Abstract
This study assessed spatial memory and orientation strategies in Chiloscyllium griseum. In the presence of visual landmarks, six sharks were trained in a fixed turn response. Group 1 started from two possible compartments approaching two goal locations, while group 2 started from and approached only one location, respectively. The learning criterion was reached within 9 ± 5.29 (group 1) and 8.3 ± 3.51 sessions (group 2). Transfer tests revealed that sharks had applied a direction strategy, possibly in combination with some form of place learning. Without visual cues, sharks relied solely on the former. To identify the underlying neural substrate(s), telencephalic were lesioned and performance compared before and after surgery. Ablation of the dorsal and medial pallia only had an effect on one shark (group 1), indicating that the acquisition and retention of previously gained knowledge were unaffected in the remaining four individuals. Nonetheless, the shark re-learned the task. In summary, C. griseum can utilize fixed turn responses to navigate to a goal; there is also some evidence for the use of external visual landmarks while orienting. Probably, strategies can be used alone or in combination. Neither the dorsal nor medial pallium seems to be responsible for the acquisition and processing of egocentric information.
Similar content being viewed by others
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
- TrP:
-
Training phase
- TP:
-
Transfer phase
References
Able KP (1989) Skylight polarization patterns and the orientation of migratory birds. J Exp Biol 141:241–256
Aronson LR (1951) Orientation and jumping behavior in the gobiid fish, Bathygobius soporator. Am Mus Novit 1486:1–22
Barnes CA, Nadel L, Honig WK (1980) Spatial memory deficit in senescent rats. Can J Psychol 34(1):29–39
Bingman VP, Jones TJ (1994) Sun compass-based spatial learning impaired in homing pigeons with hippocampal lesions. Neuroscience 14(11):6687–6694
Bingman VP, Mench J (1990) Homing behavior of hippocampus and parahippocampus lesioned pigeons following short-distance releases. Behav Brain Res 40(3):227–238
Bingman VP, Bagnoli P, Ioalé P, Casini G (1989) Behavioral and anatomical studies of the avian hippocampus. Wiley, New York
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
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
Brown C, Gardner C, Braithwaite VA (2005) Differential stress responses in fish from areas of high- and low-predation pressures. J Comp Physiol B 175:305–312
Burda H, Marhold S, Westenberger T, Wiltschko R, Wiltschko W (1990) Magnetic compass orientation in the subterranean rodent Cryptomys hottentotus (Bathyergidae). Experientia 46:528–530
Burt de Perera T, Macias Garcia C (2003) Amarillo fish (Girardinichthys multiradiatus) use visual landmarks to orient in space. Ethology 109:341–350
Dodson JJ (1988) The nature and role of learning in the orientation and migratory behavior of fishes. Environ Biol Fish 23(3):161–182
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
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
Edren S and Gruber S (2005) Homing ability of young lemon sharks, Negaprion brevirostris. Environ Biol Fish 72(3):267–281
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) Place learning prior to and after telencephalon ablation in bamboo and coral cat sharks (Chiloscyllium griseum and Atelomycterus marmoratus). J Comp Physiol A (in this issue). doi:10.1007/s00359-013-0859-x
Gaffan D, Harrison S (1989) Place memory and scene memory: effects of fornix transection in the monkey. Exp Brain Res 74(1):202–212
Good M (1987) The effects of hippocampal-area parahippocampalis lesions on discrimination learning in the pigeon. Behav Brain Res 26:171–184
Good M, Macphail EM (1994a) The avian hippocampus and short-term-memory for spatial and nonspatial information. J Exp Psychol B 47:293–317
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
Hofmann MH, Northcutt RG (2012) Forebrain organization in elasmobranchs. Brain Behav Evol 80:142–151
Holbrook R, de Perera Burt (2011) Three-dimensional spatial cognition: information in the vertical dimension overrides information from the horizontal. Anim Cogn 14(4):613–619
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
Huntingford FA, Wright PJ (1989) How sticklebacks learn to avoid dangerous feeding places. Behav Process 19:181–189
Ingle D, Sahagian D (1973) Solution of a spatial constancy problem by goldfish. Physiol Pscychol 1(1):83–84
Jacobs LF (2003) The evolution of the cognitive map. Brain Behav Evolut 62(2):128–139
Kandel ER, Schwartz JH, Jessell TM (1995) Neurowissenschaften: Eine Einführung. Spektrum Akademischer, Heidelberg, p 324
Kleerekoper H, Timms AM, Westlake GF (1970) An analysis of locomotor behaviour of goldfish (Carassius auratus). Anim Behav 18:317
Kleerekoper H, Matis J, Gensler P, Maynard P (1974) Exploratory behaviour of goldfish Carassius auratus. Anim Behav 22:124–132
Labhart T, Meyer EP (2002) Neural mechanisms in insect navigation: polarization compass and odometer. Curr Opin Neurobiol 12(6):707–714
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
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
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
Martín I, Gómez A, Salas C, Puerto A, Rodríguez F (2011) Dorsomedial pallium lesions impair taste aversion learning in goldfish. Neurobiol Learn Mem 96:297–305
Mazmanian DS, Roberts WA (1983) Spatial memory in rats under restricted viewing conditions. Learn Motiv 14:123–139
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
Morris RGN, Garrud P, Rawlins JNP (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297(5868):681–683
Northcutt RG (1977) Elasmobranch central nervous system organization and its possible evolutionary significance. Am Zool 17:411–429
Northcutt RG (1981) Evolution of the telencephalon in nonmammals. Annu Rev Neurosci 4:301–350
Northcutt RG (1995) The forebrain of gnathostomes: in search of a morphotype. Brain Behav Evol 46:275–318
Northcutt RG (2011) Do teleost fishes possesses a homolog of mammalian isocortex? Brain Behav Evol 78:136–138
Northcutt RG, Braford MR (1980) New observations on the organization and evolution of the telencephalon in actinopterygian fishes. Comparative neurology of the telencephalon. Plenum Press, New York
O’Gower AK (1995) Speculations on a spatial memory for the Port Jackson shark (Heterodontus portusjacksoni) (Heterodontidae). Marine Freshw Res 46:861–871
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
O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, Oxford
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
Odling-Smee L, Braithwaite VA (2003) The role of learning in fish orientation. Fish Fish 4(3):235–246
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
Olton DS, Papas B (1979) Spatial memory and hippocampal function. Neuropsychologia 17:669–682
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
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
Peterson E (1980) Behavioral studies of telencephalic function in reptiles. Comparative neurology of the telencephalon. Plenum Press, New York
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
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
Rasmussen M, Barnes CA, McNaughton BL (1989) A systematic test of cognitive mapping, working-memory, and temporal discontinuity theories of hippocampal function. Psychobiology 17(4):335–348
Reese ES (1989) Orientation behavior of butterfly fishes (family Chaetodontidae) on coral reefs: spatial learning of route specific landmarks and cognitive maps. Environ Biol Fish 25(1–3):79–86
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
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
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
Roitblatt HL (1982) The meaning of representation in animal memory. Behav Brain Sci 5:353–406
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
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
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
Schluessel V, Bleckmann H (2005) Spatial memory and orientation strategies in the elasmobranch Potamotrygon motoro. J Comp Physiol A 191(8):695–706
Schluessel V, Bleckmann H (2012) Spatial learning and memory retention in the grey bamboo shark (Chiloscyllium griseum). Zoology 115(6):346–353
Sherry DF, Vaccarino AL, Buckenham K, Herz RS (1989) The hippocampal complex of food-storing birds. Brain Behav Evol 34:308–317
Smeets WJAJ, Nieuwenhuys R, Roberts BL (1983) The central nervous system of cartilaginous fishes. Springer, Berlin
Smith ML, Milner B (1981) The role of the right hippocampus in the recall of spatial location. Neuropsychologia 19(6):781–793
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
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 Proc 29:199–210
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
Sovrano VA, Bisazza A, Vallortigara G (2007) How fish do geometry in large and in small spaces. Anim Cogn 10:47–54
Thinus-Blanc C (1988) Animal spatial condition. Thought without language. Oxford University Press, Oxford
Tolman EC (1948) Cognitive maps in rats and men. Psychol Rev 55:189–208
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
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
von Frisch K (1967) The dance language and orientation of bees. Harvard University Press, Cambridge
Walcott C (1996) Pigeon homing: observations, experiments, and confusions. J Exp Biol 199:21–27
Wallraff HG (2003) Olfactory navigation by birds. J für Ornithologie 144:1–32
Warburton K (1990) The use of local landmarks by foraging goldfish. Anim Behav 40(3):500–505
Warrant EJ, Kelber A, Gislén A, Greiner B, Ribi W, Wcislo WT (2004) Nocturnal vision and landmark orientation in a tropical halictid bee. Curr Biol 14(15):1309–1318
Wiltschko R, Wiltschko W (1996) Magnetic orientation in birds. J Exp Biol 199:29–38
Yopak KE (2012) Neuroecology of cartilaginous fishes: the functional implications of brain scaling. Fish Biol 80(5):1968–2023
Acknowledgments
We would like to thank Ursula Dung for conducting experiments during the training phase and 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).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Fuss, T., Bleckmann, H. & Schluessel, V. The shark Chiloscyllium griseum can orient using turn responses before and after partial telencephalon ablation. J Comp Physiol A 200, 19–35 (2014). https://doi.org/10.1007/s00359-013-0858-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-013-0858-y