Representation of edges, head direction, and swimming kinematics in the brain of freely-navigating fish.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
08 09 2020
Historique:
received: 24 03 2020
accepted: 07 08 2020
entrez: 9 9 2020
pubmed: 10 9 2020
medline: 27 3 2021
Statut: epublish

Résumé

Like most animals, the survival of fish depends on navigation in space. This capacity has been documented in behavioral studies that have revealed navigation strategies. However, little is known about how freely swimming fish represent space and locomotion in the brain to enable successful navigation. Using a wireless neural recording system, we measured the activity of single neurons in the goldfish lateral pallium, a brain region known to be involved in spatial memory and navigation, while the fish swam freely in a two-dimensional water tank. We found that cells in the lateral pallium of the goldfish encode the edges of the environment, the fish head direction, the fish swimming speed, and the fish swimming velocity-vector. This study sheds light on how information related to navigation is represented in the brain of fish and addresses the fundamental question of the neural basis of navigation in this group of vertebrates.

Identifiants

pubmed: 32901058
doi: 10.1038/s41598-020-71217-1
pii: 10.1038/s41598-020-71217-1
pmc: PMC7479115
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

14762

Références

Tsoar, A. et al. Large-scale navigational map in a mammal. Proc. Natl. Acad. Sci. USA 108, 718 (2011).
Wehner, R. Desert ant navigation: How miniature brains solve complex tasks. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 189, 579–588 (2003).
pubmed: 12879352
Dittman, A. & Quinn, T. Homing in Pacific salmon: Mechanisms and ecological basis. J. Exp. Biol. 199, 83–91 (1996).
pubmed: 9317381
Lipp, H. et al. Pigeon homing along highways and exits. Curr. Biol. 14, 1239–1249 (2004).
pubmed: 15268853
McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I. & Moser, M. Path integration and the neural basis of the’cognitive map’. Nat. Rev. Neurosci. 7, 663–678 (2006).
pubmed: 16858394
Moser, E. I., Kropff, E., & Moser, M. B.  Place cells, grid cells, and the brain's spatial representation system. Annu. Rev. Neurosci. 31, 69–89 (2008).
Moser, E. I. et al. Grid cells and cortical representation. Nat. Rev. Neurosci. 15, 466–481 (2014).
pubmed: 24917300
Seelig, J. D. & Jayaraman, V. Neural dynamics for landmark orientation and angular path integration. Nature 521, 186–191 (2015).
pubmed: 25971509 pmcid: 4704792
Buzsáki, G. & Moser, E. I. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 16, 130–138 (2013).
pubmed: 23354386 pmcid: 4079500
Rowland, D. C., Roudi, Y., Moser, M. & Moser, E. I. Ten years of grid cells. Annu. Rev. Neurosci. 39, 19–40 (2016).
pubmed: 27023731
O’Keefe, J. & Dostrovsky, J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171–175 (1971).
pubmed: 5124915
Hafting, T., Fyhn, M., Molden, S., Moser, M. & Moser, E. I. Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801–806 (2005).
pubmed: 15965463
Taube, J. S., Muller, R. U. & Ranck, J. B. Jr. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10, 420–435 (1990).
pubmed: 2303851 pmcid: 6570151
Taube, J. S., Muller, R. U. & Ranck, J. B. Jr. Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J. Neurosci. 10, 436–447 (1990).
pubmed: 2303852 pmcid: 6570161
Solstad, T., Boccara, C. N., Kropff, E., Moser, M. B. & Moser, E. I. Representation of geometric borders in the entorhinal cortex. Science 322, 1865–1868 (2008).
pubmed: 19095945
Kropff, E., Carmichael, J. E., Moser, M. & Moser, E. I. Speed cells in the medial entorhinal cortex. Nature 523, 419–424 (2015).
pubmed: 26176924
Agrillo, C., Dadda, M., Serena, G. & Bisazza, A. Do fish count? Spontaneous discrimination of quantity in female mosquitofish. Anim. Cogn. 11, 495–503 (2008).
pubmed: 18247068
Brown, C., Laland, K. & Krause, J. Fish Cognition and Behavior (Wiley, New York, 2011).
Bshary, R. & Brown, C. Fish cognition. Curr. Biol. 24, R947–R950 (2014).
pubmed: 25291632
Holbrook, R. I. & de Perera, T. B. Three-dimensional spatial cognition: Freely swimming fish accurately learn and remember metric information in a volume. Anim. Behav. 86, 1077–1083 (2013).
Karlsson, C., Willis, J., Patel, M. & de Perera, T. B. Teleost fish can accurately estimate distance travelled. bioRxiv 834341 (2019). https://doi.org/10.1101/834341 .
Siebeck, U. E., Litherland, L. & Wallis, G. M. Shape learning and discrimination in reef fish. J. Exp. Biol. 212, 2113–2119 (2009).
pubmed: 19525438
Newport, C., Wallis, G., Reshitnyk, Y. & Siebeck, U. E. Discrimination of human faces by archerfish (Toxotes chatareus). Sci. Rep. 6, 27523 (2016).
pubmed: 27272551 pmcid: 4895153
Rodriguez, F., Duran, E., Vargas, J. P., Torres, B. & Salas, C. Performance of goldfish trained in allocentric and egocentric maze procedures suggests the presence of a cognitive mapping system in fishes. Anim. Learn. Behav. 22, 409–420 (1994).
Rodriguez, F. et al. Conservation of spatial memory function in the pallial forebrain of reptiles and ray-finned fishes. J. Neurosci. 22, 2894–2903 (2002).
pubmed: 11923454 pmcid: 6758289
Broglio, C., Rodriguez, F. & Salas, C. Spatial cognition and its neural basis in teleost fishes. Fish Fish. 4, 247–255 (2003).
Broglio, C., Gómez, A., Durán, E., Salas, C. & Rodríguez, F. Brain and cognition in teleost fish. Fish Cognition and Behavior 325–358 (2011).
Salas, C. et al. Neuropsychology of learning and memory in teleost fish. Zebrafish 3, 157–171 (2006).
pubmed: 18248258
Durán, E., Ocaña, F. M., Broglio, C., Rodríguez, F. & Salas, C. Lateral but not medial telencephalic pallium ablation impairs the use of goldfish spatial allocentric strategies in a “hole-board” task. Behav. Brain Res. 214, 480–487 (2010).
pubmed: 20600353
Vargas, J. P., Bingman, V. P., Portavella, M. & López, J. C. Telencephalon and geometric space in goldfish. Eur. J. Neurosci. 24, 2870–2878 (2006).
pubmed: 17156211
Vargas, J. P., López, J. C., Salas, C. & Thinus-Blanc, C. Encoding of geometric and featural spatial information by goldfish (Carassius auratus). J. Comp. Psychol. 118, 206 (2004).
pubmed: 15250808
Canfield, J. G. & Mizumori, S. J. Methods for chronic neural recording in the telencephalon of freely behaving fish. J. Neurosci. Methods 133, 127–134 (2004).
pubmed: 14757353
Rodrıguez, F. et al. Spatial memory and hippocampal pallium through vertebrate evolution: Insights from reptiles and teleost fish. Brain Res. Bull. 57, 499–503 (2002).
pubmed: 11923018
Northcutt, R. G. Do teleost fishes possess a homolog of mammalian isocortex?. Brain Behav. Evol. 78, 136–138 (2011).
pubmed: 21952091
Elliott, S. B., Harvey-Girard, E., Giassi, A. C. & Maler, L. Hippocampal-like circuitry in the pallium of an electric fish: Possible substrates for recursive pattern separation and completion. J. Comp. Neurol. 525, 8–46 (2017).
pubmed: 27292574
Vinepinsky, E., Donchin, O. & Segev, R. Wireless electrophysiology of the brain of freely swimming goldfish. J. Neurosci. Methods 278, 76–86 (2017).
pubmed: 28069391
Cohen, L., Vinepinsky, E., Segev, R. Wireless electrophysiological recording of neurons by movable tetrodes in freely swimming fish. J. Vis. Exp. 153, e60524 (2019).
Gofman, X. et al. Dissociation between postrhinal cortex and downstream parahippocampal regions in the representation of egocentric boundaries. Curr. Biol. 29, 2751-2757.e4 (2019).
pubmed: 31378610
Alexander, A. S. et al. Egocentric boundary vector tuning of the retrosplenial cortex. Sci. Adv. 6, eaaz2322 (2020).
LaChance, P. A., Todd, T. P. & Taube, J. S. A sense of space in postrhinal cortex. Science 365, eaax4192 (2019).
pubmed: 31296737 pmcid: 7063980
Derdikman, D. & Moser, E. I. Space time and memory in the hippocampal formation 107–125 (Springer, New York, 2014).
Yoder, R. M. & Taube, J. S. Head direction cell activity in mice: robust directional signal depends on intact otolith organs. J. Neurosci. 29, 1061–1076 (2009).
pubmed: 19176815 pmcid: 2768409
Wullimann, M. F. & Rink, E. The teleostean forebrain: A comparative and developmental view based on early proliferation, Pax6 activity and catecholaminergic organization. Brain Res. Bull. 57, 363–370 (2002).
pubmed: 11922990
Mueller, T. & Wullimann, M. F. An evolutionary interpretation of teleostean forebrain anatomy. Brain Behav. Evol. 74, 30–42 (2009).
pubmed: 19729894
Northcutt, R. G. Connections of the lateral and medial divisions of the goldfish telencephalic pallium. J. Comp. Neurol. 494, 903–943 (2006).
pubmed: 16385483
Hartley, T., Lever, C., Burgess, N. & O’Keefe, J. Space in the brain: How the hippocampal formation supports spatial cognition. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 369, 20120510 (2013).
pubmed: 24366125
Winter, S. S. & Taube, J. S. Space, Time and Memory in the Hippocampal Formation 83–106 (Springer, New York, 2014).
Broglio, C., Rodríguez, F., Gómez, A., Arias, J. L. & Salas, C. Selective involvement of the goldfish lateral pallium in spatial memory. Behav. Brain Res. 210, 191–201 (2010).
pubmed: 20178818
Durán, E. et al. Telencephalon ablation impairs goldfish allocentric spatial learning in a “hole-board” task. Acta Neurobiol. Exp. (Wars) 68, 519–525 (2008).
Fotowat, H., Lee, C., Jun, J. J. & Maler, L. Neural activity in a hippocampus-like region of the teleost pallium is associated with active sensing and navigation. eLife 8, e44119 (2019).
pubmed: 30942169 pmcid: 6469930
Ulanovsky, N. & Moss, C. F. Hippocampal cellular and network activity in freely moving echolocating bats. Nat. Neurosci. 10, 224–233 (2007).
pubmed: 17220886
Yartsev, M. M., Witter, M. P. & Ulanovsky, N. Grid cellswithout theta oscillations in the entorhinal cortex of bats. Nature 479, 103 (2011).
pubmed: 22051680
Butler, A. B. & Hodos, W. Comparative Vertebrate Neuroanatomy: Evolution and Adaptation (Wiley, Hoboken, 2005).
Yartsev, M. M. & Ulanovsky, N. Representation of three-dimensional space in the hippocampus of flying bats. Science 340, 367–372 (2013).
pubmed: 23599496
Finkelstein, A., Las, L. & Ulanovsky, N. 3-D maps and compasses in the brain. Annu. Rev. Neurosci. 39, 171–196 (2016).
pubmed: 27442069
Sarel, A., Finkelstein, A., Las, L. & Ulanovsky, N. Vectorial representation of spatial goals in the hippocampus of bats. Science 355, 176–180 (2017).
pubmed: 28082589
Jung, M. W., Wiener, S. I. & McNaughton, B. L. Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J. Neurosci. 14, 7347–7356 (1994).
pubmed: 7996180 pmcid: 6576902
Trinh, A., Clarke, S. E., Harvey-Girard, E. & Maler, L. Cellular and network mechanisms may generate sparse coding of sequential object encounters in hippocampal-like circuits. eNeuro 6, 4 (2019).
Bingman, V. P., Hough, G. E. 2nd., Kahn, M. C. & Siegel, J. J. The homing pigeon hippocampus and space: In search of adaptive specialization. Brain Behav. Evol. 62, 117–127 (2003).
pubmed: 12937350
H. L. Payne, D. Aronov. Interaction of place and gaze representations in the hippocampus of food-caching birds. Program No. 604.22. 2019 Neuroscience Meeting Planner. Society for Neuroscience, Chicago, IL, 2019).
Ahrens, M. B., Huang, K. H., Narayan, S., Mensh, B. D. & Engert, F. Two-photon calcium imaging during fictive navigation in virtual environments. Front. Neural Circuits 7, 104 (2013).
pubmed: 23761738 pmcid: 3674334
Varga, A. G. & Ritzmann, R. E. Cellular basis of head direction and contextual cues in the insect brain. Curr. Biol. 26, 1816–1828 (2016).
pubmed: 27397888
Peter, R. E. & Gill, V. E. A stereotaxic atlas and technique for forebrain nuclei of the goldfish, Carassius auratus. J. Comp. Neurol. 159, 69–101 (1975).
pubmed: 1088950
Segev, R., Goodhouse, J., Puchalla, J. & Berry, M. J. Recording spikes from a large fraction of the ganglion cells in a retinal patch. Nat. Neurosci. 7, 1155–1162 (2004).
Lewicki, M. S. A review of methods for spike sorting: the detection and classification of neural action potentials. Netw. Comput. Neural Syst. 9, 53–78 (1998).
Ye, J., Witter, M. P., Moser, M. B. & Moser, E. I. Entorhinal fast-spiking speed cells project to the hippocampus. Proc. Natl. Acad. Sci. USA 115, E1627–E1636 (2018).
pubmed: 29386397

Auteurs

Ehud Vinepinsky (E)

Department of Life Sciences, Ben Gurion University of the Negev, 84105, Beer Sheva, Israel.
Zlotowski Center for Neuroscience, Ben Gurion University of the Negev, 84105, Beer Sheva, Israel.

Lear Cohen (L)

Zlotowski Center for Neuroscience, Ben Gurion University of the Negev, 84105, Beer Sheva, Israel.
Department of Biomedical Engineering, Ben Gurion University of the Negev, 84105, Beer Sheva, Israel.

Shay Perchik (S)

Zlotowski Center for Neuroscience, Ben Gurion University of the Negev, 84105, Beer Sheva, Israel.
Department of Cognitive and Brain Sciences, Ben-Gurion University of the Negev, 84105, Beer Sheva, Israel.

Ohad Ben-Shahar (O)

Zlotowski Center for Neuroscience, Ben Gurion University of the Negev, 84105, Beer Sheva, Israel.
Department of Computer Sciences, Ben Gurion University of the Negev, 84105, Beer Sheva, Israel.

Opher Donchin (O)

Zlotowski Center for Neuroscience, Ben Gurion University of the Negev, 84105, Beer Sheva, Israel.
Department of Biomedical Engineering, Ben Gurion University of the Negev, 84105, Beer Sheva, Israel.

Ronen Segev (R)

Department of Life Sciences, Ben Gurion University of the Negev, 84105, Beer Sheva, Israel. ronensgv@bgu.ac.il.
Zlotowski Center for Neuroscience, Ben Gurion University of the Negev, 84105, Beer Sheva, Israel. ronensgv@bgu.ac.il.
Department of Biomedical Engineering, Ben Gurion University of the Negev, 84105, Beer Sheva, Israel. ronensgv@bgu.ac.il.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH