Session B8: The Representation of Three-Dimensional Space in Fish

Abstract: To navigate around their local environment, animals must recognise their own position with respect to their goal. This task can be completed successfully if they have a representation of space in their brain, built upon learning and remembering environmental features. This representation can be thought of as a neural map. Previous research has focused on how animals navigate horizontally, however most must also move vertically. This is exemplified by flying or swimming animals, which move with six degrees of freedom (unlike surface constrained animals that move with three). By using behavioural experimental and theoretical approaches, we study both the sensory basis of 3D navigation in fish and also how the information gained from the environment is learned and remembered. We show that the vertical and horizontal components of space are stored separately in the fishes’ representation of space, which simplifies the problem of encoding complex information in the brain, and that the vertical axis contains particularly salient spatial cues, including hydrostatic pressure. We also demonstrate that fish that swim freely through a volume of water are able to accurately learn and remember 3D metric information – that is, distance and direction. Our work suggests that the spatial information obtained by a fish’s sensory systems is pulled together into a supramodal representation of space that is similar to the place cells in the hippocampus of mammals. We also suggest the putative neurones that encode space in fish fire with a spherical distribution, allowing the animals to navigate effectively in three-dimensions

Separate encoding of vertical and horizontal components of space during orientation in fish

The ability to orient through familiar areas is key to the success of many animal groups. To date, research has focused on how animals orient horizontally and very little work has considered three-dimensional environments, particularly the volumetric surroundings inhabited by many birds, flying insects and fish. These animals do not have their movement constrained by surfaces, and can move with three degrees of freedom. This extra freedom of movement increases the amount of navigational information potentially available, which could lead to an information-processing problem. We studied how a fish, the sighted banded tetra, Astyanax fasciatus, copes with this problem by testing how it learns and stores information from its volumetric surroundings. Using a novel assay based on associative learning of the vertical (up/down) and horizontal (left/right) components of a rotating Y-maze, we found that banded tetras learned and remembered information from the vertical and horizontal components when they were presented either separately or as an integrated three-dimensional unit. Furthermore, when information from the two components conflicted, the fish used the previously learned vertical information in preference to the horizontal, possibly because the vertical axis contained an extra, global, cue: hydrostatic pressure. We propose that animals that navigate through volumes may simplify the information storage problem by encoding the horizontal and vertical components separately. These components could then be used togther for rapid, efficient orientation

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

GPS csv files for tracks of all birds

The data is saved in the formate 01_"flock number"_"bird ID"_"release". For example, 01_08_S01_12 is flock 8, bird S01 and release 12. The data are in CSV files with all columns named. There are 8 flocks with 5 birds

Visual odometry of Rhinecanthus aculeatus depends on the visual density of the environment

Distance travelled is a crucial metric that underpins an animal’s ability to navigate in the short-range. While there is extensive research on how terrestrial animals measure travel distance, it is unknown how animals navigating in aquatic environments estimate this metric. A common method used by land animals is to measure optic flow, where the speed of self-induced visual motion is integrated over the course of a journey. Whether freely-swimming aquatic animals also measure distance relative to a visual frame of reference is unclear. Using the marine fish Rhinecanthus aculeatus, we show that teleost fish can use visual motion information to estimate distance travelled. However, the underlying mechanism differs fundamentally from previously studied terrestrial animals. Humans and terrestrial invertebrates measure the total angular motion of visual features for odometry, a mechanism which does not vary with visual density. In contrast, the visual odometer used by Rhinecanthus acuelatus is strongly dependent on the visual density of the environment. Odometry in fish may therefore be mediated by a movement detection mechanism akin to the system underlying the optomotor response, a separate motion-detection mechanism used by both vertebrates and invertebrates for course and gaze stabilisation

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

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

Data from: 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

Visual odometry of Rhinecanthus aculeatus depends on the visual density of the environment.

Funder: Oxford University | St. John's College, University of OxfordFunder: RCUK | Biotechnology and Biological Sciences Research CouncilDistance travelled is a crucial metric that underpins an animal's ability to navigate in the short-range. While there is extensive research on how terrestrial animals measure travel distance, it is unknown how animals navigating in aquatic environments estimate this metric. A common method used by land animals is to measure optic flow, where the speed of self-induced visual motion is integrated over the course of a journey. Whether freely-swimming aquatic animals also measure distance relative to a visual frame of reference is unclear. Using the marine fish Rhinecanthus aculeatus, we show that teleost fish can use visual motion information to estimate distance travelled. However, the underlying mechanism differs fundamentally from previously studied terrestrial animals. Humans and terrestrial invertebrates measure the total angular motion of visual features for odometry, a mechanism which does not vary with visual density. In contrast, the visual odometer used by Rhinecanthus acuelatus is strongly dependent on the visual density of the environment. Odometry in fish may therefore be mediated by a movement detection mechanism akin to the system underlying the optomotor response, a separate motion-detection mechanism used by both vertebrates and invertebrates for course and gaze stabilisation

Weakly electric fish use self-generated motion to discriminate object shape

Body movements are known to play an active role in sensing. However, it is not fully understood what information is provided by these movements. The Peter’s elephantnose fish, Gnathonemus petersii sense their environment through active electrolocation during which they use epidermal electroreceptors to perceive object-induced distortions of a self-produced electric field. The analysis of electric images projected on their skin enables them to discriminate between three-dimensional objects. While we know the electric image parameters used to encode numerous object properties, we don’t understand how these images encode object shape. We hypothesise that ‘movement-induced modulations’ (MIMs) evoked by body movements might be involved in shape discrimination during active electrolocation. To test this, we trained fish to complete a shape discrimination task in a two-alternative forced-choice setup, and then manipulated the space available to individuals for scanning movements to see if this led to a change in their discrimination performance. We found that if enough space was available, fish were very good at discriminating objects of different shapes. However, performance decreased when the space was reduced so that scanning movements were impaired. Our study demonstrates the importance of body movements for gaining complex environmental information such as object shape through active electrolocation. Movement can enhance perception by allowing the extraction of certain kinds of information. Similar observations have been made in other animals using different senses, suggesting that the core principles of sensory-motor integration might be valid for various sensory modalities