Electric signal synchronization as a behavioural strategy to generate social attention in small groups of mormyrid weakly electric fish and a mobile fish robot

African weakly electric fish communicate at night by constantly emitting and perceiving brief electrical signals (electric organ discharges, EOD) at variable inter-discharge intervals (IDI). While the waveform of single EODs contains information about the sender’s identity, the variable IDI patterns convey information about its current motivational and behavioural state. Pairs of fish can synchronize their EODs to each other via echo responses, and we have previously formulated a ‘social attention hypothesis’ stating that fish use echo responses to address specific individuals and establish brief dyadic communication frameworks within a group. Here, we employed a mobile fish robot to investigate the behaviour of small groups of up to four Mormyrus rume and characterized the social situations during which synchronizations occurred. An EOD-emitting robot reliably evoked social following behaviour, which was strongest in smaller groups and declined with increasing group size. We did not find significant differences in motor behaviour of M. rume with either an interactive playback (echo response) or a random control playback by the robot. Still, the robot reliably elicited mutual synchronizations with other fish. Synchronizations mostly occurred during relatively close social interactions, usually when the fish that initiated synchronization approached either the robot or another fish from a distance. The results support our social attention hypothesis and suggest that electric signal synchronization might facilitate the exchange of social information during a wide range of social behaviours from aggressive territorial displays to shoaling and even cooperative hunting in some mormyrids

The Mormyrid Optic Tectum Is a Topographic Interface for Active Electrolocation and Visual Sensing

The African weakly electric fish Gnathonemus petersii is capable of cross-modal object recognition using its electric sense or vision. Thus, object features stored in the brain are accessible by multiple senses, either through connections between unisensory brain regions or because of multimodal representations in multisensory areas. Primary electrosensory information is processed in the medullary electrosensory lateral line lobe, which projects topographically to the lateral nucleus of the torus semicircularis (NL). Visual information reaches the optic tectum (TeO), which projects to various other brain regions. We investigated the neuroanatomical connections of these two major midbrain visual and electrosensory brain areas, focusing on the topographical relationship of interconnections between the two structures. Thus, the neural tracer Dil was injected systematically into different tectal quadrants, as well as into the NL. Tectal tracer injections revealed topographically organized retrograde and anterograde label in the NL. Rostral and caudal tectal regions were interconnected with rostral and caudal areas of the NL, respectively. However, dorsal and ventral tectal regions were represented in a roughly inverted fashion in NL, as dorsal tectal injections labeled ventral areas in NL and vice versa. In addition, tracer injections into TeO or NL revealed extensive inputs to both structures from ipsilateral (NL also contralateral) efferent basal cells in the valvula cerebelli;the NL furthermore projected back to the valvula. Additional tectal and NL connections were largely confirmatory to earlier studies. For example, the TeO received ipsilateral inputs from the central zone of the dorsal telencephalon, torus longitudinalis, nucleus isthmi, various tegmental, thalamic and pretectal nuclei, as well as other nuclei of the torus semicircularis. Also, the TeO projected to the dorsal preglomerular and dorsal posterior thalamic nuclei as well as to nuclei in the torus semicircularis and nucleus isthmi. Beyond the clear topographical relationship of NL and TeO interconnections established here, the known neurosensory upstream circuitry was used to suggest a model of how a defined spot in the peripheral sensory world comes to be represented in a common associated neural locus both in the NL and the TeO, thereby providing the neural substrate for cross-modal object recognition

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

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

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

Fechner S, Grant K, von der Emde G, Engelmann J. Physiological evidence of sensory integration in the electrosensory lateral line lobe of Gnathonemus petersii. PLOS ONE. 2018;13(4): e0194347.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

The ecology of animal senses : Matched filters for economical sensing

The collection of chapters in this book present the concept of matched filters: Response characteristics “matching” the characteristics of crucially important sensory inputs, which allows detection of vital sensory stimuli while sensory inputs not necessary for the survival of the animal tend to be filtered out, or sacrificed. The individual contributions discuss that the evolution of sensing systems resulted from the necessity to achieve the most efficient sensing of vital information at the lowest possible energetic cost. Matched filters are found in all senses including vision, hearing, olfaction, mechanoreception, electroreception and infrared sensing and different cases will be referred to in detail

Classification of insects by echolocating greater horseshoe bats

Echolocating greater horseshoe bats (Rhinolophus ferrumequinum) detect insects by concentrating on the characteristic amplitude- and frequency modulation pattern fluttering insects impose on the returning echoes. This study shows that horseshoe bats can also further analyse insect echoes and thus recognize and categorize the kind of insect they are echolocating. Four greater horseshoe bats were trained in a twoalternative forced-choice procedure to choose the echo of one particular insect species turning its side towards the bat (Fig. 1). The bats were able to discriminate with over 90% correct choices between the reward-positive echo and the echoes of other insect species all fluttering with exactly the same wingbeat rate (Fig. 4). When the angular orientation of the reward-positive insect was changed (Fig. 2), the bats still preferred these unknown echoes over echoes from other insect species (Fig. 5) without any further training. Because the untrained bats did not show any prey preference, this indicates that the bats were able to perform an aspect-anglein-dependent classification of insects. Finally we tested what parameters in the echo were responsible for species recognition. It turned out that the bats especially used the small echo-modulations in between glints as a source of information (Fig. 7). Neither the amplitudenor the frequencymodulation of the echoes alone was sufficient for recognition of the insect species (Fig. 8). Bats performed a pattern recognition task based on complex computations of several acoustic parameters, an ability which might be termed cognitive

Active Electrolocation

Engelmann J, Gerhard von der E. Active Electrolocation. In: A.P. F, ed. Encyclopedia of Fish Physiology: From Genome to Environment. Vol 1. 1st ed. San Diego: Academic Press; 2011: 375-386

Sensory influence on navigation in the weakly electric fish Gnathonemus petersii

Most animals possess multiple sensory systems, which can be used during navigation. Different senses obtain environmental information on different spatial scales and thus provide a different basis for efficient navigation. Here we used the weakly electric fish Gnathonemus petersii to investigate how different sensory inputs influence the navigational strategy and whether landmark information can be transferred flexibly between two sensory systems. Fish were trained to swim through a maze using a particular route indicated by either visual landmarks, electrical landmarks or without any landmarks. In subsequent tests, egocentric (internal cues, such as motion patterns) and allocentric cues (external cues like landmarks) were put in conflict by relocating the local landmarks. We found that all fish, independent of the available sensory input, chose the egocentric over the allocentric route. However, visual landmarks significantly improved the training duration compared to the other groups, suggesting an involvement of allocentric visual cues during route acquisition. In a second experimental series, fish were trained to use either visual or electrical landmarks for navigation and were subsequently tested in sensory transfer tests. Fish trained with visual landmarks were able to learn this allocentric navigation task and were capable of cross-modal landmark recognition, although navigation based on electrical landmarks was less efficient. The fish trained with electrical landmarks did not learn the task at all, suggesting that the short perceptual range of the electric sense prevented learning of allocentric navigation. Together our results show that the type of sensory input influences the efficiency of allocentric navigation in G. petersii and that these fish are able to use egocentric and allocentric strategies flexibly to navigate successfully under varying environmental conditions

Sensory influence on navigation in the weakly electric fish Gnathonemus petersii

Most animals possess multiple sensory systems, which can be used during navigation. Different senses obtain environmental information on different spatial scales and thus provide a different basis for efficient navigation. Here we used the weakly electric fish Gnathonemus petersii to investigate how different sensory inputs influence the navigational strategy and whether landmark information can be transferred flexibly between two sensory systems. Fish were trained to swim through a maze using a particular route indicated by either visual landmarks, electrical landmarks or without any landmarks. In subsequent tests, egocentric (internal cues, such as motion patterns) and allocentric cues (external cues like landmarks) were put in conflict by relocating the local landmarks. We found that all fish, independent of the available sensory input, chose the egocentric over the allocentric route. However, visual landmarks significantly improved the training duration compared to the other groups, suggesting an involvement of allocentric visual cues during route acquisition. In a second experimental series, fish were trained to use either visual or electrical landmarks for navigation and were subsequently tested in sensory transfer tests. Fish trained with visual landmarks were able to learn this allocentric navigation task and were capable of cross-modal landmark recognition, although navigation based on electrical landmarks was less efficient. The fish trained with electrical landmarks did not learn the task at all, suggesting that the short perceptual range of the electric sense prevented learning of allocentric navigation. Together our results show that the type of sensory input influences the efficiency of allocentric navigation in G. petersii and that these fish are able to use egocentric and allocentric strategies flexibly to navigate successfully under varying environmental conditions