovea, the field polarizing nearby objects is coherent and collimated. This favors the high resolution sampling of images of small objects and perception of electric color. Besides, the high sensitivity of the fovea allows the detection and tracking of large faraway objects in rostral regions. 2) In the trunk and tail region a multiplicity of sources illuminate different regions of the object, allowing the characterization of the shape and position of a large object. In this region, electroreceptors are of a unique type and capacitive detection should be based in the pattern of the afferents response. 3) Far from the fish, active electroreception is not possible but the collimated field is suitable to be used for electrocommunication and detection of large objects at the sides and caudally

On the Role of Sensory Cancellation and Corollary Discharge in Neural Coding and Behavior

Studies of cerebellum-like circuits in fish have demonstrated that synaptic plasticity shapes the motor corollary discharge responses of granule cells into highly-specific predictions of self- generated sensory input. However, the functional significance of such predictions, known as negative images, has not been directly tested. Here we provide evidence for improvements in neural coding and behavioral detection of prey-like stimuli due to negative images. In addition, we find that manipulating synaptic plasticity leads to specific changes in circuit output that disrupt neural coding and detection of prey-like stimuli. These results link synaptic plasticity, neural coding, and behavior and also provide a circuit-level account of how combining external sensory input with internally-generated predictions enhances sensory processing. In addition, the mammalian dorsal cochlear nucleus (DCN) integrates auditory nerve input with a diverse array of sensory and motor signals processed within circuity similar to the cerebellum. Yet how the DCN contributes to early auditory processing has been a longstanding puzzle. Using electrophysiological recordings in mice during licking behavior we show that DCN neurons are largely unaffected by self-generated sounds while remaining sensitive to external acoustic stimuli. Recordings in deafened mice, together with neural activity manipulations, indicate that self-generated sounds are cancelled by non-auditory signals conveyed by mossy fibers. In addition, DCN neurons exhibit gradual reductions in their responses to acoustic stimuli that are temporally correlated with licking. Together, these findings suggest that DCN may act as an adaptive filter for cancelling self-generated sounds. Adaptive filtering has been established previously for cerebellum-like sensory structures in fish suggesting a conserved function for such structures across vertebrates

Spatial processing of conspecific signals in weakly electric fish: from sensory image to neural population coding

In this dissertation, I examine how an animal’s nervous system encodes spatially realistic conspecific signals in their environment and how the encoding mechanisms support behavioral sensitivity. I begin by modeling changes in the electrosensory signals exchanged by weakly electric fish in a social context. During this behavior, I estimate how the spatial structure of conspecific stimuli influences sensory responses at the electroreceptive periphery. I then quantify how space is represented in the hindbrain, specifically in the primary sensory area called the electrosensory lateral line lobe. I show that behavioral sensitivity is influenced by the heterogeneous properties of the pyramidal cell population. I further demonstrate that this heterogeneity serves to start segregating spatial and temporal information early in the sensory pathway. Lastly, I characterize the accuracy of spatial coding in this network and predict the role of network elements, such as correlated noise and feedback, in shaping the spatial information. My research provides a comprehensive understanding of spatial coding in the first stages of sensory processing in this system and allows us to better understand how network dynamics shape coding accuracy

The development of seahorse vision: morphological and behavioural aspects

Seahorses are visually guided feeders that rely on a well-developed visual system to successfully predate on small shrimp and plankton. Despite their dependence on vision for feeding and survival, very little is known about seahorse vision and visual development. Many species of seahorse have a specialisation in their retina associated with acute vision, a convexiclivate, rod-free fovea located at the centre of gaze. In the first part of this thesis, the foveae of temperate Hippocampus abdominalis and tropical H. taeniopterus seahorses are characterised. Both species possess a rod-free convexiclivate fovea and the pattern of photoreceptor and ganglion cell distribution is similar. Despite these similarities, H. taeniopterus has higher cell densities on the foveal slope and better theoretical and behaviourally measured visual resolution compared to H. abdominalis. These data indicate that seahorses have a well-developed acute visual system, and this tropical seahorse species has higher visual resolution compared to this species of temperate seahorse. In the second part of the thesis, developmental changes in foveal morphology are analysed using three increasingly larger sized groups of H. taeniopterus seahorses. Morphologically, the depression of the foveal pit deepens as the fish grows. The area of rod-free zone also increases with fish size. The photoreceptor and ganglion cell densities increase at the foveal slope, although there is a decrease in cone and ganglion cell density at the foveal centre this is observed as the fish grows. Both the theoretical and the behavioural visual resolution improve with increasing fish size, with larger fish being able to detect the same sized prey at a greater distance. The behaviourally measured increased visual function correlates with changes in morphology with fish size. The last aspect of the thesis uses five H. taeniopterus seahorse groups of increasing size to analyse the morphological and behavioural development of the fovea and rod-free zone, with an emphasis on the contribution of cell death and proliferation. The behavioural visual resolution improves with size. Morphologically, the area of rod-free zone increases in size during development. BrdU labelling, a measure of cell proliferation, shows the absence of cell division in the ONL; however, there are dividing neuroretinal cells in the INL within the rod-free zone. The TUNEL assay confirms the lack of programmed large-scale photoreceptor cell death in and around the rod-free zone during development. Taken together, our data are not able to rule out the possibility of cone photoreceptor cell generation from INL stem cells within the rod-free zone, although cell death is not likely to be a major mechanism of foveal development. Future studies are designed to determine the underlying mechanism in the establishment of the adult rod-free zone

Fish behavior and its use in the capture and culture of fishes

Fishery management, Behaviour, Food fish, Fish culture, Conferences