Original Research PaperWeakly electric fish learn both visual and electrosensory cues in a multisensory object discrimination task
Introduction
Most animals have more than a single sensory system and usually salient objects stimulate more than a single sensory modality. The information provided by the different sensory modalities about the object may be integrated to successfully and robustly guide behavior. Indeed, in the context of foraging, for example, information provided by several senses is combined to improve the system’s overall performance (e.g. in barn owl, bat, or fish; Knudsen and Knudsen, 1989, Boonman et al., 2013, von der Emde and Bleckmann, 1998, respectively). Multimodal integration has often been found to be in line with Bayesian optimality, i.e. a weighted combination of the individual modalities in which the weight is proportional to the reliability of the respective senses (e.g. Knill and Pouget, 2004, Ernst and Bülthoff, 2004, Angelaki et al., 2009).
In addition to the visual, olfactory, and mechanosensory senses weakly electric fish possess an electric sense (for review, e.g. Bullock and Heiligenberg, 1986). The electrosensory system is divided into two subsystems, namely the active and the passive system. The passive, or ampullary, electrosensory system is phylogenetically ancient and ampullary electroreceptors respond to low-frequency electric fields as evoked for example by muscle activity of other animate objects in the surrounding (e.g. Kalmijn, 1974). The active, tuberous, system, on the other hand, is tuned to higher frequencies such as the fish’s self-generated electric field. With the active electrosense fish sense distortions of their own field that are caused by nearby objects during navigation and prey-detection (e.g Bastian, 1981, Nelson and MacIver, 1999) or originating from interference with electric fields of other electric fish and electrocommunication signals (e.g. Benda et al., 2013).
During foraging weakly electric fish use all their senses depending on availability (von der Emde and Bleckmann, 1998, Nelson and MacIver, 1999, for Gnathonemus petersii and Apteronotus albifrons, respectively). During shelter tracking behavior, i.e. maintenance of a position within a moving shelter, in both the mormyrid G. petersii and the gymnotiform Eigenmannia virescens combining visual and electrosensory information enhances behavioral performance (Moller, 2002, Stamper et al., 2012, Sutton et al., 2016; see also Schumacher et al., 2016).
Cognitive abilities of weakly electric fish such as object recognition and discrimination have been studied mainly in the African weakly electric fish, in particular in G. petersii. These fish can be trained to distinguish objects of different conductive or capacitive properties (von der Emde and Ringer, 1992, von der Emde and Ronacher, 1994) or to distinguish and recognize spatial properties of objects with their electric sense (von der Emde and Schwarz, 2000, Graff et al., 2004). The electric sense enables these fish to occupy a particular niche characterized by low-visibility and nocturnal activity. However, they still use all their senses whenever other sensory information is available (e.g. von der Emde and Bleckmann, 1998, Moller, 2002, Walton and Moller, 2010). The South American weakly electric fish are an established model system for the encoding of sensory information and studies on electrocommunication (e.g. Benda et al., 2013, Krahe and Maler, 2014, Chacron et al., 2011). However, relatively little is known about the cognitive abilities of the South American weakly electric fish (Jun et al., 2014, Jun et al., 2016).
Here we investigate the importance of visual and electrosensory information in an object discrimination task in the South American weakly electric fish A. albifrons. Even though the eyes of A. albifrons are small compared to other fish (Sas and Maler, 1986), have a rather low density of retinal ganglion cells and relatively poor spatial resolution (Takiyama et al., 2015), visual motion information affects the encoding of moving electrosensory stimuli (Bastian, 1982). In this study we conditioned fish to discriminate objects that carried unique combinations of electrosensory as well as visual cues. By setting both cues in conflict, we assessed the sensory hierarchy of visual and electrosensory information. Our results show that A. albifrons can be trained to this type of object-recognition task and that in all tested animals the electrosense dominates over the visual sense. However, they are still able to use visual information if electrosensory cues are not available. We can further show that fish not only learn the rewarded stimulus combination but also learn the non-rewarded combination.
Section snippets
Methods
In this study four adult individuals of the black ghost knifefish Apteronotus albifrons were conditioned in a discrimination task. Fish were obtained from a commercial fish dealer (Aquarium Glaser, Rodgau, Germany) and were kept in groups of 3 fish per tank. Animals were kept in a 12 h:12 h day – night cycle, water temperatures were 26–27 °C and water conductivity was adjusted to 180–200 μS cm−1. All experimental protocols complied with national and European law and were approved by the Ethics
Fish can be trained to the discrimination task
Four fish were trained to perform a discrimination task in which two objects were presented. Objects were cubes of either graphite or aluminum that were covered with cotton hoods. The cloth was either white or dyed black. The objects were thus characterized by the combination of electrosensory and visual information. Fish were trained to expect a food reward at the object that carried a certain combination of electrosensory and visual cues (Table 1). Fish signaled a decision by staying close to
Discussion
Individuals of Apteronotus albifrons can be conditioned to reliably solve an object discrimination task that involves combinations of electrosensory and visual cues. Targeted manipulations of the objects were used to test for the hierarchy of the involved senses and the fish’s ability to memorize object characteristics.
Acknowledgments
Anatolie Ender and Florian Sälzle helped establishing the conditioning protocols. Eileen Winkel performed several control experiments. We thank Delwen Franzen for comments on the manuscript.
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