Taking a shortcut: what mechanisms do fish use?

Path integration is a powerful navigational mechanism whereby individuals continuously update their distance and angular vector of movement to calculate their position in relation to their departure location, allowing them to return along the most direct route even across unfamiliar terrain. While path integration has been investigated in several terrestrial animals, it has never been demonstrated in aquatic vertebrates, where movement occurs through volumetric space and sensory cues available for navigation are likely to differ substantially from those in terrestrial environments. By performing displacement experiments with Lamprologus ocellatus, we show evidence consistent with fish using path integration to navigate alongside other mechanisms (allothetic place cues and route recapitulation). These results indicate that the use of path integration is likely to be deeply rooted within the vertebrate phylogeny irrespective of the environment, and suggests that fish may possess a spatial encoding system that parallels that of mammals.

Vision in the Vertical Axis: How Important Are Visual Cues in Foraging and Navigation?

In both terrestrial and aquatic environments, a large number of animal behaviors rely on visual cues, with vision acting as the dominant sense for many fish. However, many other streams of information are available, and multiple cues may be incorporated simultaneously. Being free from the constraints of many of their terrestrial counterparts, fish have an expanded range of possible movements typified by a volume rather than an area. Cues such as hydrostatic pressure, which relates to navigation in a vertical plane, may provide more salient and reliable information to fish as they are not affected by poor light conditions or turbidity. Here, we tested banded tetra fish (Astyanax fasciatus) in a simple foraging task in order to determine whether visual cues would be prioritized over other salient information, most notably hydrostatic pressure gradients. We found that in both vertical and horizontal arrays there was no evidence for fish favoring one set of cues over the other, with subjects making choices at random once cues were placed into conflict. Visual cues remained as important in the vertical axis as they were in the horizontal axis.

Distance estimation in the goldfish (Carassius auratus).

Neurophysiological advances have given us exciting insights into the systems responsible for spatial mapping in mammals. However, we are still lacking information on the evolution of these systems and whether the underlying mechanisms identified are universal across phyla, or specific to the species studied. Here we address these questions by exploring whether a species that is evolutionarily distant from mammals can perform a task central to mammalian spatial mapping-distance estimation. We developed a behavioural paradigm allowing us to test whether goldfish (Carassius auratus) can estimate distance and explored the behavioural mechanisms that underpin this ability. Fish were trained to swim a set distance within a narrow tank covered with a striped pattern. After changing the background pattern, we found that goldfish use the spatial frequency of their visual environment to estimate distance, doubling the spatial frequency of the background pattern resulted in a large overestimation of the swimming distance. We present robust evidence that goldfish can accurately estimate distance and show that they use local optic flow to do so. These results provide a compelling basis to use goldfish as a model system to interrogate the evolution of the mechanisms that underpin spatial cognition, from brain to behaviour.

Electrosensory capture during multisensory discrimination of nearby objects in the weakly electric fish Gnathonemus petersii.

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.

Validating two-dimensional leadership models on three-dimensionally structured fish schools.

Identifying leader-follower interactions is crucial for understanding how a group decides where or when to move, and how this information is transferred between members. Although many animal groups have a three-dimensional structure, previous studies investigating leader-follower interactions have often ignored vertical information. This raises the question of whether commonly used two-dimensional leader-follower analyses can be used justifiably on groups that interact in three dimensions. To address this, we quantified the individual movements of banded tetra fish (Astyanax mexicanus) within shoals by computing the three-dimensional trajectories of all individuals using a stereo-camera technique. We used these data firstly to identify and compare leader-follower interactions in two and three dimensions, and secondly to analyse leadership with respect to an individual's spatial position in three dimensions. We show that for 95% of all pairwise interactions leadership identified through two-dimensional analysis matches that identified through three-dimensional analysis, and we reveal that fish attend to the same shoalmates for vertical information as they do for horizontal information. Our results therefore highlight that three-dimensional analyses are not always required to identify leader-follower relationships in species that move freely in three dimensions. We discuss our results in terms of the importance of taking species' sensory capacities into account when studying interaction networks within groups.

Object discrimination through active electrolocation: Shape recognition and the influence of electrical noise.

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.

Misinformed leaders lose influence over pigeon flocks.

In animal groups where certain individuals have disproportionate influence over collective decisions, the whole group's performance may suffer if these individuals possess inaccurate information. Whether in such situations leaders can be replaced in their roles by better-informed group mates represents an important question in understanding the adaptive consequences of collective decision-making. Here, we use a clock-shifting procedure to predictably manipulate the directional error in navigational information possessed by established leaders within hierarchically structured flocks of homing pigeons (Columba livia). We demonstrate that in the majority of cases when leaders hold inaccurate information they lose their influence over the flock. In these cases, inaccurate information is filtered out through the rearrangement of hierarchical positions, preventing errors by former leaders from propagating down the hierarchy. Our study demonstrates that flexible decision-making structures can be valuable in situations where 'bad' information is introduced by otherwise influential individuals.

Cross-modal object recognition and dynamic weighting of sensory inputs in a fish.

Most animals use multiple sensory modalities to obtain information about objects in their environment. There is a clear adaptive advantage to being able to recognize objects cross-modally and spontaneously (without prior training with the sense being tested) as this increases the flexibility of a multisensory system, allowing an animal to perceive its world more accurately and react to environmental changes more rapidly. So far, spontaneous cross-modal object recognition has only been shown in a few mammalian species, raising the question as to whether such a high-level function may be associated with complex mammalian brain structures, and therefore absent in animals lacking a cerebral cortex. Here we use an object-discrimination paradigm based on operant conditioning to show, for the first time to our knowledge, that a nonmammalian vertebrate, the weakly electric fish Gnathonemus petersii, is capable of performing spontaneous cross-modal object recognition and that the sensory inputs are weighted dynamically during this task. We found that fish trained to discriminate between two objects with either vision or the active electric sense, were subsequently able to accomplish the task using only the untrained sense. Furthermore we show that cross-modal object recognition is influenced by a dynamic weighting of the sensory inputs. The fish weight object-related sensory inputs according to their reliability, to minimize uncertainty and to enable an optimal integration of the senses. Our results show that spontaneous cross-modal object recognition and dynamic weighting of sensory inputs are present in a nonmammalian vertebrate.

The Representation of Three-Dimensional Space in Fish.

In mammals, the so-called "seat of the cognitive map" is located in place cells within the hippocampus. Recent work suggests that the shape of place cell fields might be defined by the animals' natural movement; in rats the fields appear to be laterally compressed (meaning that the spatial map of the animal is more highly resolved in the horizontal dimensions than in the vertical), whereas the place cell fields of bats are statistically spherical (which should result in a spatial map that is equally resolved in all three dimensions). It follows that navigational error should be equal in the horizontal and vertical dimensions in animals that travel freely through volumes, whereas in surface-bound animals would demonstrate greater vertical error. Here, we describe behavioral experiments on pelagic fish in which we investigated the way that fish encode three-dimensional space and we make inferences about the underlying processing. Our work suggests that fish, like mammals, have a higher order representation of space that assembles incoming sensory information into a neural unit that can be used to determine position and heading in three-dimensions. Further, our results are consistent with this representation being encoded isotropically, as would be expected for animals that move freely through volumes. Definitive evidence for spherical place fields in fish will not only reveal the neural correlates of space to be a deep seated vertebrate trait, but will also help address the questions of the degree to which environment spatial ecology has shaped cognitive processes and their underlying neural mechanisms.

Navigating in a volumetric world: metric encoding in the vertical axis of space.

Animals navigate through three-dimensional environments, but we argue that the way they encode three-dimensional spatial information is shaped by how they use the vertical component of space. We agree with Jeffery et al. that the representation of three-dimensional space in vertebrates is probably bicoded (with separation of the plane of locomotion and its orthogonal axis), but we believe that their suggestion that the vertical axis is stored "contextually" (that is, not containing distance or direction metrics usable for novel computations) is unlikely, and as yet unsupported. We describe potential experimental protocols that could clarify these differences in opinion empirically.

Three-dimensional spatial representation in freely swimming fish.

Research on spatial cognition has focused on how animals encode the horizontal component of space. However, most animals travel vertically within their environments, particularly those that fly or swim. Pelagic fish move with six degrees of freedom and must integrate these components to navigate accurately--how do they do this? Using an assay based on associative learning of the vertical and horizontal components of space within a rotating Y-maze, we found that fish (Astyanax fasciatus) learned and remembered information from both horizontal and vertical axes when they were presented either separately or as an integrated three-dimensional unit. When information from the two components conflicted, the fish used the previously learned vertical information in preference to the horizontal. This not only demonstrates that the horizontal and vertical components are stored separately in the fishes' representation of space (simplifying the problem of 3D navigation), but also suggests that the vertical axis contains particularly salient spatial cues--presumably including hydrostatic pressure. To explore this latter possibility, we developed a physical theoretical model that shows how fish could determine their absolute depth using pressure. We next considered full volumetric spatial cognition. Astyanax were trained to swim towards a reward in a Y-maze that could be rotated, before the arms were removed during probe trials. The subjects were tracked in three dimensions as they swam freely through the surrounding cubic tank. The results revealed that fish are able to accurately encode metric information in a volume, and that the error accrued in the horizontal and vertical axes whilst swimming in probe trials was similar. Together, these experiments demonstrate that unlike in surface-bound rats, the vertical component of the representation of space is vitally important to fishes. We hypothesise that the representation of space in the brain of vertebrates could ultimately be shaped by the number of the degrees of freedom of movement that binds the navigating animal.

Three-dimensional spatial cognition: information in the vertical dimension overrides information from the horizontal.

Fish live in three-dimensional environments, through which they swim with three translational and three rotational degrees of freedom. Navigating through such environments is recognised as a difficult problem, yet fish, and other animals that swim and fly, achieve this regularly. Despite this, the vast majority of research has considered how animals navigate horizontally from place to place and has ignored the vertical component. Here, we test the importance of the vertical axis of space for fish solving a three-dimensional spatial cognition task. We trained banded tetras (Astyanax fasciatus) to learn the route towards a goal in a rotating Y-maze in which the arms led either up and left or down and right in an environment that allowed access to visual landmarks providing horizontal and vertical information. Our results revealed that the landmarks increased navigational efficiency during training. However, these landmarks were ignored when the horizontal and vertical components were placed in conflict with each other by rotating the maze 90° during testing. From this surprising result, we conclude that the cues that are present in the vertical axis (presumably hydrostatic pressure) override landmark cues that have been shown to be salient in experiments that only consider the horizontal component of space.

The function of wall-following behaviors in the Mexican blind cavefish and a sighted relative, the Mexican tetra (Astyanax).

Mexican blind cavefish exhibit an unconditioned wall-following behavior in response to novel environments. Similar behaviors have been observed in a wide variety of animals, but the biological significance and evolutionary history of this behavior are largely unknown. In this study, the behaviors of Mexican blind cavefish (Astyanax sp.) and sighted Mexican tetra (Astyanax mexicanus) were videotaped after fish were introduced into a novel environment under dark (infrared) or well-lit conditions. Under dark conditions, both sighted and blind morphs exhibited wall-following behaviors with subtle but significant differences. Blind morphs swam more nearly parallel to the wall, exhibited greater wall-following continuity and reached higher levels of sustained swimming speeds more quickly than sighted morphs. In contrast, sighted morphs in the light remained motionless near the wall for long periods of time or moved slowly around the center of the tank without entraining to the walls. These results are consistent with the idea that wall-following is a shared, primitive trait that serves an exploratory function under dark conditions to compensate for the absence of vision. This behavior has become more honed in blind morphs for exploratory purposes--in large part due to the enhanced, active-flow sensing abilities of the lateral line.

Fish can encode order in their spatial map.

Animals must often orient through areas that are larger than their perceptual range. The blind Mexican cave fish, Astyanax fasciatus, depends on detecting self-induced near-field wave perturbations by objects via the use of its lateral line organ. Its perceptual range (less than or equal to 0.05 m) is greatly exceeded by its ecological ranging requirements (ca. 30 m). Although known to possess a spatial map of its environment, it is not known how this fish links places (or the area over which the perceptual range extends) together. Using the blind cave fish's propensity to accelerate when faced with objects or environments that are recognizably different, I used a behavioural assay to test whether fishes can learn and remember the order of a landmark sequence. I show, to my knowledge for the first time, that blind Mexican cave fish can encode order in their spatial map. The ability to represent the order in which a series of places are spatially linked is a powerful tool for animals that must orient beyond the limit of their perceptual range. The resulting spatial map would be analogous to a jigsaw puzzle, where each piece represents a place whose size is constrained by the animal's perceptual range.