Encoding and processing of sensory information in neuronal spike trains

Recently, a statistical signal-processing technique has allowed the information carried by single spike trains of sensory neurons on time-varying stimuli to be characterized quantitatively in a variety of preparations. In weakly electric fish, its application to first-order sensory neurons encoding electric field amplitude (P-receptor afferents) showed that they convey accurate information on temporal modulations in a behaviorally relevant frequency range (<80 Hz). At the next stage of the electrosensory pathway (the electrosensory lateral line lobe, ELL), the information sampled by first-order neurons is used to extract upstrokes and downstrokes in the amplitude modulation waveform. By using signal-detection techniques, we determined that these temporal features are explicitly represented by short spike bursts of second-order neurons (ELL pyramidal cells). Our results suggest that the biophysical mechanism underlying this computation is of dendritic origin. We also investigated the accuracy with which upstrokes and downstrokes are encoded across two of the three somatotopic body maps of the ELL (centromedial and lateral). Pyramidal cells of the centromedial map, in particular I-cells, encode up- and downstrokes more reliably than those of the lateral map. This result correlates well with the significance of these temporal features for a particular behavior (the jamming avoidance response) as assessed by lesion experiments of the centromedial map

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

Multisensory integration in weakly electric fish

Animals integrate information from across sensory systems, such as vision and hearing, to improve perception. To understand how neural circuits in the central nervous system integrate information from different senses, the responses of midbrain neurons to two categories of electrosensory stimuli in Eigenmannia virescens were studied. The first category of stimulus is electrical signals with frequencies below 50 Hz that are encoded in the activity of ampullary receptors. The second category is amplitude modulations of the electric organ discharge, which are encoded by p-type tuberous receptors. Six multisensory neurons were found that responded to both categories of stimuli. However, when the stimuli were presented simultaneously, the responses to one of the two categories were suppressed. Further, in six neurons that responded to one modality, responses were significantly reduced when the two categories of stimuli were presented simultaneously. These data suggest that multisensory information does not enhance neural responses

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

Insights into neural mechanisms and evolution of behaviour from electric fish.

Behaviour, although multifaceted and diverse, also seems to be convergent across taxa. Even distantly related organisms can show similar behaviours, involving sensory pattern recognition, locomotion and experiencedependent changes in sensory processing and motor output. In neuroscience, the prevalent use of particular systems as models for understanding the function of the human nervous system rests on this functional overlap and structural homology. However, we are only beginning to understand whether similarities in behaviour are paralleled by similarities in control mechanisms, neural circuitry and processing. This gap in knowledge is not surprising; the identification of the neural control of any particular behaviour or function can be a formidable challenge. As we learn more about how neural circuits control behaviour, we hope to gain a greater understanding of why particular solutions have developed 1 . Integration of information at these two levels will be essential for revealing the uniqueness of particular neural circuits 2 and mechanisms, as well as for understanding the roles of historical forces in determining the final architecture of neural circuits and processing. Electrosensory systems (BOX 1) are well suited to addressing these questions. In addition to their established utility for investigating receptor 3 and ion channel 4 function, electric fish have increasingly been used for studying the neural circuits that control behaviour 5 . Some fish are purely electroreceptive, whereas others can both sense and produce electric fields. Most species of the latter type continue to produce discharges of their electric organs (EODs, electric organ discharges) when prepared for in vivo neurophysiological recording. Furthermore, changes in these EODs produce a variety of electrosensory behaviours, permitting investigators to study the entire neural circuit for the control of these behaviours 5, Jamming avoidance responses Behaviour. Wave-type electric fish generate electric fields INSIGHTS INTO NEURAL MECHANISMS AND EVOLUTION OF BEHAVIOUR FROM ELECTRIC FISH Gary J. Rose Abstract | Both behaviour and its neural control can be studied at two levels. At the proximate level, we aim to identify the neural circuits that control behaviour and to understand how information is represented and processed in these circuits. Ultimately, however, we are faced with questions of why particular neural solutions have arisen, and what factors govern the ways in which neural circuits are modified during the evolution of new behaviours. Only by integrating these levels of analysis can we fully understand the neural control of behaviour. Recent studies of electrosensory systems show how this synthesis can benefit from the use of tractable systems and comparative studies

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

Neural mechanisms for sensory prediction in a cerebellum-like structure

Any animal must be able to predict and cancel the sensory consequences of its own movements to avoid ambiguity in the origin of sensory input. Theoretical and human behavioral studies suggest that nervous systems contain internal models that use copies of outgoing motor signals along with incoming sensory feedback to predict the consequences of movements. Many studies propose the cerebellum as one possible site of such internal models. Yet whether such an internal model exists and how such an internal model might be implemented in neural circuits is largely speculative. Early work in cerebellum-like structures of mormyrid fish identified neural mechanisms of sensory predictions at the levels of synapses, cells, and circuits, and successfully linked those mechanisms to the systems-level function--the cancellation of electrosensory input due to the fish's own behavior. However, those early studies were restricted to predicting and cancelling the electrosensory consequences of relatively simple and rather specialized electromotor behavior. The research described here takes an in vivo electrophysiological approach to generalize the previous work in mormyrid fish to the more ubiquitous problem of predicting and cancelling the sensory consequences of movements. First, I demonstrate that neurons in the electrosensory lobe of weakly electric mormyrid fish generate predictions at the cellular level, termed negative images, about the sensory consequences of the fish's own movements based on ascending spinal corollary discharge signals. Second, I examine the interactions between corollary discharge and proprioceptive feedback under conditions that simulate real movements. Using experiments and modeling, I show that plasticity acting on random, nonlinear mixtures of corollary discharge and proprioceptive signals can account for key properties of negative images observed in vivo. Mossy fibers originating in the spinal cord carry randomly mixed, though linear, corollary discharge and proprioceptive signals, while properties of granule cells observed in vivo are consistent with a nonlinear re-coding of these signals. The conclusion of these studies is that both corollary discharge and proprioception, in combination with an associative neural network endowed with synaptic plasticity, provide a powerful and flexible basis for solving the ubiquitous problems of predicting the sensory consequences of movements

Stimulus Encoding and Feature Extraction by Multiple Sensory Neurons

Neighboring cells in topographical sensory maps may transmit similar information to the next higher level of processing. How information transmission by groups of nearby neurons compares with the performance of single cells is a very important question for understanding the functioning of the nervous system. To tackle this problem, we quantified stimulus-encoding and feature extraction performance by pairs of simultaneously recorded electrosensory pyramidal cells in the hindbrain of weakly electric fish. These cells constitute the output neurons of the first central nervous stage of electrosensory processing. Using random amplitude modulations (RAMs) of a mimic of the fish’s own electric field within behaviorally relevant frequency bands, we found that pyramidal cells with overlapping receptive fields exhibit strong stimulus-induced correlations. To quantify the encoding of the RAM time course, we estimated the stimuli from simultaneously recorded spike trains and found significant improvements over single spike trains. The quality of stimulus reconstruction, however, was still inferior to the one measured for single primary sensory afferents. In an analysis of feature extraction, we found that spikes of pyramidal cell pairs coinciding within a time window of a few milliseconds performed significantly better at detecting upstrokes and downstrokes of the stimulus compared with isolated spikes and even spike bursts of single cells. Coincident spikes can thus be considered “distributed bursts.” Our results suggest that stimulus encoding by primary sensory afferents is transformed into feature extraction at the next processing stage. There, stimulus-induced coincident activity can improve the extraction of behaviorally relevant features from the stimulus

Calcium-mediated change in neuronal intrinsic excitability in weakly electric fish: biasing mechanisms of homeostatis for those of plasticity

textAlthough the processes used for temporarily storing and manipulating neural information have been extensively studied at the synaptic level far less attention has been given to the underlying cellular and molecular mechanisms that contribute to change in the intrinsic excitability of neurons. More importantly, how do these mechanisms of plasticity integrate with ongoing mechanisms of regulation of neural intrinsic excitability and, in turn, homeostasis of entire neural circuits? In this dissertation I describe the underlying mechanisms that contribute to persistent neural activity and, more globally, sensorimotor adaptation using weakly electric fish as my model system. Weakly electric fish have evolved a behavior adaptation known as the jamming avoidance response (JAR), and it is this adaptation that allows the organism to elevate its own electrical discharge in response to intraspecific interactions and subsequent distortions of the animal’s electric field. The elevation operates over a wide range and in vivo can last tens of hours upon cessation of a jamming stimulus. I demonstrate that the underlying mechanisms of the adaptation are mediated by calcium-dependent signaling in the pacemaker nucleus and that calcium-mediated phosphorylation plays an important role in the regulation of the long-term frequency elevation (LTFE). I demonstrate using an in vitro brain slice preparation from the weakly electric fish, Apteronotus leptorhynchus that the engram of memory formation depends on the cooperativity of calcium-dependent protein kinases and protein phosphatases. In addition, I show that the memory formation (in the form of LTFE) does not depend on the continued flux of calcium, but rather the phosphorylation events downstream of NMDA receptor activation. Moreover, I describe the differences in the expression of protein phosphatases and protein kinases as they relate to species-specific differences in sensorimotor adaptation. It is important to note that this is the first time that the cooperativity between different isoforms of protein kinase C (PKC) have been shown to play a role in graded long-term change in neuronal activity and, in turn, providing the neural basis of species-specific behavior. The neural adaptation of the electromotor system in weakly electric fish provides an excellent model system to study the underlying cellular and molecular events of vertebrate memory formation.Biological Sciences, School o

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