Publications by authors named "Jacob Engelmann"

46 Publications

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

Front Behav Neurosci 2021 11;15:718491. Epub 2021 Oct 11.

Active Sensing, Faculty of Biology, Bielefeld University, Bielefeld, Germany.

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 . 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.
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http://dx.doi.org/10.3389/fnbeh.2021.718491DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8542711PMC
October 2021

Motion parallax for object localization in electric fields.

Bioinspir Biomim 2021 12 22;17(1). Epub 2021 Dec 22.

Biomechatronics Group, Faculty of Engineering and Mathematics, University of Applied Sciences, Bielefeld, Germany.

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.
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http://dx.doi.org/10.1088/1748-3190/ac3215DOI Listing
December 2021

Linking active sensing and spatial learning in weakly electric fish.

Curr Opin Neurobiol 2021 12 12;71:1-10. Epub 2021 Aug 12.

Department of Cell and Molecular Medicine, Brain and Mind Institute and Centre for Neural Dynamics, University of Ottawa Ottawa, Ontario, K1H 8M5, Canada. Electronic address:

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.
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http://dx.doi.org/10.1016/j.conb.2021.07.002DOI Listing
December 2021

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

J Neurosci 2020 01 9;40(5):1097-1109. Epub 2019 Dec 9.

AG Active Sensing, Faculty of Biology/Cluster of Excellence Cognitive Interaction Technology, Bielefeld University, D-33501 Bielefeld, Germany, and

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 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. 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 , 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.
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http://dx.doi.org/10.1523/JNEUROSCI.1024-19.2019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6989011PMC
January 2020

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

Behav Brain Res 2019 05 7;364:41-49. Epub 2019 Feb 7.

Center for Mind/Brain Sciences, University of Trento, Piazza Manifattura 1, I-38068 Rovereto, Italy. Electronic address:

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.
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http://dx.doi.org/10.1016/j.bbr.2019.02.013DOI Listing
May 2019

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.

Bioinspir Biomim 2018 10 16;13(6):066008. Epub 2018 Oct 16.

Biomechatronics Group, Faculty of Engineering and Mathematics, University of Applied Sciences, Bielefeld, Germany. Active Sensing, Faculty of Biology, Bielefeld University, Bielefeld, Germany.

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.
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http://dx.doi.org/10.1088/1748-3190/aae23fDOI Listing
October 2018

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

Sci Rep 2018 Jul 17;8(1):10799. Epub 2018 Jul 17.

Unit of Evolutionary Biology and Systematic Zoology, Institute of Biochemistry/Biology, University of Potsdam, 14476, Potsdam, Germany.

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.
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http://dx.doi.org/10.1038/s41598-018-29132-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6050243PMC
July 2018

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

PLoS One 2018 11;13(4):e0194347. Epub 2018 Apr 11.

University of Bonn, Institute for Zoology, Bonn, Germany.

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.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0194347PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5894992PMC
July 2018

Male-mediated species recognition among African weakly electric fishes.

R Soc Open Sci 2018 Feb 14;5(2):170443. Epub 2018 Feb 14.

Institute of Biochemistry and Biology, Unit of Evolutionary Biology/Systematic Zoology, University of Potsdam, 14476 Potsdam, Germany.

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 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 males associated significantly more with the conspecific EOD waveform when playback stimuli were provided, while no such association preference was observed in 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 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.
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http://dx.doi.org/10.1098/rsos.170443DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5830707PMC
February 2018

Motion parallax in electric sensing.

Proc Natl Acad Sci U S A 2018 01 2;115(3):573-577. Epub 2018 Jan 2.

Department of Biology, University of Ottawa, Ottawa, ON, K1N 6N5 Canada;

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.
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http://dx.doi.org/10.1073/pnas.1712380115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5776971PMC
January 2018

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

Brain Behav Evol 2017 9;90(2):98-116. Epub 2017 Oct 9.

Ludwig-Maximilians-Universität München, Department Biology II, Division of Neurobiology, Martinsried-Planegg, Germany.

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.
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http://dx.doi.org/10.1159/000456646DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5653922PMC
May 2018

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

J Neurosci 2017 01;37(2):302-312

Bielefeld University, Active Sensing, Cognitive Interaction Technology-Center of Excellence and Faculty of Biology, 33501 Bielefeld, Germany, and

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.
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http://dx.doi.org/10.1523/JNEUROSCI.1361-16.2016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6596575PMC
January 2017

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

Bioinspir Biomim 2016 09 13;11(5):055007. Epub 2016 Sep 13.

Bielefeld University, Faculty of Biology/CITEC, AG Active Sensing, Universitätsstraße 25, 33615 Bielefeld, Germany.

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.
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http://dx.doi.org/10.1088/1748-3190/11/5/055007DOI Listing
September 2016

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

Bioinspir Biomim 2016 08 17;11(5):055002. Epub 2016 Aug 17.

Biomechatronics Group, Faculty of Engineering and Mathematics, University of Applied Sciences, Bielefeld, Germany.

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.
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http://dx.doi.org/10.1088/1748-3190/11/5/055002DOI Listing
August 2016

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

J Comp Neurol 2016 08 2;524(12):2479-91. Epub 2016 Feb 2.

Department of Biology, Active Sensing and Center of Excellence 'Cognitive Interaction Technology,', Bielefeld University, Bielefeld, Germany.

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.
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http://dx.doi.org/10.1002/cne.23963DOI Listing
August 2016

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

J Neurophysiol 2015 Nov 16;114(5):2893-902. Epub 2015 Sep 16.

Active Sensing and Center of Excellence Cognitive Interaction Technology, Bielefeld University, Bielefeld, Germany; and.

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.
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http://dx.doi.org/10.1152/jn.00568.2015DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4737423PMC
November 2015

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

J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2015 Apr 10;201(4):357-74. Epub 2015 Mar 10.

Unit of Evolutionary Biology/Systematic Zoology, Institute of Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Str. 24-25, Haus 26, 14476, Potsdam-Golm, Germany.

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.
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http://dx.doi.org/10.1007/s00359-015-0995-6DOI Listing
April 2015

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

J Comp Neurol 2015 Apr 19;523(5):769-89. Epub 2014 Dec 19.

Department of Neuroethology/Sensory Ecology, Institute for Zoology, University of Bonn, Bonn, Germany.

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.
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http://dx.doi.org/10.1002/cne.23710DOI Listing
April 2015

Motor patterns during active electrosensory acquisition.

Front Behav Neurosci 2014 28;8:186. Epub 2014 May 28.

Active Sensing, Faculty of Biology, Cognitive Interaction Technology - Center of Excellence, Bielefeld University Bielefeld, Germany.

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.
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http://dx.doi.org/10.3389/fnbeh.2014.00186DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4036139PMC
June 2014

Grouped retinae and tapetal cups in some Teleostian fish: occurrence, structure, and function.

Prog Retin Eye Res 2014 Jan 22;38:43-69. Epub 2013 Oct 22.

Paul-Flechsig-Institute of Brain Research, Leipzig University, Leipzig, Germany. Electronic address:

This article presents a summary and critical review of what is known about the 'grouped retina', a peculiar type of retinal organization in fish in which groups of photoreceptor cell inner and outer segments are arranged in spatially separated bundles. In most but not all cases, these bundles are embedded in light-reflective cups that are formed by the retinal pigment epithelial cells. These cups constitute a specialized type of retinal tapetum (i.e., they are biological 'mirrors' that cause eye shine) and appear to be optimized for different purposes in different fishes. Generally, the large retinal pigment epithelial cells are filled with light-reflecting photonic crystals that consist of guanine, uric acid, or pteridine depending on species, and which ensure that the incoming light becomes directed onto the photoreceptor outer segments. This structural specialization has so far been found in representatives of 17 fish families; of note, not all members of a given family must possess a grouped retina, and the 17 families are not all closely related to each other. In many cases (e.g., in Osteoglossomorpha and Aulopiformes) the inner surface of the cup is formed by three to four layers of strikingly regularly shaped and spaced guanine platelets acting as an optical multilayer. It has been estimated that this provides an up to 10fold increase of the incident light intensity. In certain deep-sea fish (many Aulopiformes and the Polymixidae), small groups of rods are embedded in such 'parabolic mirrors'; most likely, this is an adaptation to the extremely low light intensities available in their habitat. Some of these fishes additionally possess similar tapetal cups that surround individual cones and, very likely, also serve as amplifiers of the weak incident light. In the Osteoglossomorpha, however, that inhabit the turbid water of rivers or streams, the structure of the cups is more complex and undergoes adaptation-dependent changes. At dim daylight, probably representing the usual environmental conditions of the fish, the outer segments of up to 30 cone cells are placed at the bottom of the cup where light intensity is maximized. Strikingly, however, a large number of rod receptor cells are positioned behind each mirroring cup. This peculiar arrangement (i) allows vision at deep red wavelenghts, (ii) matches the sensitivity of rod and cone photoreceptors, and (iii) facilitates the detection of low-contrast and color-mixed stimuli, within the dim, turbid habitat. Thus, for these fish the grouped retina appears to aid in reliable and quick detection of large, fast moving, biologically relevant stimuli such as predators. Overall, the grouped retina appears as a peculiar type of general retinal specialization in a variety of fish species that is adaptive in particular habitats such as turbid freshwater but also the deep-sea. The authors were prompted to write this review by working on the retina of Gnathonemus petersii; the data resulting from this work (Landsberger et al., 2008; Kreying et al., 2012) are included in the present review.
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http://dx.doi.org/10.1016/j.preteyeres.2013.10.001DOI Listing
January 2014

Spatial resolution of an eye containing a grouped retina: ganglion cell morphology and tectal physiology in the weakly electric fish Gnathonemus petersii.

J Comp Neurol 2013 Dec;521(17):4075-93

Bonn University, Institute of Zoology, Department Neuroethology/Sensory Ecology, 53115, Bonn, Germany.

The retina of the weakly electric fish Gnathonemus petersii is a so-called grouped retina where photoreceptors are bundled. These bundles are regarded as functional units and this type of retinal specialization is uniquely found in teleosts. To understand how this anatomical organization influences visual information processing we investigated the morphology and distribution of retinal ganglion cells (GCs) and the response properties of retinal afferents terminating in the major retinorecipient area, the optic tectum. GCs were classified based on their dendritic morphology (dendritic field diameters <90-100 μm: narrow-field GCs; 110-280 μm: widefield GCs; >280 μm: giant GCs). Within these classes subtypes were distinguished based on the ramification patterns of the dendrites in the sublaminae of the inner plexiform layer. Properties of presumed optic nerve terminals were investigated in the optic tectum using extracellular recordings. Physiological classes could be observed based on their response to visual stimuli (on; off; on-off, and fast units). Receptive field sizes and spatiotemporal properties were classified and the topographical representation of the visual space was mapped in the tectum. Gratings of low spatial frequencies were best responded to and followed up to high temporal frequencies (>30 Hz). Most of the recorded units were directionally selective. No evidence of distorted topographies in the tectum was found, i.e., no overrepresentation of the retina was seen in the tectum opticum. The grouped retina of G. petersii seems to be optimized for the detection of large, fast objects in an environment of low optical quality.
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http://dx.doi.org/10.1002/cne.23397DOI Listing
December 2013

Sensory flow shaped by active sensing: sensorimotor strategies in electric fish.

J Exp Biol 2013 Jul;216(Pt 13):2487-500

Bielefeld University, Faculty of Biology/CITEC, AG Active Sensing, Universitätsstraße 25, 33615 Bielefeld, Germany.

Goal-directed behavior in most cases is composed of a sequential order of elementary motor patterns shaped by sensorimotor contingencies. The sensory information acquired thus is structured in both space and time. Here we review the role of motion during the generation of sensory flow focusing on how animals actively shape information by behavioral strategies. We use the well-studied examples of vision in insects and echolocation in bats to describe commonalities of sensory-related behavioral strategies across sensory systems, and evaluate what is currently known about comparable active sensing strategies in electroreception of electric fish. In this sensory system the sensors are dispersed across the animal's body and the carrier source emitting energy used for sensing, the electric organ, is moved while the animal moves. Thus ego-motions strongly influence sensory dynamics. We present, for the first time, data of electric flow during natural probing behavior in Gnathonemus petersii (Mormyridae), which provide evidence for this influence. These data reveal a complex interdependency between the physical input to the receptors and the animal's movements, posture and objects in its environment. Although research on spatiotemporal dynamics in electrolocation is still in its infancy, the emerging field of dynamical sensory systems analysis in electric fish is a promising approach to the study of the link between movement and acquisition of sensory information.
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http://dx.doi.org/10.1242/jeb.082420DOI Listing
July 2013

Monitoring of single-cell responses in the optic tectum of adult zebrafish with dextran-coupled calcium dyes delivered via local electroporation.

PLoS One 2013 7;8(5):e62846. Epub 2013 May 7.

AG Active Sensing and Center of Excellence 'Cognitive Interaction Technology', Bielefeld University, Bielefeld, Germany.

The zebrafish (Danio rerio) has become one of the major animal models for in vivo examination of sensory and neuronal computation. Similar to Xenopus tadpoles neural activity in the optic tectum, the major region controlling visually guided behavior, can be examined in zebrafish larvae by optical imaging. Prerequisites of these approaches are usually the transparency of larvae up to a certain age and the use of two-photon microscopy. This principle of fluorescence excitation was necessary to suppress crosstalk between signals from individual neurons, which is a critical issue when using membrane-permeant dyes. This makes the equipment to study neuronal processing costly and limits the approach to the study of larvae. Thus there is lack of knowledge about the properties of neurons in the optic tectum of adult animals. We established a procedure to circumvent these problems, enabling in vivo calcium imaging in the optic tectum of adult zebrafish. Following local application of dextran-coupled dyes single-neuron activity of adult zebrafish can be monitored with conventional widefield microscopy, because dye labeling remains restricted to tens of neurons or less. Among the neurons characterized with our technique we found neurons that were selective for a certain pattern orientation as well as neurons that responded in a direction-selective way to visual motion. These findings are consistent with previous studies and indicate that the functional integrity of neuronal circuits in the optic tectum of adult zebrafish is preserved with our staining technique. Overall, our protocol for in vivo calcium imaging provides a useful approach to monitor visual responses of individual neurons in the optic tectum of adult zebrafish even when only widefield microscopy is available. This approach will help to obtain valuable insight into the principles of visual computation in adult vertebrates and thus complement previous work on developing visual circuits.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0062846PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3647071PMC
December 2013

Research focus on neuroethology. Editorial.

Authors:
Jacob Engelmann

J Physiol Paris 2013 Jan-Apr;107(1-2). Epub 2012 Oct 17.

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http://dx.doi.org/10.1016/j.jphysparis.2012.10.001DOI Listing
June 2015

From static electric images to electric flow: towards dynamic perceptual cues in active electroreception.

J Physiol Paris 2013 Jan-Apr;107(1-2):95-106. Epub 2012 Jul 7.

Bielefeld University, Faculty of Biology, AG Active Sensing, Universitätsstraße 25, 33615 Bielefeld, Germany.

Active electroreception is an ancestral trait found in many aquatic vertebrates and has evolved independently in two teleost lineages, the Gymnotiformes and the Mormyriformes. Unique to these so-called weakly electric fish is their ability to actively generate electrical currents in the water and sense the electrical properties of the environment. How natural behavior contributes to this sensory system has been of interest to neuroethologists since the pioneering works of Lissmann. Here we report on a mutual modeling and experimental study of the stimuli available during active electrolocation of Gnathonemus petersii (Mormyridae). We show the validity of the model (I) by demonstrating that localized spatial patterns of object induced modulations in the electric field (electric images) are comparable to experimentally mapped 2-dimensional electric images and (II) by replicating earlier key findings showing that a normalized metric of electric image width provides an unambiguous cue for distance estimation. We then show that electric images and the distance metric vary systematically when an object is moved along the trunk. These potential ambiguities with regard to localization lead us to a spatiotemporal analysis of electric images. We introduce a new temporal metric for distance estimation that is based on the normalized spatial properties of electrical images. Finally, based on a survey of exploratory behavior, we show how objects situated at the tail, a region previously neglected, cast global electric images that extend over the whole sensory epithelium of the animals.
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http://dx.doi.org/10.1016/j.jphysparis.2012.06.003DOI Listing
June 2015

A grouped retina provides high temporal resolution in the weakly electric fish Gnathonemus petersii.

J Physiol Paris 2013 Jan-Apr;107(1-2):84-94. Epub 2012 Jul 3.

Bielefeld University, Faculty of Biology, AG Active Sensing, Universitätsstraße 25, 33615 Bielefeld, Germany. Electronic address:

Weakly electric fish orient, hunt and communicate by emitting electrical pulses, enabling them to discriminate objects, conspecifics and prey. In addition to the electrosensory modality - although dominating in importance in these fishes - other modalities, like vision, play important roles for survival. The visual system of Gnathonemus petersii, a member of the family mormyridae living in West African blackwater streams shows remarkable specializations: Cone photoreceptors are grouped in bundles within a light reflecting tapetum lucidum, while the rods are also bundled but located at the back within a light-scattering guanine layer. Such an organization does not improve light sensitivity nor does it provide high spatial resolution. Thus, the function of the grouped retinal arrangement for the visual performance of the fish remains unclear. Here we investigated the contrast sensitivity of the temporal transfer properties of the visual system of Gnathonemus. To do so, we analyzed visual evoked potentials in the optic tectum and tested the critical flicker fusion frequency in a behavioral paradigm. Results obtained in Gnathonemus are compared to results obtained with goldfish (Carassius auratus), revealing differences in the filter characteristics of their visual systems: While goldfish responds best to low frequencies, Gnathonemus responds best at higher frequencies. The visual system of goldfish shows characteristics of a low-pass filter while the visual system of Gnathonemus has characteristics of a band-pass filter. Furthermore we show that the visual system of Gnathonemus is more robust towards contrast reduction as compared to the goldfish. The grouped retina might enable Gnathonemus to see large, fast moving objects even under low contrast conditions. Due to the fact that the electric sense is a modality of limited range, it is tempting to speculate that the retinal specialization of Gnathonemus petersii might be advantageous for predator avoidance even when brightness differences are small.
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http://dx.doi.org/10.1016/j.jphysparis.2012.06.002DOI Listing
June 2015

Photonic crystal light collectors in fish retina improve vision in turbid water.

Science 2012 Jun;336(6089):1700-3

Cavendish Laboratory, Department of Physics, University of Cambridge, Cambridge CB3 0HE, UK.

Despite their diversity, vertebrate retinae are specialized to maximize either photon catch or visual acuity. Here, we describe a functional type that is optimized for neither purpose. In the retina of the elephantnose fish (Gnathonemus petersii), cone photoreceptors are grouped together within reflecting, photonic crystal-lined cups acting as macroreceptors, but rod photoreceptors are positioned behind these reflectors. This unusual arrangement matches rod and cone sensitivity for detecting color-mixed stimuli, whereas the photoreceptor grouping renders the fish insensitive to spatial noise; together, this enables more reliable flight reactions in the fish's dim and turbid habitat as compared with fish lacking this retinal specialization.
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http://dx.doi.org/10.1126/science.1218072DOI Listing
June 2012

Temporal precision and reliability in the velocity regime of a hair-cell sensory system: the mechanosensory lateral line of goldfish, Carassius auratus.

J Neurophysiol 2012 May 29;107(10):2581-93. Epub 2012 Feb 29.

Univ. of Bielefeld, AG Active Sensing, 33501 Bielefeld, Germany.

Fish and aquatic frogs detect minute water motion by means of a specialized mechanosensory system, the lateral line. Ubiquitous in fish, the lateral-line system is characterized by hair-cell based sensory structures across the fish's surface called neuromasts. These neuromasts occur free-standing on the skin as superficial neuromasts (SN) or are recessed into canals as canal neuromasts. SNs respond to rapid changes of water velocity in a small layer of fluid around the fish, including the so-called boundary layer. Although omnipresent, the boundary layer's impact on the SN response is still a matter of debate. For the first time using an information-theoretic approach to this sensory system, we have investigated the SN afferents encoding capabilities. Combining covariance analysis, phase analysis, and modeling of recorded neuronal responses of primary lateral line afferents, we show that encoding by the SNs is adequately described as a linear, velocity-responsive mechanism. Afferent responses display a bimodal distribution of opposite Wiener kernels that likely reflected the two hair-cell populations within a given neuromast. Using frozen noise stimuli, we further demonstrate that SN afferents respond in an extremely precise manner and with high reproducibility across a broad frequency band (10-150 Hz), revealing that an optimal decoder would need to rely extensively on a temporal code. This was further substantiated by means of signal reconstruction of spike trains that were time shifted with respect to their original. On average, a time shift of 3.5 ms was enough to diminish the encoding capabilities of primary afferents by 70%. Our results further demonstrate that the SNs' encoding capability is linearly related to the stimulus outside the boundary layer, and that the boundary layer can, therefore, be neglected while interpreting lateral line response of SN afferents to hydrodynamic stimuli.
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http://dx.doi.org/10.1152/jn.01073.2011DOI Listing
May 2012

3-Dimensional Scene Perception during Active Electrolocation in a Weakly Electric Pulse Fish.

Front Behav Neurosci 2010 28;4:26. Epub 2010 May 28.

Neuroethology/Sensory Ecology, Institute of Zoology, University of Bonn Bonn, Germany.

Weakly electric fish use active electrolocation for object detection and orientation in their environment even in complete darkness. The African mormyrid Gnathonemus petersii can detect object parameters, such as material, size, shape, and distance. Here, we tested whether individuals of this species can learn to identify 3-dimensional objects independently of the training conditions and independently of the object's position in space (rotation-invariance; size-constancy). Individual G. petersii were trained in a two-alternative forced-choice procedure to electrically discriminate between a 3-dimensional object (S+) and several alternative objects (S-). Fish were then tested whether they could identify the S+ among novel objects and whether single components of S+ were sufficient for recognition. Size-constancy was investigated by presenting the S+ together with a larger version at different distances. Rotation-invariance was tested by rotating S+ and/or S- in 3D. Our results show that electrolocating G. petersii could (1) recognize an object independently of the S- used during training. When only single components of a complex S+ were offered, recognition of S+ was more or less affected depending on which part was used. (2) Object-size was detected independently of object distance, i.e. fish showed size-constancy. (3) The majority of the fishes tested recognized their S+ even if it was rotated in space, i.e. these fishes showed rotation-invariance. (4) Object recognition was restricted to the near field around the fish and failed when objects were moved more than about 4 cm away from the animals. Our results indicate that even in complete darkness our G. petersii were capable of complex 3-dimensional scene perception using active electrolocation.
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http://dx.doi.org/10.3389/fnbeh.2010.00026DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2889722PMC
July 2011

Wake tracking and the detection of vortex rings by the canal lateral line of fish.

Phys Rev Lett 2009 Aug 13;103(7):078102. Epub 2009 Aug 13.

Physik Department T35, Technische Universität München, Garching bei München 85747, Germany.

Research on the lateral line of fish has mainly focused on the detection of oscillating objects. Yet many fish are able to track vortex wakes that arise from other fish. It is not yet known what the sensory input from a wake looks like and how fish can extract relevant information from it. We present a mathematical model to determine how vortices stimulate the canal lateral line and verify it by neuronal recordings. We also show how the information about the orientation of a vortex ring is captured by the lateral-line sensors so as to enable fish to follow a vortex street.
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http://dx.doi.org/10.1103/PhysRevLett.103.078102DOI Listing
August 2009
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