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 acc...

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Published inCognitive processing Vol. 13; no. Suppl 1; pp. 107 - 111
Main Authors Burt de Perera, Theresa, Holbrook, Robert I.
Format Journal Article
LanguageEnglish
Published Berlin/Heidelberg Springer-Verlag 01.08.2012
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ISSN1612-4782
1612-4790
1612-4790
DOI10.1007/s10339-012-0473-9

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Abstract 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.
AbstractList 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.
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.
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.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.
Author Holbrook, Robert I.
Burt de Perera, Theresa
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Cites_doi 10.1098/rsif.2009.0522
10.1016/j.bbr.2011.02.035
10.1201/9781134186310
10.1016/S0003-3472(06)80014-X
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10.1038/nn.2892
10.1007/s10071-011-0393-6
10.1016/j.cub.2011.09.031
10.1111/j.1467-2979.2010.00399.x
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Snippet Research on spatial cognition has focused on how animals encode the horizontal component of space. However, most animals travel vertically within their...
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SubjectTerms Animals
Artificial Intelligence
Astyanax
Astyanax fasciatus
Behavioral Sciences
Biomedical and Life Sciences
Biomedicine
Fishes - physiology
Hydrostatic Pressure
Maze Learning
Neurosciences
Orientation - physiology
Short Report
Space Perception - physiology
Spatial Behavior - physiology
Swimming
Title Three-dimensional spatial representation in freely swimming fish
URI https://link.springer.com/article/10.1007/s10339-012-0473-9
https://www.ncbi.nlm.nih.gov/pubmed/22915259
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