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Place learning prior to and after telencephalon ablation in bamboo and coral cat sharks (Chiloscyllium griseum and Atelomycterus marmoratus)

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Abstract

This study assessed complex spatial learning and memory in two species of shark, the grey bamboo shark (Chiloscyllium griseum) and the coral cat shark (Atelomycterus marmoratus). It was hypothesized that sharks can learn and apply an allocentric orientation strategy. Eight out of ten sharks successfully completed the initial training phase (by locating a fixed goal position in a diamond maze from two possible start points) within 14.9 ± 7.6 sessions and proceeded to seven sets of transfer tests, in which sharks had to perform under altered environmental conditions. Transfer tests revealed that sharks had oriented and solved the tasks visually, using all of the provided environmental cues. Unintentional cueing did not occur. Results correspond to earlier studies on spatial memory and cognitive mapping in other vertebrates. Future experiments should investigate whether sharks possess a cognitive spatial mapping system as has already been found in several teleosts and stingrays. Following the completion of transfer tests, sharks were subjected to ablation of most of the pallium, which compromised their previously acquired place learning abilities. These results indicate that the telencephalon plays a crucial role in the processing of information on place learning and allocentric orientation strategies.

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Abbreviations

ITI:

Inter-trial-interval

MS222:

Tricaine methanesulfonate

PFA:

Paraformaldehyde

POP:

Post-operative phase

SC:

Starting compartment

T1, T2, T3:

Transfer test 1, transfer test 2, transfer test 3

TP:

Transfer phase

TrP:

Training phase

References

  • Aronson LR (1951) Orientation and jumping behavior in the gobiid fish, Bathygobius soporator. Am Mus Novit 1486:1–22

    Google Scholar 

  • Barnes CA, Nadel L, Honig WK (1980) Spatial memory deficit in senescent rats. Can J Psychol 34(1):29–39

    Article  CAS  PubMed  Google Scholar 

  • Bingman VP (1992) The importance of comparative studies and ecological validity for understanding hippocampal structure and cognitive function. Hippocampus 2:213–220

    Article  CAS  PubMed  Google Scholar 

  • Bingman VP, Jones TJ (1994) Sun compass-based spatial learning impaired in homing pigeons with hippocampal lesions. Neuroscience 14(11):6687–6694

    CAS  PubMed  Google Scholar 

  • Bingman VP, Mench J (1990) Homing behavior of hippocampus and parahippocampus lesioned pigeons following short-distance releases. Behav Brain Res 40(3):227–238

    Article  CAS  PubMed  Google Scholar 

  • Bingman VP, Bagnoli P, Ioalé P, Casini G (1989) Behavioral and anatomical studies of the avian hippocampus. Liss, New York

    Google Scholar 

  • Broglio C, Rodriguez F, Salas C (2003) Spatial cognition and its neural basis in teleost fishes. Fish Fish 4(3):247–255

    Article  Google Scholar 

  • Broglio C, Gómez A, Durán E, Ocaña FM, Jiminez-Moya F, Rodríguez F, Salas C (2005) Hallmarks of a common forebrain vertebrate plan: specialized pallial areas for spatial, temporal and emotional memory in actinopterygian fish. Brain Res Bull 66(4–6):277–281

    Article  CAS  PubMed  Google Scholar 

  • Broglio C, Rodríguez F, Gómez A, Arias JL, Salas C (2010) Selective involvement of the goldfish lateral pallium in spatial memory. Behav Brain Res 210(2):191–201

    Article  CAS  PubMed  Google Scholar 

  • Burgess N, Jeffery KJ, O’Keefe J (1999) The hippocampal and parietal foundations of spatial cognition. Oxford University Press, London

    Google Scholar 

  • Burt de Perera T, Macias Garcia C (2003) Amarillo fish (Girardinichthys multiradiatus) use visual landmarks to orient in space. Ethology 109:341–350

    Article  Google Scholar 

  • Dodson JJ (1988) The nature and role of learning in the orientation and migratory behavior of fishes. Environ Biol Fish 23(3):161–182

    Article  Google Scholar 

  • Durán E, Ocaña FM, Gómez A, Jiménez-Moya F, Broglio C, Rodríguez F, Salas C (2008) Telencephalon ablation impairs goldfish allocentric spatial learning in a “hole-board” task. Acta Neurobiol Exp 68:519–525

    Google Scholar 

  • Durán E, Ocaña FM, Broglio C, Rodríguez F, Salas C (2010) Lateral but not medial telencephalic pallium ablation impairs the use of goldfish spatial allocentric strategies in a “hole-board” task. Behav Brain Res 214(2):480–487

    Article  PubMed  Google Scholar 

  • Edren S, Gruber S (2005) Homing ability of young lemon sharks, Negaprion brevirostris. Environ Biol Fish 72(3):267–281

    Article  Google Scholar 

  • Font E, Gómez-Gómez A (1991) Spatial memory and exploration in lizards: role of the medial cortex. Abstracts of the Animal Behavior Society Meeting, Wilmington

  • Fuss T, Bleckmann H, Schluessel V (2013) The shark Chiloscyllium griseum can orient using turn responses before and after partial telencephalon ablation. J Comp Physiol A (in this issue). doi:10.1007/s00359-013-0858-y

  • Gaffan D, Harrison S (1989) Place memory and scene memory: effects of fornix transection in the monkey. Exp Brain Res 74(1):202–212

    Article  CAS  PubMed  Google Scholar 

  • Galistel CR (1990) The organization of learning. Bradford Books/MIT Press, Cambridge

    Google Scholar 

  • Good M (1987) The effects of hippocampal-area parahippocampalis lesions on discrimination learning in the pigeon. Behav Brain Res 26:171–184

    Article  CAS  PubMed  Google Scholar 

  • Good M, Macphail EM (1994a) The avian hippocampus and short-term-memory for spatial and nonspatial information. J Exp Psychol B 47:293–317

    CAS  Google Scholar 

  • Good M, Macphail EM (1994b) Hippocampal-lesions in pigeons (Columba livia) disrupt reinforced preexposure but not overshadowing or blocking. J Exp Psychol B 47:263–291

    CAS  Google Scholar 

  • Hodgson ES, Mathewson RF (1979) Sensory biology of sharks, skates, and rays. Sensory biology of sharks, skates and rays. US Government Printing Office, Washington, DC, pp 227–267

  • Hughes R, Blight C (2000) Two intertidal fish species use visual association learning to track the status of food patches in a radial maze. Anim Behav 59(3):613–621

    Article  PubMed  Google Scholar 

  • Ingle D, Sahagian D (1973) Solution of a spatial constancy problem by goldfish. Physiol Pscychol 1(1):83–84

    Article  Google Scholar 

  • Kalmijn AJ (1971) Electroreception in sharks and rays. Environ Biol 55:371–383

    CAS  Google Scholar 

  • Kleerekoper H, Timms AM, Westlake GF (1970) An analysis of locomotor behaviour of goldfish (Carassius auratus). Anim Behav 18: 317 ff

    Google Scholar 

  • Lee SA, Vallortigara G, Ruga V, Sovrano VA (2012) Independent effects of geometry and landmark in a spontaneous reorientation task: a study of two species of fish. Anim Cogn 15(5):861–870

    Article  PubMed  Google Scholar 

  • Lee SA, Vallortigara G, Flore M, Spelke ES, Sovrano VA (2013) Navigation by environmental geometry: the use of zebrafish as a model. J Exp Biol 216(Pt 19):3693–3699

    Google Scholar 

  • López JC, Broglio C, Rodríguez F, Thinus-Blanc C, Salas C (1999) Multiple spatial learning strategies in goldfish (Carassius auratus). Anim Cogn 2:109–120

    Article  Google Scholar 

  • López JC, Rodríguez F, Gómez Y, Vargas JP, Broglio C, Salas C (2000) Place and cue learning in turtles. Anim Learn Behav 28(4):360–372

    Article  Google Scholar 

  • López JC, Vargas JP, Gómez Y, Salas C (2003) Spatial and non-spatial learning in turtles: the role of medial cortex. Behav Brain Res 143(2):109–120

    Article  PubMed  Google Scholar 

  • Mazmanian DS, Roberts WA (1983) Spatial memory in rats under restricted viewing conditions. Learn Motiv 14:123–139

    Article  Google Scholar 

  • Meyer C, Papastamatiou K, Holland KN (2010) A multiple instrument approach to quantifying the movement patterns and habitat use of tiger (Galeocerdo cuvier) and Galapagos sharks (Carcharhinus galapagensis) at French Frigate Shoals, Hawaii. Mar Biol 157(8):1857–1868

    Article  Google Scholar 

  • Morris RGN, Garrud P, Rawlins JNP (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297(5868):681–683

    Google Scholar 

  • Nadel L (1991) Multiple memory systems: what and why. Cogn Neurosci 4(3):179–188

    Article  Google Scholar 

  • Nadel L (1994) Multiple memory systems: what and why. An update. MIT Press, Cambridge

    Google Scholar 

  • Nakajima S, Izawa E, Matsushima T (2003) Hippocampal lesion delays the acquisition of egocentric spatial memory in chicks. Neuro Report 14:1475–1480

    Google Scholar 

  • Nieuwenhuys R (2009) The forebrain of actinopterygians revisited. Brain Behav Evol 73:229–252

    Article  PubMed  Google Scholar 

  • Northcutt RG (1977) Elasmobranch central nervous system organization and its possible evolutionary significance. Am Zool 17:411–429

    Google Scholar 

  • Northcutt RG (1981) Evolution of the telencephalon in nonmammals. Annu Rev Neurosci 4:301–350

    Article  CAS  PubMed  Google Scholar 

  • Northcutt RG (1995) The forebrain of gnathostomes: in search of a morphotype. Brain Behav Evol 46:275–318

    Article  CAS  PubMed  Google Scholar 

  • Northcutt RG, Braford MR (1980) New observations on the organization and evolution of the telencephalon in actinopterygian fishes. In: Ebbeson SOE (ed) Comparative neurology of the telencephalon. Plenum Press, New York, pp 41–98

  • O’Gower AK (1995) Speculations on a spatial memory for the Port Jackson shark (Heterodontus portusjacksoni) (Heterodontidae). Marine Freshw Res 46:861–871

    Article  Google Scholar 

  • O’Keefe J, Burgess N (1996) Geometric determinants of the place fields of hippocampal neurons. Nature 381:425–428

    Article  PubMed  Google Scholar 

  • O’Keefe J, Conway DH (1978) Hippocampal place units in the freely moving rat: why they fire where they fire. Exp Brain Res 31:573–590

    PubMed  Google Scholar 

  • O’Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map: preliminary evidence from unit activity in the freely moving rat. Behav Brain Res 34:171–175

    Google Scholar 

  • O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, Oxford

    Google Scholar 

  • O’Keefe J, Nadel L, Keightleya S, Kill D (1975) Fornix lesions selectively abolish place learning in the rat. Exp Neurol 48(1):152–166

    Article  PubMed  Google Scholar 

  • Odling-Smee L, Braithwaite VA (2003) The role of learning in fish orientation. Fish Fish 4(3):235–246

    Article  Google Scholar 

  • Odling-Smee L, Boughman JW, Braithwaite VA (2008) Sympatric species of three spine stickleback differ in their performance in a spatial learning task. Behav Ecol Sociobiol 62(12):1935–1945

    Article  Google Scholar 

  • Okaichi H, Oshima Y (1990) Choice behavior of hippocampectomized rats in the radial arm maze. Psychobiology 18(4):416–421

    Google Scholar 

  • O’Keefe J (1991) The hippocampal cognitive map and navigational strategies. Oxford University Press, Oxford

    Google Scholar 

  • Olton DS, Papas B (1979) Spatial memory and hippocampal function. Neuropsychologia 17:669–682

    Article  CAS  PubMed  Google Scholar 

  • Papastamatiou YP, Cartamil DP, Lowe CG, Meyer CG, Wetherbee BM, Holland KN (2011) Scales of orientation, directed walks and movement path structure in sharks. Anim Ecol 80:864–874

    Article  Google Scholar 

  • Parkinson JK, Murray EA, Mishkin M (1988) A selective mnemonic role for the hippocampus in monkeys: memory for location of objects. Neuroscience 8:4159–4167

    CAS  PubMed  Google Scholar 

  • Peterson E (1980) Behavioral studies of telencephalic function in reptiles. Plenum Press, New York

    Google Scholar 

  • Pico RM, Gerbrandt LK, Pondel M, Ivy G (1985) During stepwise cue deletion, rat place behaviors correlate with place unit response. Brain Res Bull 330:369–372

    CAS  Google Scholar 

  • Portavella M, Vargas JP, Torres B, Salas C (2002) The effects of telencephalic pallial lesions on spatial, temporal, and emotional learning in goldfish. Brain Res Bull 57:397–399

    Article  CAS  PubMed  Google Scholar 

  • Rasmussen M, Barnes CA, McNaughton BL (1989) A systematic test of cognitive mapping, working-memory, and temporal discontiguity theories of hippocampal function. Psychobiology 17(4):335–348

    Google Scholar 

  • Reese ES (1989) Orientation behavior of butterflyfishes (family Chaetodontidae) on coral reefs: spatial learning of route specific landmarks and cognitive maps. Environ Biol Fish 25(1–3):79–86

    Article  Google Scholar 

  • Rodríguez F, Durán E, Vargas JP, Torres B, Salas C (1994) Performance of goldfish trained in allocentric and egocentric maze procedures suggests the presence of a cognitive mapping system in fishes. Anim Learn Behav 22(4):409–420

    Article  Google Scholar 

  • Rodríguez F, López JC, Vargas JF, Gómez Y, Broglio C, Salas C (2002a) Conservation of spatial memory function in the pallial forebrain of reptiles and ray-finned fishes. Neuroscience 22(7):2894–2903

    PubMed  Google Scholar 

  • Rodríguez F, López JC, Vargas JF, Broglio C, Gómez Y, Salas C (2002b) Spatial memory and hippocampal pallium through vertebrate evolution: insights from reptiles and teleost fish. Brain Res Bull 57:499–503

    Article  PubMed  Google Scholar 

  • Roitblatt HL (1982) The meaning of representation in animal memory. Behav Brain Sci 5:353–406

    Article  Google Scholar 

  • Salas C, Broglio C, Rodríguez F (2003) Evolution of forebrain and spatial cognition in vertebrates: conservation across diversity. Brain Behav Evol 62(2):72–82

    Google Scholar 

  • Salas C, Rodríguez F, Vargas JP, Durán E, Torres B (1996a) Spatial learning and memory deficits after telencephalic ablation in goldfish trained in place and turn maze procedures. Behav Neurosci 5(110):965–980

    Article  Google Scholar 

  • Salas C, Broglio C, Rodríguez F, López JC, Portavella M, Torres B (1996b) Telencephalic ablation in goldfish impairs performance in a ‘spatial constancy’ problem but not in a cued one. Behav Brain Res 79:193–200

    Article  CAS  PubMed  Google Scholar 

  • Schluessel V, Bleckmann H (2005) Spatial memory and orientation strategies in the elasmobranch Potamotrygon motoro. J Comp Physiol A 191(8):695–706

    Article  Google Scholar 

  • Schluessel V, Bleckmann H (2012) Spatial learning and memory retention in the grey bamboo shark (Chiloscyllium griseum). Zool 115(6):346–353

    Article  Google Scholar 

  • Sherry DF, Vaccarino AL, Buckenham K, Herz RS (1989) The hippocampal complex of food-storing birds. Brain Behav Evol 34:308–317

    Article  CAS  PubMed  Google Scholar 

  • Smith ML, Milner B (1981) The role of the right hippocampus in the recall of spatial location. Neuropsychologia 19(6):781–793

    Article  CAS  PubMed  Google Scholar 

  • Sovrano VA, Bisazza A, Vallortigara G (2002) Modularity and spatial reorientation in a simple mind: encoding of geometric and nongeometric properties of a spatial environment by fish. Cognition 85:B51–B59

    Article  PubMed  Google Scholar 

  • Sovrano VA, Bisazza A, Vallortigara G (2003) Modularity as a fish views it: conjoining geometric and nongeometric information for spatial reorientation. J Exp Psychol Anim Behav Process 29:199–210

    Google Scholar 

  • Sovrano VA, Bisazza A, Vallortigara G (2005) Animals’ use of landmarks and metric information to reorient: effects of the size of the experimental space. Cognition 97:121–133

    Article  PubMed  Google Scholar 

  • Sovrano VA, Bisazza A, Vallortigara G (2007) How fish do geometry in large and in small spaces. Anim Cogn 10:47–54

    Article  PubMed  Google Scholar 

  • Thinus-Blanc C (1996) Animal spatial cognition. Behavioral and brain approach. World Scientific, Singapore

    Book  Google Scholar 

  • Tolman EC (1948) Cognitive maps in rats and men. Psychol Rev 55:189–208

    Article  CAS  PubMed  Google Scholar 

  • Tommasi L, Gagliardo A, Andrew RJ, Vallortigara G (2003) Separate processing mechanisms for encoding of geometric and landmark information in the avian hippocampus. Eur J Neurosci 17:1695–1702

    Article  PubMed  Google Scholar 

  • Vargas JP, López JC, Salas C, Thinus-Blanc C (2004) Encoding of geometric and featural spatial information by goldfish (Carassius auratus). Comp Psychol 118(2):206–216

    Article  Google Scholar 

  • Warburton K (1990) The use of local landmarks by foraging goldfish. Anim Behav 40(3):500–505

    Article  Google Scholar 

  • Wullimann MF, Mueller T (2004) Teleostean and mammalian forebrains contrasted: evidence from genes to behavior. J Comp Neurol 475:143–162

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Slawa Braun for animal caretaking, maintenance and repairs. We are specifically grateful to Dr. med. Ulrich Gerigk for his valuable help with surgical sewing. The research reported herein was performed under the guidelines established by the current German animal protection law (Landesamt für Natur, Umwelt und Verbraucherschutz NRW, 8.87-50.10.37.09.198).

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Fuss, T., Bleckmann, H. & Schluessel, V. Place learning prior to and after telencephalon ablation in bamboo and coral cat sharks (Chiloscyllium griseum and Atelomycterus marmoratus). J Comp Physiol A 200, 37–52 (2014). https://doi.org/10.1007/s00359-013-0859-x

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