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 in | Cognitive processing Vol. 13; no. Suppl 1; pp. 107 - 111 |
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Main Authors | , |
Format | Journal Article |
Language | English |
Published |
Berlin/Heidelberg
Springer-Verlag
01.08.2012
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Subjects | |
Online Access | Get full text |
ISSN | 1612-4782 1612-4790 1612-4790 |
DOI | 10.1007/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. |
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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 10.1016/j.anbehav.2009.03.021 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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Keywords | Fish Navigation Hydrostatic pressure Three-dimensional spatial cognition |
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References | GrobetyMCSchenkFSpatial-learning in a 3-dimensional mazeAnim Behav1992431011102010.1016/S0003-3472(06)80014-X UlanovskyNNeuroscience: how is three-dimensional space encoded in the brain?Curr Biol201121R886R8882207542710.1016/j.cub.2011.09.0311:CAS:528:DC%2BC3MXhsVKmurbM HaymanRVerriotisMAJovalekicAFentonAAJefferyKJAnisotropic encoding of three-dimensional space by place cells and grid cellsNat Neuro2011141182124410.1038/nn.28921:CAS:528:DC%2BC3MXpvVOkuro%3D HolbrookRIBurt de PereraTFish navigation in the vertical dimension: can fish use hydrostatic pressure to determine depth?Fish Fish20111237037910.1111/j.1467-2979.2010.00399.x TaylorGKHolbrookRIBurt de PereraTFractional rate of change of swim-bladder volume is reliably related to absolute depth during vertical displacements in teleost fishJ Roy Soc Interface201071379138210.1098/rsif.2009.0522 HolbrookRIBurt de PereraTSeparation of vertical and horizontal information simplifies the problem of navigating through a three-dimensional environment in fishAnim Behav20097824124510.1016/j.anbehav.2009.03.021 JovalekicAHaymanRBecaresNReidHThomasGWilsonJJefferyKHorizontal biases in rats’ use of three-dimensional spaceBehav Brain Res20112222792882141917210.1016/j.bbr.2011.02.035 BoneQMooreRHBiology of fishes20083AbingdonTaylor & Francis Group HolbrookRIBurt de PereraTThree-dimensional spatial cognition: information in the vertical dimension overrides information from the horizontalAnim Cogn2011146136192145204810.1007/s10071-011-0393-6 RI Holbrook (473_CR8) 2011; 14 R Hayman (473_CR6) 2011; 14 RI Holbrook (473_CR7) 2009; 78 Q Bone (473_CR1) 2008 MC Grobety (473_CR5) 1992; 43 RI Holbrook (473_CR9) 2011; 12 A Jovalekic (473_CR10) 2011; 222 GK Taylor (473_CR11) 2010; 7 N Ulanovsky (473_CR12) 2011; 21 21419172 - Behav Brain Res. 2011 Sep 23;222(2):279-88 21822271 - Nat Neurosci. 2011 Aug 07;14(9):1182-8 20190038 - J R Soc Interface. 2010 Sep 6;7(50):1379-82 22075427 - Curr Biol. 2011 Nov 8;21(21):R886-8 21452048 - Anim Cogn. 2011 Jul;14(4):613-9 |
References_xml | – reference: BoneQMooreRHBiology of fishes20083AbingdonTaylor & Francis Group – reference: HolbrookRIBurt de PereraTThree-dimensional spatial cognition: information in the vertical dimension overrides information from the horizontalAnim Cogn2011146136192145204810.1007/s10071-011-0393-6 – reference: UlanovskyNNeuroscience: how is three-dimensional space encoded in the brain?Curr Biol201121R886R8882207542710.1016/j.cub.2011.09.0311:CAS:528:DC%2BC3MXhsVKmurbM – reference: GrobetyMCSchenkFSpatial-learning in a 3-dimensional mazeAnim Behav1992431011102010.1016/S0003-3472(06)80014-X – reference: HaymanRVerriotisMAJovalekicAFentonAAJefferyKJAnisotropic encoding of three-dimensional space by place cells and grid cellsNat Neuro2011141182124410.1038/nn.28921:CAS:528:DC%2BC3MXpvVOkuro%3D – reference: HolbrookRIBurt de PereraTSeparation of vertical and horizontal information simplifies the problem of navigating through a three-dimensional environment in fishAnim Behav20097824124510.1016/j.anbehav.2009.03.021 – reference: HolbrookRIBurt de PereraTFish navigation in the vertical dimension: can fish use hydrostatic pressure to determine depth?Fish Fish20111237037910.1111/j.1467-2979.2010.00399.x – reference: JovalekicAHaymanRBecaresNReidHThomasGWilsonJJefferyKHorizontal biases in rats’ use of three-dimensional spaceBehav Brain Res20112222792882141917210.1016/j.bbr.2011.02.035 – reference: TaylorGKHolbrookRIBurt de PereraTFractional rate of change of swim-bladder volume is reliably related to absolute depth during vertical displacements in teleost fishJ Roy Soc Interface201071379138210.1098/rsif.2009.0522 – volume: 7 start-page: 1379 year: 2010 ident: 473_CR11 publication-title: J Roy Soc Interface doi: 10.1098/rsif.2009.0522 – volume: 222 start-page: 279 year: 2011 ident: 473_CR10 publication-title: Behav Brain Res doi: 10.1016/j.bbr.2011.02.035 – volume-title: Biology of fishes year: 2008 ident: 473_CR1 doi: 10.1201/9781134186310 – volume: 43 start-page: 1011 year: 1992 ident: 473_CR5 publication-title: Anim Behav doi: 10.1016/S0003-3472(06)80014-X – volume: 78 start-page: 241 year: 2009 ident: 473_CR7 publication-title: Anim Behav doi: 10.1016/j.anbehav.2009.03.021 – volume: 14 start-page: 1182 year: 2011 ident: 473_CR6 publication-title: Nat Neuro doi: 10.1038/nn.2892 – volume: 14 start-page: 613 year: 2011 ident: 473_CR8 publication-title: Anim Cogn doi: 10.1007/s10071-011-0393-6 – volume: 21 start-page: R886 year: 2011 ident: 473_CR12 publication-title: Curr Biol doi: 10.1016/j.cub.2011.09.031 – volume: 12 start-page: 370 year: 2011 ident: 473_CR9 publication-title: Fish Fish doi: 10.1111/j.1467-2979.2010.00399.x – reference: 21822271 - Nat Neurosci. 2011 Aug 07;14(9):1182-8 – reference: 20190038 - J R Soc Interface. 2010 Sep 6;7(50):1379-82 – reference: 22075427 - Curr Biol. 2011 Nov 8;21(21):R886-8 – reference: 21419172 - Behav Brain Res. 2011 Sep 23;222(2):279-88 – reference: 21452048 - Anim Cogn. 2011 Jul;14(4):613-9 |
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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 |
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