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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.

Weakly electric fish emit electric signals with an electric organ in their tail and perceive them with cutaneous electroreceptor organs. During active electrolocation, objects are detected and analyzed because they distort the self-produced electrical field and project electric images onto the electroreceptive skin surface. To optimize electrical imaging of the environment, the fish perform certain electromotor and locomotor behaviors (probing motor acts). For fine spatial analysis, the mormyrid Gnathonemus petersii focuses electric images of objects onto two ‘foveal’ skin regions: the ‘Schnauzenorgan’ and the ‘nasal region.’ Sudden emergences of novel stimuli evoke the so-called novelty responses (electromotor) and Schnauzenorgan responses (movements of the chin).

Publisher Summary Many groups of fishes perceive naturally occurring electric stimuli. They possess ampullary electroreceptor organs that respond to low‐frequency electric fields. Two nocturnally active teleost groups produce weak electric signals (electric organ discharges, EOD), which they perceive with tuberous electroreceptor organs. In addition to “passive electrolocation,” these weakly electric fish perform “active electrolocation,” during which they detect alterations of their EOD caused by nearby objects. This enables them to perceive the complex impedance of objects and thus to identify animated objects. In addition, they can measure distance, size, shape, and other 3D object properties. When inspecting an object, the weakly electric fish Gnathonemus petersii employs two “electrical foveae" that are located on their moveable chin appendage and in the nasal region. The former is used for object inspection, while the latter is used for object detection during foraging. The brain of weakly electric fishes extracts information about objects by analyzing the input from the electroreceptor organs. The study of electroreceptive brain areas has revealed many general principals of neural processing of sensory and motor information.

SUMMARY 1. The Medullary Command Nucleus (MCN) in the four weakly electric fish families, Gymnarchidae, Gymnotidae, Electrophoridae and Mormyridae (in one species of each family) was investigated by means of spinal HRP injections. In the four species examined, Gymnarchus niloticus , Hypopomus sp ., Electrophorus electricus , Gnathonemus petersii , only the large (relay) cells of the MCN send their axons into the spinal cord. Comparing wave ( G.niloticus ) and pulse species ( Hypopomus sp ., E. electricus ), the former shows more MCN axons reaching more caudal spinal levels than the latter. In contrast to gymnotoids and G. niloticus , where the electromotoneurons are distributed all along the spinal cord, the electromotoneurons in mormyrids make up a compact pool at the level of the caudal peduncle; all large cells of the MCN reach this region of the spinal cord. 2. In E. electricus the EMN and motoneurons (MN) were identified in the spinal cord by injection of HRP into the different electric organs and into the muscle. EMN have a spinal location distinct from that of MN and are somatotopically organised within the spinal cord in respect to the different electric organs.

SUMMARY Series of electric organ discharges of Gnathonemus petersii were recorded by means of a pair of symmetrical electrode assemblies on each side of the fish. The spontaneous EODs in the stationary phase were differentiated (into two groups) according to amplitude variations; the left-dominant and the right-dominant groups. It is concluded that the electric organs are discharging alternately with a monomodal interval distribution on each side. A small distance between bilateral electric organs which would produce temporal EOD slipping-off is far more effective for detection of the electric field disturbances.