Taking a shortcut: what mechanisms do fish use?

Path integration is a powerful navigational mechanism whereby individuals continuously update their distance and angular vector of movement to calculate their position in relation to their departure location, allowing them to return along the most direct route even across unfamiliar terrain. While path integration has been investigated in several terrestrial animals, it has never been demonstrated in aquatic vertebrates, where movement occurs through volumetric space and sensory cues available for navigation are likely to differ substantially from those in terrestrial environments. By performing displacement experiments with Lamprologus ocellatus, we show evidence consistent with fish using path integration to navigate alongside other mechanisms (allothetic place cues and route recapitulation). These results indicate that the use of path integration is likely to be deeply rooted within the vertebrate phylogeny irrespective of the environment, and suggests that fish may possess a spatial encoding system that parallels that of mammals.

Motion parallax for object localization in electric fields.

Parallax, as a visual effect, is used for depth perception of objects. But is there also the effect of parallax in the context of electric field imagery? In this work, the example of weakly electric fish is used to investigate how the self-generated electric field that these fish utilize for orientation and communication alike, may be used as a template to define electric parallax. The skin of the electric fish possesses a vast amount of electroreceptors that detect the self-emitted dipole-like electric field. In this work, the weakly electric fish is abstracted as an electric dipole with a sensor line in between the two emitters. With an analytical description of the object distortion for a uniform electric field, the distortion in a dipole-like field is simplified and simulated. On the basis of this simulation, the parallax effect could be demonstrated in electric field images i.e. by closer inspection of voltage profiles on the sensor line. Therefore, electric parallax can be defined as the relative movement of a signal feature of the voltage profile (here, the maximum or peak of the voltage profile) that travels along the sensor line peak trace (PT). The PT width correlates with the object's vertical distance to the sensor line, as close objects create a large PT and distant objects a small PT, comparable with the effect of visual motion parallax.

The Use of Supervised Learning Models in Studying Agonistic Behavior and Communication in Weakly Electric Fish.

Despite considerable advances, studying electrocommunication of weakly electric fish, particularly in pulse-type species, is challenging as very short signal epochs at variable intervals from a few hertz up to more than 100 Hz need to be assigned to individuals. In this study, we show that supervised learning approaches offer a promising tool to automate or semiautomate the workflow, and thereby allowing the analysis of much longer episodes of behavior in a reasonable amount of time. We provide a detailed workflow mainly based on open resource software. We demonstrate the usefulness by applying the approach to the analysis of dyadic interactions of Gnathonemus petersii. Coupling of the proposed methods with a boundary element modeling approach, we are thereby able to model the information gained and provided during agonistic encounters. The data indicate that the passive electrosensory input, in particular, provides sufficient information to localize a contender during the pre-contest phase, fish did not use or rely on the theoretically also available sensory information of the contest outcome-determining size difference between contenders before engaging in agonistic behavior.

Linking active sensing and spatial learning in weakly electric fish.

Weakly electric fish can learn the spatial layout of their environment using only their short-range electric sense. During spatial learning, active sensing motions are used to memorize landmark locations so that they can serve as anchors for idiothetic-based navigation. A hindbrain feedback circuit selectively amplifies the electrosensory input arising from these motions. The ascending electrolocation pathway preferentially transmits this information to the pallial regions involved in spatial learning and navigation. Similarities in both behavioral patterns and hindbrain circuitry of gymnotiform and mormyrid fish, two families that independently evolved their electrosense, suggest that amplification and transmission of active sensing motion inputs are fundamental mechanisms for spatial memory acquisition.

Task-Related Sensorimotor Adjustments Increase the Sensory Range in Electrolocation.

Perception and motor control traditionally are studied separately. However, motor activity can serve as a scaffold to shape the sensory flow. This tight link between motor actions and sensing is particularly evident in active sensory systems. Here, we investigate how the weakly electric mormyrid fish Gnathonemus petersii of undetermined sex structure their sensing and motor behavior while learning a perceptual task. We find systematic adjustments of the motor behavior that correlate with an increased performance. Using a model to compute the electrosensory input, we show that these behavioral adjustments improve the sensory input. As we find low neuronal detection thresholds at the level of medullary electrosensory neurons, it seems that the behavior-driven improvements of the sensory input are highly suitable to overcome the sensory limitations, thereby increasing the sensory range. Our results show that motor control is an active component of sensory learning, demonstrating that a detailed understanding of contribution of motor actions to sensing is needed to understand even seemingly simple behaviors.SIGNIFICANCE STATEMENT Motor-guided sensation and perception are intertwined, with motor behavior serving as a scaffold to shape the sensory input. We characterized how the weakly electric mormyrid fish Gnathonemus petersii, as it learns a perceptual task, restructures its sensorimotor behavior. We find that systematic adjustments of the motor behavior correlate with increased performance and a shift of the sensory attention of the animal. Analyzing the afferent electrosensory input shows that a significant gain in information results from these sensorimotor adjustments. Our results show that motor control can be an active component of sensory learning. Researching the sensory corollaries of motor control thus can be crucial to understand sensory sensation and perception under naturalistic conditions.

Social odour activates the hippocampal formation in zebra finches (Taeniopygia guttata).

Experiments from our research group have demonstrated that the olfactory sense of birds, which has been considered as unimportant for a long time, plays a prominent role as communication channel in social behaviour. Odour cues are used e.g. by zebra finch chicks to recognize the mother, by adult birds to distinguish their own eggs from others, or to recognize kin. While there is quite a lot of evidence for the importance of odour for social behaviour, it is not known as yet which brain areas may be involved in the processing of socially relevant odours. We therefore compared the brain activation pattern of zebra finch males exposed to their own offspring odour with that induced by a neutral odour stimulus. By measuring head saccade changes as behavioural reaction and using the expression of the immediate early gene product c-Fos as brain activity marker, we show here that the activation pattern, namely the activity difference between the left and the right hemisphere, of several hippocampal areas in zebra finch males is altered by the presentation of the odour of their own nestlings. In contrast, the nucleus taeniae of the amygdala (TnA) exhibits a tendency of a reduction of c-Fos activation in both hemispheres as a consequence of exposure to the nestling odour. We conclude that the hippocampus is involved in odour based processing of social information, while the role of TnA remains unclear.

Application of reduced sensor movement sequences as a precursor for search area partitioning and a selection of discrete EEV contour-ring fragments for active electrolocation.

In addition to their visual sense, weakly electric fish use active electrolocation to detect and analyse objects in their nearby environment. Their ability to generate and sense electric fields combined with scanning-like swimming movements are intended to extract further parameters like the size, shape and material properties of objects. Inspired by this biological example, this work introduces an application for active electrolocation based on reduced sensor movement sequences as presented in Wolf-Homeyer et al (2016 Bioinspir. Biomim. 11 055002). Initially, the application is conducted with a simulated receptor-system consisting of an emitter-dipole and an orthogonally arranged pair of sensor-electrodes. Close inspection of a minimal set of scanning movements allows the exclusion of sectors of the general search area early in the proposed localization algorithm (search area partitioning). Furthermore, the proposed algorithm is based on an analytical representation of the electric field and of the so-called EEV (ensemble of electrosensory viewpoints) (Solberg et al 2008 Int. J. Robot. Res. 27 529-48) rather than using computationally expensive FEM simulations, rendering it suitable for embedded computer systems. Two-dimensional discrete EEV contour-ring points (CRPs) of desired accuracy are extracted. In the core of the localization algorithm, fragments of the EEV are selected from valid sectors of the search area, which generates sets of CRPs, one for each sensor-emitter position/orientation. These sets are investigated by means of a nearness metric to find points in different sets which correspond to each other in order to estimate the object position. Two resultant scanning strategies/localization algorithms are introduced.

Electric pulse characteristics can enable species recognition in African weakly electric fish species.

Communication is key to a wide variety of animal behaviours and multiple modalities are often involved in this exchange of information from sender to receiver. The communication of African weakly electric fish, however, is thought to be predominantly unimodal and is mediated by their electric sense, in which species-specific electric organ discharges (EODs) are generated in a context-dependent and thus variable sequence of pulse intervals (SPI). While the primary function of the electric sense is considered to be electrolocation, both of its components likely carry information regarding identity of the sender. However, a clear understanding of their contribution to species recognition is incomplete. We therefore analysed these two electrocommunication components (EOD waveform and SPI statistics) in two sympatric mormyrid Campylomormyrus species. In a set of five playback conditions, we further investigated which components may drive interspecific recognition and discrimination. While we found that both electrocommunication components are species-specific, the cues necessary for species recognition differ between the two species studied. While the EOD waveform and SPI were both necessary and sufficient for species recognition in C. compressirostris males, C. tamandua males apparently utilize other, non-electric modalities. Mapped onto a recent phylogeny, our results suggest that discrimination by electric cues alone may be an apomorphic trait evolved during a recent radiation in this taxon.

Physiological evidence of sensory integration in the electrosensory lateral line lobe of Gnathonemus petersii.

Mormyrid fish rely on reafferent input for active electrolocation. Their electrosensory input consists of phase and amplitude information. These are encoded by differently tuned receptor cells within the Mormyromasts, A- and B-cells, respectively, which are distributed over the animal's body. These convey their information to two topographically ordered medullary zones in the electrosensory lateral line lobe (ELL). The so-called medial zone receives only amplitude information, while the dorsolateral zone receives amplitude and phase information. Using both sources of information, Mormyrid fish can disambiguate electrical impedances. Where and how this disambiguation takes place is presently unclear. We here investigate phase-sensitivity downstream from the electroreceptors. We provide first evidence of phase-sensitivity in the medial zone of ELL. In this zone I-cells consistently decreased their rate to positive phase-shifts (6 of 20 cells) and increased their rate to negative shifts (11/20), while E-cells of the medial zone (3/9) responded oppositely to I-cells. In the dorsolateral zone the responses of E- and I-cells were opposite to those found in the medial zone. Tracer injections revealed interzonal projections that interconnect the dorsolateral and medial zones in a somatotopic manner. In summary, we show that phase information is processed differently in the dorsolateral and the medial zones. This is the first evidence for a mechanism that enhances the contrast between two parallel sensory channels in Mormyrid fish. This could be beneficial for impedance discrimination that ultimately must rely on a subtractive merging of these two sensory streams.

Male-mediated species recognition among African weakly electric fishes.

Effective communication among sympatric species is often instrumental for behavioural isolation, where the failure to successfully discriminate between potential mates could lead to less fit hybrid offspring. Discrimination between con- and heterospecifics tends to occur more often in the sex that invests more in offspring production, i.e. females, but males may also mediate reproductive isolation. In this study, we show that among two Campylomormyrus African weakly electric fish species, males preferentially associate with conspecific females during choice tests using live fish as stimuli, i.e. when all sensory modalities potentially used for communication were present. We then conducted playback experiments to determine whether the species-specific electric organ discharge (EOD) used for electrocommunication serves as the cue for this conspecific association preference. Interestingly, only C. compressirostris males associated significantly more with the conspecific EOD waveform when playback stimuli were provided, while no such association preference was observed in C. tamandua males. Given our results, the EOD appears to serve, in part, as a male-mediated pre-zygotic isolation mechanism among sympatric species. However, the failure of C. tamandua males to discriminate between con- and heterospecific playback discharges suggests that multiple modalities may be necessary for species recognition in some African weakly electric fish species.

Motion parallax in electric sensing.

A crucial step in forming spatial representations of the environment involves the estimation of relative distance. Active sampling through specific movements is considered essential for optimizing the sensory flow that enables the extraction of distance cues. However, in electric sensing, direct evidence for the generation and exploitation of sensory flow is lacking. Weakly electric fish rely on a self-generated electric field to navigate and capture prey in the dark. This electric sense provides a blurred representation of the environment, making the exquisite sensory abilities of electric fish enigmatic. Stereotyped back-and-forth swimming patterns reminiscent of visual peering movements are suggestive of the active generation of sensory flow, but how motion contributes to the disambiguation of the electrosensory world remains unclear. Here, we show that a dipole-like electric field geometry coupled to motion provides the physical basis for a nonvisual parallax. We then show in a behavioral assay that this cue is used for electrosensory distance perception across phylogenetically distant taxa of weakly electric fish. Notably, these species electrically sample the environment in temporally distinct ways (using discrete pulses or quasisinusoidal waves), suggesting a ubiquitous role for parallax in electric sensing. Our results demonstrate that electrosensory information is extracted from sensory flow and used in a behaviorally relevant context. A better understanding of motion-based electric sensing will provide insight into the sensorimotor coordination required for active sensing in general and may lead to improved electric field-based imaging applications in a variety of contexts.

Sensing External and Self-Motion with Hair Cells: A Comparison of the Lateral Line and Vestibular Systems from a Developmental and Evolutionary Perspective.

Detection of motion is a feature essential to any living animal. In vertebrates, mechanosensory hair cells organized into the lateral line and vestibular systems are used to detect external water or head/body motion, respectively. While the neuronal components to detect these physical attributes are similar between the two sensory systems, the organizational pattern of the receptors in the periphery and the distribution of hindbrain afferent and efferent projections are adapted to the specific functions of the respective system. Here we provide a concise review comparing the functional organization of the vestibular and lateral line systems from the development of the organs to the wiring from the periphery and the first processing stages. The goal of this review is to highlight the similarities and differences to demonstrate how evolution caused a common neuronal substrate to adapt to different functions, one for the detection of external water stimuli and the generation of sensory maps and the other for the detection of self-motion and the generation of motor commands for immediate behavioral reactions.

Sensory Flow as a Basis for a Novel Distance Cue in Freely Behaving Electric Fish.

The sensory input that an animal receives is directly linked to its motor activity. Behavior thus enables animals to influence their sensory input, a concept referred to as active sensing. How such behavior can serve as a scaffold for generating sensory information is of general scientific interest. In this article, we investigate how behavior can shape sensory information by using some unique features of the sensorimotor system of the weakly electric fish. Based on quantitative behavioral characterizations and computational reconstruction of sensory input, we show how electrosensory flow is actively created during highly patterned, spontaneous behavior in Gnathonemus petersii. The spatiotemporal structure of the sensory input provides information for the computation of a novel distance cue, which allows for a continuous estimation of distance. This has significant advantages over previously known nondynamic distance estimators as determined from electric image blur. Our investigation of the sensorimotor interactions in pulsatile electrolocation shows, for the first time, that the electrosensory flow contains behaviorally relevant information accessible only through active behavior. As patterned sensory behaviors are a shared feature of (active) sensory systems, our results have general implications for the understanding of (active) sensing, with the proposed sensory flow-based measure being potentially pertinent to a broad range of sensory modalities. SIGNIFICANCE STATEMENT: Acquisition of sensory information depends on motion, as either an animal or its sensors move. Behavior can thus actively influence the sensory flow; and in this way, behavior can be seen as a manifestation of the brain's integrative functions. The properties of the active pulsatile electrolocation system in Gnathonemus petersii allow for the sensory input to be computationally reconstructed, enabling us to link the informational content of spatiotemporal sensory dynamics to behavior. Our study reveals a novel sensory cue for estimating depth that is actively generated by the fishes' behavior. The physical and behavioral similarities between electrolocation and other active sensory systems suggest that this may be a mechanism shared by (active) sensory systems.

Modeling latency code processing in the electric sense: from the biological template to its VLSI implementation.

Understanding the coding of sensory information under the temporal constraints of natural behavior is not yet well resolved. There is a growing consensus that spike timing or latency coding can maximally exploit the timing of neural events to make fast computing elements and that such mechanisms are essential to information processing functions in the brain. The electric sense of mormyrid fish provides a convenient biological model where this coding scheme can be studied. The sensory input is a physically ordered spatial pattern of current densities, which is coded in the precise timing of primary afferent spikes. The neural circuits of the processing pathway are well known and the system exhibits the best known illustration of corollary discharge, which provides the reference to decoding the sensory afferent latency pattern. A theoretical model has been constructed from available electrophysiological and neuroanatomical data to integrate the principal traits of the neural processing structure and to study sensory interaction with motor-command-driven corollary discharge signals. This has been used to explore neural coding strategies at successive stages in the network and to examine the simulated network capacity to reproduce output neuron responses. The model shows that the network has the ability to resolve primary afferent spike timing differences in the sub-millisecond range, and that this depends on the coincidence of sensory and corollary discharge-driven gating signals. In the integrative and output stages of the network, corollary discharge sets up a proactive background filter, providing temporally structured excitation and inhibition within the network whose balance is then modulated locally by sensory input. This complements the initial gating mechanism and contributes to amplification of the input pattern of latencies, conferring network hyperacuity. These mechanisms give the system a robust capacity to extract behaviorally meaningful features of the electric image with high sensitivity over a broad working range. Since the network largely depends on spike timing, we finally discuss its suitability for implementation in robotic applications based on neuromorphic hardware.

Electrolocation of objects in fluids by means of active sensor movements based on discrete EEVs.

Weakly electric fish use self-generated electric fields for communication and for active electrolocation. The sensor part of the biological system consists of a vast amount of electroreceptors which are distributed across the skin of the electric fish. Fish utilise changes of their position and body geometry to aid in the extraction of sensory information. Inspired by the biological model, this study looks for a fixed, minimal scanning strategy compiled of active receptor-system movements that allows unique identification of the positions of objects in the vicinity. The localisation method is based on the superposition of numerical extracted contour-rings of rotated and/or linearly shifted EEVs (Solberg et al 2008 Int. J. Rob. Res. 27 529-48), simulated by means of FEM. For the evaluation of a movement sequence, matrices of unique intersection points and respective contrast functions are introduced. The resultant optimal scanning strategy consists of a combination of a linear shift and a rotation of the original EEV.

Somatotopic map of the active electrosensory sense in the midbrain of the mormyrid Gnathonemus petersii.

In many vertebrates parallel processing in topographically ordered maps is essential for efficient sensory processing. In the active electrosensory pathway of mormyrids afferent input is processed in two parallel somatotopically ordered hindbrain maps of the electrosensory lateral line lobe (ELL), the dorsolateral zone (DLZ), and the medial zone (MZ). Here phase and amplitude modulations of the self-generated electric field were processed separately. Behavioral data indicates that this information must be merged for the sensory system to categorically distinguish capacitive and resistive properties of objects. While projections between both zones of the ELL have been found, the available physiological data suggests that this merging takes place in the midbrain torus semicircularis (TS). Previous anatomical data indicate that the detailed somatotopic representation present in the ELL is lost in the nucleus lateralis (NL) of the TS, while a rough rostrocaudal mapping is maintained. In our study we investigated the projections from the hindbrain to the midbrain in more detail, using tracer injections. Our data reveals that afferents from both maps of the ELL terminate in a detailed somatotopic manner within the midbrain NL. Furthermore, we provide data indicating that phase and amplitude information may indeed be processed jointly in the NL. J. Comp. Neurol. 524:2479-2491, 2016. © 2016 Wiley Periodicals, Inc.

Adaptation-induced modification of motion selectivity tuning in visual tectal neurons of adult zebrafish.

In the developing brain, training-induced emergence of direction selectivity and plasticity of orientation tuning appear to be widespread phenomena. These are found in the visual pathway across different classes of vertebrates. Moreover, short-term plasticity of orientation tuning in the adult brain has been demonstrated in several species of mammals. However, it is unclear whether neuronal orientation and direction selectivity in nonmammalian species remains modifiable through short-term plasticity in the fully developed brain. To address this question, we analyzed motion tuning of neurons in the optic tectum of adult zebrafish by calcium imaging. In total, orientation and direction selectivity was enhanced by adaptation, responses of previously orientation-selective neurons were sharpened, and even adaptation-induced emergence of selectivity in previously nonselective neurons was observed in some cases. The different observed effects are mainly based on the relative distance between the previously preferred and the adaptation direction. In those neurons in which a shift of the preferred orientation or direction was induced by adaptation, repulsive shifts (i.e., away from the adapter) were more prevalent than attractive shifts. A further novel finding for visually induced adaptation that emerged from our study was that repulsive and attractive shifts can occur within one brain area, even with uniform stimuli. The type of shift being induced also depends on the difference between the adapting and the initially preferred stimulus direction. Our data indicate that, even within the fully developed optic tectum, short-term plasticity might have an important role in adjusting neuronal tuning functions to current stimulus conditions.

Comparative histology of the adult electric organ among four species of the genus Campylomormyrus (Teleostei: Mormyridae).

The electric organ (EO) of weakly electric mormyrids consists of flat, disk-shaped electrocytes with distinct anterior and posterior faces. There are multiple species-characteristic patterns in the geometry of the electrocytes and their innervation. To further correlate electric organ discharge (EOD) with EO anatomy, we examined four species of the mormyrid genus Campylomormyrus possessing clearly distinct EODs. In C. compressirostris, C. numenius, and C. tshokwe, all of which display biphasic EODs, the posterior face of the electrocytes forms evaginations merging to a stalk system receiving the innervation. In C. tamandua that emits a triphasic EOD, the small stalks of the electrocyte penetrate the electrocyte anteriorly before merging on the anterior side to receive the innervation. Additional differences in electrocyte anatomy among the former three species with the same EO geometry could be associated with further characteristics of their EODs. Furthermore, in C. numenius, ontogenetic changes in EO anatomy correlate with profound changes in the EOD. In the juvenile the anterior face of the electrocyte is smooth, whereas in the adult it exhibits pronounced surface foldings. This anatomical difference, together with disparities in the degree of stalk furcation, probably contributes to the about 12 times longer EOD in the adult.

More a finger than a nose: the trigeminal motor and sensory innervation of the Schnauzenorgan in the elephant-nose fish Gnathonemus petersii.

The weakly electric fish Gnathonemus petersii uses its electric sense to actively probe the environment. Its highly mobile chin appendage, the Schnauzenorgan, is rich in electroreceptors. Physical measurements have demonstrated the importance of the position of the Schnauzenorgan in funneling the fish's self-generated electric field. The present study focuses on the trigeminal motor pathway that controls Schnauzenorgan movement and on its trigeminal sensory innervation and central representation. The nerves entering the Schnauzenorgan are very large and contain both motor and sensory trigeminal components as well as an electrosensory pathway. With the use of neurotracer techniques, labeled Schnauzenorgan motoneurons were found throughout the ventral main body of the trigeminal motor nucleus but not among the population of larger motoneurons in its rostrodorsal region. The Schnauzenorgan receives no motor or sensory innervation from the facial nerve. There are many anastomoses between the peripheral electrosensory and trigeminal nerves, but these senses remain separate in the sensory ganglia and in their first central relays. Schnauzenorgan trigeminal primary afferent projections extend throughout the descending trigeminal sensory nuclei, and a few fibers enter the facial lobe. Although no labeled neurons could be identified in the brain as the trigeminal mesencephalic root, some Schnauzenorgan trigeminal afferents terminated in the trigeminal motor nucleus, suggesting a monosynaptic, possibly proprioceptive, pathway. In this first step toward understanding multimodal central representation of the Schnauzenorgan, no direct interconnections were found between the trigeminal sensory and electromotor command system, or the electrosensory and trigeminal motor command. The pathways linking perception to action remain to be studied.

Motor patterns during active electrosensory acquisition.

Motor patterns displayed during active electrosensory acquisition of information seem to be an essential part of a sensory strategy by which weakly electric fish actively generate and shape sensory flow. These active sensing strategies are expected to adaptively optimize ongoing behavior with respect to either motor efficiency or sensory information gained. The tight link between the motor domain and sensory perception in active electrolocation make weakly electric fish like Gnathonemus petersii an ideal system for studying sensory-motor interactions in the form of active sensing strategies. Analyzing the movements and electric signals of solitary fish during unrestrained exploration of objects in the dark, we here present the first formal quantification of motor patterns used by fish during electrolocation. Based on a cluster analysis of the kinematic values we categorized the basic units of motion. These were then analyzed for their associative grouping to identify and extract short coherent chains of behavior. This enabled the description of sensory behavior on different levels of complexity: from single movements, over short behaviors to more complex behavioral sequences during which the kinematics alter between different behaviors. We present detailed data for three classified patterns and provide evidence that these can be considered as motor components of active sensing strategies. In accordance with the idea of active sensing strategies, we found categorical motor patterns to be modified by the sensory context. In addition these motor patterns were linked with changes in the temporal sampling in form of differing electric organ discharge frequencies and differing spatial distributions. The ability to detect such strategies quantitatively will allow future research to investigate the impact of such behaviors on sensing.