Sarah Schumacher’s research while affiliated with University of Bonn and other places

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 certain 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 can use egocentric and allocentric strategies flexibly to navigate successfully under varying environmental conditions.

Animal multisensory systems are able to cope with discrepancies in information provided by individual senses by integrating information using a weighted average of the sensory inputs. Such sensory weighting often leads to a dominance of a certain sense during particular tasks and conditions, also called sensory capture. Here we investigated the interaction of vision and active electrolocation during object discrimination in the weakly electric fish Gnathonemus petersii. Fish were trained to discriminate between two objects using both senses and were subsequently tested using either only vision or only the active electric sense. We found that at short range the electric sense dominates over vision, leading to a decreased ability to discriminate between objects visually when vision and electrolocation provide conflicting information. In line with visual capture in humans, we call this dominance of the electric sense electrosensory capture. Further, our results suggest that the fish are able to exploit the advantages of multiple senses using vision and electrolocation redundantly, synergistically and complementarily. Together our results show that by providing similar information about the environment on different spatial scales, vision and the electric sense of G. petersii are well attuned to each other producing a robust and flexible percept.

The weakly electric fish Gnathonemus petersii can recognise objects using active electrolocation. Here, we tested two aspects of object recognition; first whether shape recognition might be influenced by movement of the fish, and second whether object discrimination is affected by the presence of electrical noise from conspecifics. (i) Unlike other object features, such as size or volume, no parameter within a single electrical image has been found that encodes object shape. We investigated whether shape recognition might be facilitated by movement-induced modulations (MIM) of the set of electrical images that are created as a fish swims past an object. Fish were trained to discriminate between pairs of objects that either created similar or dissimilar levels of MIM of the electrical images. As predicted, the fish were able to discriminate between objects up to a longer distance if there was a large difference in MIM between the objects than if there was a small difference. This supports an involvement of MIMs in shape recognition but the use of other cues cannot be excluded. (ii) Electrical noise might impair object recognition if the noise signals overlap with the EODs of an electrolocating fish. To avoid jamming, we predicted that fish might employ pulsing strategies to prevent overlaps. To investigate the influence of electrical noise on discrimination performance, two fish were tested either in the presence of a conspecific or of playback signals and the electric signals were recorded during the experiments. The fish were surprisingly immune to jamming by conspecifics: While the discrimination performance of one fish dropped to chance level when more than 22% of its EODs overlapped with the noise signals, the performance of the other fish was not impaired even when all its EODs overlapped. Neither of the fish changed their pulsing behaviour, suggesting that they did not use any kind of jamming avoidance strategy.

Significance Being able to spontaneously recognize objects across different senses increases the flexibility of a multisensory system, because the reliability of different sensory inputs depends on the environment and range. However, this ability has only been found in mammals, suggesting such a high-level function might be associated with complex mammalian brain structures. We show that the weakly electric fish Gnathonemus petersii , is also capable of spontaneous cross-modal object recognition, discriminating objects learned visually with the active electric sense and vice versa. Furthermore, the modality-specific inputs are weighted dynamically according to their reliability at different ranges. This finding suggests that these complex cognitive abilities are present in fish in addition to mammals, and therefore do not require a cerebral cortex.

The way animals move through space is likely to affect the way they learn and remember spatial information. For example, a pelagic fish, Astyanax fasciatus, moves freely in vertical and horizontal space and encodes information from both dimensions with similar accuracy. Benthic fish can also move with six degrees of freedom, but spend much of their time travelling over the substrate; hence they might be expected to prioritise the horizontal dimension. To understand how benthic fish encode and deploy three-dimensional spatial information we used a fully rotational Y-maze to test whether Corydoras aeneus (i) encode space as an integrated three-dimensional unit or as separate elements, by testing whether they can decompose a three-dimensional trajectory into its vertical and horizontal components, and (ii) whether they prioritise vertical or horizontal information when the two conflict. In contradiction to the expectation generated by our hypothesis, our results suggest that C. aeneus are better at extracting vertical information than horizontal information from a three-dimensional trajectory, suggesting that the vertical axis is learned and remembered robustly. Our results also showed that the fish prioritise vertical information when it conflicts with horizontal information. From these results, we infer that benthic fish attend preferentially to a cue unique to the vertical axis, and we suggest that this cue is hydrostatic pressure.

Seeing in the Dark Elephantnose fish are known to use electrosensing to navigate their murky freshwater environment. However, unlike some other animals from dark environments, they have retained their eyes and some dependence on vision. While most vertebrate vision optimizes either photon catch (for increased light capture) or visual acuity, Kreysing et al. (p. 1700 ) show that the unique structures of the grouped retinae found in the eyes of this species matches rod and cone sensitivity, which allows for the simultaneous use of both types of photoreceptors over a large range of dim light intensities.

Gnathonemus petersii is a weakly electric fish, which orients in its environment by detecting changes in a self generated electric field caused by objects. They generate electric signals with an electric organ located in the tail and perceive the resulting electric images with epidermal electroreceptors. During electrolocation G. petersii is able to discriminate between two objects up to a distance of about 4 cm, as shown by previous experiments. In this project we tested whether interfering electric signals from a conspecific influence the effectiveness of object discrimination. Fish were trained to discriminate between two objects in a food-rewarded two-alternative forced-choice procedure while a second fish was present or when a computer generated playback signal was presented. We tested whether the discrimination performance changed under these conditions at object distances of 1 and 3 cm. In addition, we recorded the electric signals of the fish during these experiments and tested whether G. petersii has a certain strategy to avoid jamming by signals from another fish. Our results show that there is no longterm degradation of the performance when a second fish is present. The experiments with playback signals showed no consistent results: The discrimination performance of one fish deteriorated at playback frequencies greater than200 Hz, while another one was not effected even at frequencies of 1.5 kHz. Regarding the recordings of the electrical signals there is no obvious jamming avoidance strategy. The results show that G. petersii is able to discriminate objects in presents of conspecifics without a decrease of effectiveness.