Advertisement

Active Electrolocation and Spatial Learning

  • Sarah Nicola Jung
  • Jacob EngelmannEmail author
Chapter
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 70)

Abstract

This chapter presents an overview of the emerging research on spatial learning in weakly electric fish. In the first part, mechanisms by which active electrolocation can provide spatial information are summarized. This includes research on the intricate dynamics of sensorimotor behaviors that enable weakly electric fish to actively generate electrosensory flow. Starting from a summary of spatial learning mechanisms in nonelectric teleost fish, behavioral studies that have begun to investigate spatial learning in weakly electric fish are presented. The behavioral data are then connected with what is known about the neuronal substrate of spatial cognition in teleost fish in general, with a particular focus on the involvement of the dorsal telencephalon. Based on this, the final section summarizes the current data on the telencephalic networks of weakly electric fish. Comparative studies have led to partially novel and hypothetical views that posit similarities between forebrain networks of weakly electric fish and mammalian cortical and thalamocortical networks. Although being a newly emerging line of research, the sensory specialties of the active sensory system of weakly electric fish clearly offer a chance to widen research on the spatial cognition of teleosts by providing novel insights through comparative approaches.

Keywords

Active electrolocation Allocentric Egocentric Electric image Electrosensory flow Navigation Path integration Pattern completion Pattern separation Spatial learning Telencephalic networks 

Notes

Compliance with Ethics Requirements

Sarah Nicola Jung declares that she has no conflict of interest.

Jacob Engelmann declares that he has no conflict of interest.

References

  1. Aronson LR (1971) Further studies on orientation and jumping behavior in the gobid fish, Bathygobius soporator. Ann N Y Acad Sci 188:378–392.  https://doi.org/10.1111/j.1749-6632.1971.tb13110.xCrossRefGoogle Scholar
  2. Babineau D, Lewis JE, Longtin A (2007) Spatial acuity and prey detection in weakly electric fish. PLoS Comput Biol 3(3):e38.  https://doi.org/10.1371/journal.pcbi.0030038CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bacelo J, Engelmann J, Hollmann M et al (2008) Functional foveae in an electrosensory system. J Comp Neurol 511(3):342–359.  https://doi.org/10.1002/cne.21843CrossRefPubMedGoogle Scholar
  4. Bastian J (1982) Vision and electroreception: Integration of sensory information in the optic tectum of the weakly electric fish Apteronotus albifrons. J Comp Physiol A 147(3):287–297.  https://doi.org/10.1007/BF00609662CrossRefGoogle Scholar
  5. Bell CC, Maler L (2005) Central neuroanatomy of electrosensory systems in fish. In: Bullock TH, Hopkins CD, Popper AN, Fay RR (eds) Electroreception. Springer, New York, pp 68–111.  https://doi.org/10.1007/0-387-28275-0_4CrossRefGoogle Scholar
  6. Braford MR (2009) Stalking the everted telencephalon: comparisons of forebrain organization in basal ray-finned fishes and teleosts. Brain Behav Evol 74(1):56–76.  https://doi.org/10.1159/000229013CrossRefPubMedGoogle Scholar
  7. Broglio C, Rodríguez F, Gómez A et al (2010) Selective involvement of the goldfish lateral pallium in spatial memory. Behav Brain Res 210(2):480–487.  https://doi.org/10.1016/j.bbr.2010.06.010CrossRefGoogle Scholar
  8. Burt de Perera T, Holbrook RI, Davis V (2016) The representation of three-dimensional space in fish. Front Behav Neurosci 10:40.  https://doi.org/10.3389/fnbeh.2016.00040CrossRefPubMedPubMedCentralGoogle Scholar
  9. Buzsáki G (2005) Theta rhythm of navigation: Link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15(7):827–840.  https://doi.org/10.1002/hipo.20113CrossRefPubMedGoogle Scholar
  10. Buzsáki G, Moser EI (2013) Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 16(2):130–138.  https://doi.org/10.1038/nn.3304CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cain P (1995) Navigation in familiar environments by the weakly electric elephantnose fish, Gnathonemus petersii L. (Mormyriformes, Teleostei). Ethology 99(4):332–349.  https://doi.org/10.1111/j.1439-0310.1995.tb00907.xCrossRefGoogle Scholar
  12. Cain P, Malwal S (2002) Landmark use and development of navigation behaviour in the weakly electric fish Gnathonemus petersii (Mormyridae; Teleostei). J Exp Biol 205:3915–3923Google Scholar
  13. Cain P, Gerin W, Moller P (1994) Short-range navigation of the weakly electric fish, Gnathonemus petersii L. (Mormyridae, Teleostei), in novel and familiar environments. Ethology 96(1):33–45.  https://doi.org/10.1111/j.1439-0310.1994.tb00879.xCrossRefGoogle Scholar
  14. Canfield JG, Mizumori SJY (2004) Methods for chronic neural recording in the telencephalon of freely behaving fish. J Neurosci Methods 133:127–134.  https://doi.org/10.1016/j.jneumeth.2003.10.011CrossRefPubMedGoogle Scholar
  15. Caputi AA, Budelli R (2006) Peripheral electrosensory imaging by weakly electric fish. J Comp Physiol A 192(6):587–600.  https://doi.org/10.1007/s00359-006-0100-2CrossRefGoogle Scholar
  16. Caputi AA, Aguilera PA, Castelló ME (2003) Probability and amplitude of novelty responses as a function of the change in contrast of the reafferent image in G. carapo. J Exp Biol 206:999–1010.  https://doi.org/10.1242/jeb.00199CrossRefGoogle Scholar
  17. Carlson BA (2002) Neuroanatomy of the mormyrid electromotor control system. J Comp Neurol 454(4):440–455.  https://doi.org/10.1002/cne.10462CrossRefGoogle Scholar
  18. Castelló ME, Aguilera PA, Trujillo-Cenóz O et al (2000) Electroreception in Gymnotus carapo: pre-receptor processing and the distribution of electroreceptor types. J Exp Biol 203:3279–3287Google Scholar
  19. Chen L, House JL, Krahe R et al (2005) Modeling signal and background components of electrosensory scenes. J Comp Physiol A 191(4):331–345.  https://doi.org/10.1007/s00359-004-0587-3CrossRefGoogle Scholar
  20. Clarke SE, Maler L (2017) Feedback synthesizes neural codes for motion. Curr Biol 27(9):1356–1361.  https://doi.org/10.1016/j.cub.2017.03.068CrossRefPubMedGoogle Scholar
  21. Clarke SE, Longtin A, Maler L (2015) The neural dynamics of sensory focus. Nat Commun 6:8764.  https://doi.org/10.1038/ncomms9764CrossRefPubMedPubMedCentralGoogle Scholar
  22. Corbet PS (1961) The food of non-cichlid fishes in the Lake Victoria Basin, with remarks on their evolution and adaptation to lacustrine conditions. Proc Zool Soc London 136(1):1–101.  https://doi.org/10.1111/j.1469-7998.1961.tb06080.xCrossRefGoogle Scholar
  23. Corrêa SA, Grant K, Hoffmann A (1998) Afferent and efferent connections of the dorsocentral telencephalon in an electrosensory teleost, Gymnotus carapo. Brain Behav Evol 52(2):81–98.  https://doi.org/10.1159/000006554
  24. Durán E, Ocaña FM, Martín-Monzón I et al (2014) Cerebellum and spatial cognition in goldfish. Behav Brain Res 259:1–8.  https://doi.org/10.1016/j.bbr.2013.10.039CrossRefPubMedGoogle Scholar
  25. Eichenbaum H, Cohen NJ (2014) Can we reconcile the declarative memory and spatial navigation views on hippocampal function? Neuron 83(4):764–770.  https://doi.org/10.1016/j.neuron.2014.07.032CrossRefPubMedPubMedCentralGoogle Scholar
  26. Elliott SB, Harvey-Girard E, Giassi ACC et al (2017) Hippocampal-like circuitry in the pallium of an electric fish: possible substrates for recursive pattern separation and completion. J Comp Neurol 525(1):8–46.  https://doi.org/10.1002/cne.24060CrossRefPubMedGoogle Scholar
  27. Ernst MO, Banks MS (2002) Humans integrate visual and haptic information in a statistically optimal fashion. Nature 415(6870):429–433.  https://doi.org/10.1038/415429aCrossRefPubMedGoogle Scholar
  28. Etienne AS (2004) Resetting the path integrator: a basic condition for route-based navigation. J Exp Biol 207(9):1491–1508.  https://doi.org/10.1242/jeb.00906CrossRefPubMedGoogle Scholar
  29. Fechler K, Holtkamp D, Neusel G et al (2012) Mind the gap: the minimal detectable separation distance between two objects during active electrolocation. J Fish Biol 81(7):2255–2276.  https://doi.org/10.1111/j.1095-8649.2012.03438.xCrossRefPubMedGoogle Scholar
  30. Fecteau JH, Munoz DP (2006) Salience, relevance, and firing: a priority map for target selection. Trends Cogn Sci 10(8):382–390.  https://doi.org/10.1016/j.tics.2006.06.011CrossRefPubMedGoogle Scholar
  31. Fyhn M, Hafting T, Treves A et al (2007) Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446(7132):190–194.  https://doi.org/10.1038/nature05601CrossRefPubMedGoogle Scholar
  32. Ganz J, Kroehne V, Freudenreich D et al (2014) Subdivisions of the adult zebrafish pallium based on molecular marker analysis. F1000Res (3):1–20.  https://doi.org/10.12688/f1000research.5595.1CrossRefGoogle Scholar
  33. Giassi ACC, Duarte TT, Ellis W et al (2012a) Organization of the gymnotiform fish pallium in relation to learning and memory: II. Extrinsic connections. J Comp Neurol 520(15):3338–3368.  https://doi.org/10.1002/cne.23109CrossRefPubMedGoogle Scholar
  34. Giassi ACC, Ellis W, Maler L (2012b) Organization of the gymnotiform fish pallium in relation to learning and memory: III. Intrinsic connections. J Comp Neurol 520(15):3369–3394.  https://doi.org/10.1002/cne.23108CrossRefPubMedGoogle Scholar
  35. Giassi ACC, Harvey-Girard E, Valsamis B et al (2012c) Organization of the gymnotiform fish pallium in relation to learning and memory: I. Cytoarchitectonics and cellular morphology. J Comp Neurol 520(15):3314–3337.  https://doi.org/10.1002/cne.23097CrossRefPubMedGoogle Scholar
  36. Gordon G, Kaplan DM, Lankow B et al (2011) Toward an integrated approach to perception and action: conference report and future directions. Front Syst Neurosci 5(20):1–6.  https://doi.org/10.3389/fnsys.2011.00020CrossRefGoogle Scholar
  37. Graff C, Kaminski G, Gresty M et al (2004) Fish perform spatial pattern recognition and abstraction by exclusive use of active electrolocation. Curr Biol 14(9):818–823.  https://doi.org/10.1016/j.cub.2004.04.039CrossRefPubMedGoogle Scholar
  38. Grandel H, Kaslin J, Ganz J et al (2006) Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev Biol 295(1):263–277.  https://doi.org/10.1016/j.ydbio.2006.03.040CrossRefPubMedGoogle Scholar
  39. Hafting T, Fyhn M, Molden S et al (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436(7052):801–806.  https://doi.org/10.1038/nature03721CrossRefPubMedGoogle Scholar
  40. Harvey-Girard E, Giassi ACC, Ellis W et al (2012) Organization of the gymnotiform fish pallium in relation to learning and memory: IV. Expression of conserved transcription factors and implications for the evolution of dorsal telencephalon. J Comp Neurol 520(15):3395–3413.  https://doi.org/10.1002/cne.23107CrossRefPubMedGoogle Scholar
  41. Heiligenberg W (1973a) Electrolocation of objects in the electric fish Eigenmannia (Rhamphichthyidae, Gymnotoidei). J Comp Physiol 87(2):137–164.  https://doi.org/10.1007/BF01352158CrossRefGoogle Scholar
  42. Heiligenberg W (1973b) “Electromotor” response in the electric fish Eigenmannia (Rhamphichthyidae, Gymnotoidei). Nature 243(5405):301–302.  https://doi.org/10.1038/243301a0CrossRefGoogle Scholar
  43. Heiligenberg W (1980) The evaluation of electroreceptive feedback in a gymnotoid fish with pulse-type electric organ discharges. J Comp Physiol – A 138(2):173–185.  https://doi.org/10.1007/BF00680441CrossRefGoogle Scholar
  44. Hofmann V, Sanguinetti-Scheck JI, Gómez-Sena L et al (2013a) From static electric images to electric flow: towards dynamic perceptual cues in active electroreception. J Physiol Paris 107(1–2):95–106.  https://doi.org/10.1016/j.jphysparis.2012.06.003CrossRefPubMedGoogle Scholar
  45. Hofmann V, Sanguinetti-Scheck JI, Kunzel S et al (2013b) Sensory flow shaped by active sensing: sensorimotor strategies in electric fish. J Exp Biol 216(13):2487–2500.  https://doi.org/10.1242/jeb.082420CrossRefPubMedGoogle Scholar
  46. Hofmann V, Sanguinetti-Scheck JI, Gómez-Sena L et al (2017) Sensory flow as a basis for a novel distance cue in freely behaving electric fish. J Neurosci 37(2):302–312.  https://doi.org/10.1523/JNEUROSCI.1361-16.2017CrossRefPubMedPubMedCentralGoogle Scholar
  47. Ikenaga T, Yoshida M, Uematsu K (2006) Cerebellar efferent neurons in teleost fish. Cerebellum 5(4):268–274.  https://doi.org/10.1080/14734220600930588CrossRefPubMedGoogle Scholar
  48. Isa T, Sasaki S (2002) Brainstem control of head movements during orienting; Organization of the premotor circuits. Prog Neurobiol l66:205–241.  https://doi.org/10.1016/S0301-0082(02)00006-0CrossRefGoogle Scholar
  49. Ishikawa Y, Yamamoto N, Yoshimoto M et al (2007) Developmental origin of diencephalic sensory relay nuclei in teleosts. Brain Behav Evol 69(2):87–95.  https://doi.org/10.1159/000095197CrossRefPubMedGoogle Scholar
  50. Ito H, Yamamoto N (2009) Non-laminar cerebral cortex in teleost fishes? Biol Lett 5(1):117–121.  https://doi.org/10.1098/rsbl.2008.0397CrossRefPubMedGoogle Scholar
  51. Jun JJ, Longtin A, Maler L (2014) Enhanced sensory sampling precedes self-initiated locomotion in an electric fish. J Exp Biol 217(20):3615–3628.  https://doi.org/10.1242/jeb.105502CrossRefPubMedGoogle Scholar
  52. Jun JJ, Longtin A, Maler L (2016) Active sensing associated with spatial learning reveals memory-based attention in an electric fish. J Neurophysiol 115(5):2577–2592.  https://doi.org/10.1152/jn.00979.2015CrossRefPubMedPubMedCentralGoogle Scholar
  53. Jung SN, Künzel S, Engelmann J (2019) Spatial learning through active electroreception in Gnathonemus petersii. Anim Behav 156:1–10. https://doi.org/10.1016/j.anbehav.2019.06.029CrossRefGoogle Scholar
  54. Knaden M (2006) Ant navigation: resetting the path integrator. J Exp Biol 209(1):26–31.  https://doi.org/10.1242/jeb.01976CrossRefPubMedGoogle Scholar
  55. Lewis JE, Maler L (2001) Neuronal population codes and the perception of object distance in weakly electric fish. J Neurosci 21(8):2842–2850CrossRefGoogle Scholar
  56. Lissmann HW (1951) Continuous electrical signals from the tail of a fish, Gymnarchus niloticus Cuv. Nature 167(4240):201–202.  https://doi.org/10.1038/167201a0CrossRefGoogle Scholar
  57. Lissmann HW (1958) On the function and evolution of electric organs in fish. J Exp Biol 35(1):156–191Google Scholar
  58. Lissmann HW, Machin KE (1958) The mechanism of object location in Gymnarchus niloticus and similar fish. J Exp Biol 35:451–486Google Scholar
  59. MacIver MA, Sharabash NM, Nelson ME (2001) Prey-capture behavior in gymnotid electric fish: motion analysis and effects of water conductivity. J Exp Biol 204(3):543–557PubMedGoogle Scholar
  60. Marr D (1969) A theory of cerebellar cortex. J Physiol 202(2):437–470.  https://doi.org/10.1113/jphysiol.1969.sp008820CrossRefPubMedPubMedCentralGoogle Scholar
  61. McNaughton BL, Battaglia FP, Jensen O et al (2006) Path integration and the neural basis of the “cognitive map”. Nat Rev Neurosci 7(8):663–678.  https://doi.org/10.1038/nrn1932CrossRefPubMedGoogle Scholar
  62. Meek J, Joosten HW (1993) Tyrosine hydroxylase-immunoreactive cell groups in the brain of the teleost fish Gnathonemus petersii. J Chem Neuroanat 6(6):431–446CrossRefGoogle Scholar
  63. Meek J, Nieuwenhuys R (1998) Holosteans and teleosts. In: Nieuwenhuys R, Donkelaar, H J ten, Nicholson, C (eds) The central nervous system of vertebrates. Springer, Berlin, Heidelberg, p 759–937. doi: https://doi.org/10.1007/978-3-642-18262-4_15CrossRefGoogle Scholar
  64. Meredith MA, Stein BE (1996) Spatial determinants of multisensory integration in cat superior colliculus neurons. J Neurophysiol 75(5):1843–1857.  https://doi.org/10.1152/jn.1996.75.5.1843CrossRefPubMedGoogle Scholar
  65. Meredith MA, Nemitz JW, Stein BE (1987) Determinants of multisensory integration in superior colliculus neurons. I. Temporal factors. J Neurosci 7(10):3215–3229CrossRefGoogle Scholar
  66. Migliaro A, Caputi AA, Budelli R (2005) Theoretical analysis of pre-receptor image conditioning in weakly electric fish. PLoS Comput Biol 1(2):e16.  https://doi.org/10.1371/journal.pcbi.0010016CrossRefPubMedCentralGoogle Scholar
  67. Mittelstaedt H, Mittelstaedt ML (1982) Homing by path integration. In: Papi F, Wallraff HG (eds) Avian navigation. Springer, Berlin, Heidelberg, pp 290–297.  https://doi.org/10.1007/978-3-642-68616-0_29CrossRefGoogle Scholar
  68. Moller P (2003) Multimodal sensory integration in weakly electric fish: a behavioral account. J Physiol Paris 96(5–6):547–556.  https://doi.org/10.1016/S0928-4257(03)00010-XCrossRefGoogle Scholar
  69. Moller P, Serrier J, Belbenoit P et al (1979) Notes on ethology and ecology of the Swashi River mormyrids (Lake Kainji, Nigeria). Behav Ecol Sociobiol 4:357–368CrossRefGoogle Scholar
  70. Monaco JD, Rao G, Roth ED et al (2014) Attentive scanning behavior drives one-trial potentiation of hippocampal place fields. Nat Neurosci 17(5):725–731.  https://doi.org/10.1038/nn.3687CrossRefPubMedPubMedCentralGoogle Scholar
  71. Mueller T, Wullimann MF (2009) An evolutionary interpretation of teleostean forebrain anatomy. Brain Behav Evol 74(1):30–42.  https://doi.org/10.1159/000229011CrossRefGoogle Scholar
  72. Mueller T, Dong Z, Berberoglu M et al (2011) The dorsal pallium in zebrafish, Danio rerio (Cyprinidae, Teleostei). Brain Res 49:95–105.  https://doi.org/10.1016/j.brainres.2010.12.089CrossRefGoogle Scholar
  73. Murray EA, Wise SP (2004) What, if anything, is the medial temporal lobe, and how can the amygdala be part of it if there is no such thing? Neurobiol Learn Mem 82(3):178–198.  https://doi.org/10.1016/j.nlm.2004.05.005CrossRefPubMedGoogle Scholar
  74. Murray EA, Wise SP, Graham KS (2017) Representational specializations of the hippocampus in phylogenetic perspective. Neurosci Lett 680:4–12.  https://doi.org/10.1016/j.neulet.2017.04.065CrossRefPubMedPubMedCentralGoogle Scholar
  75. Nelson ME, MacIver MA (1999) Prey capture in the weakly electric fish Apteronotus albifrons: sensory acquisition strategies and electrosensory consequences. J Exp Biol 202(10):1195–1203Google Scholar
  76. Nieuwenhuys R (1963) The comparative anatomy of the actinopterygian forebrain. J Hirnforsch 6:171–192Google Scholar
  77. Nieuwenhuys R (2009) The forebrain of actinopterygians revisited. Brain Behav Evol 73(4):229–252.  https://doi.org/10.1159/000225622CrossRefPubMedGoogle Scholar
  78. Northcutt RG (2008) Forebrain evolution in bony fishes. Brain Res Bull 75(2–4):191–205.  https://doi.org/10.1016/j.brainresbull.2007.10.058CrossRefPubMedGoogle Scholar
  79. O’Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34(1):171–175.  https://doi.org/10.1016/0006-8993(71)90358-1CrossRefPubMedPubMedCentralGoogle Scholar
  80. O’Keefe J, Nadel L (1979) The Hippocampus as a cognitive map. Clarendon Press, OxfordCrossRefGoogle Scholar
  81. Ocaña FM, Uceda S, Arias JL et al (2017) Dynamics of goldfish subregional hippocampal pallium activity throughout spatial memory formation. Brain Behav Evol 90(2):154–170.  https://doi.org/10.1159/000478843CrossRefPubMedGoogle Scholar
  82. Odling-Smee L, Simpson SD, Braithwaite VA (2006) The role of learning in fish orientation. In: Brown C, Laland KN, Krause J (eds) Fish cognition and behavior. Blackwell Publishing Ltd., pp 119–137Google Scholar
  83. Pedraja F, Hofmann V, Lucas K et al (2018) Motion parallax in electric sensing. PNAS 115(3):573–577.  https://doi.org/10.1073/pnas.1712380115CrossRefPubMedGoogle Scholar
  84. Pluta SR, Kawasaki M (2008) Multisensory enhancement of electromotor responses to a single moving object. J Exp Biol 211(Pt 18):2919–2930.  https://doi.org/10.1242/jeb.016154CrossRefPubMedGoogle Scholar
  85. Portavella M, Torres B, Salas C et al (2004) Lesions of the medial pallium, but not of the lateral pallium, disrupt spaced-trial avoidance learning in goldfish (Carassius auratus). Neurosci Lett 362(2):75–78.  https://doi.org/10.1016/j.neulet.2004.01.083CrossRefGoogle Scholar
  86. Post N, von der Emde G (1999) The “novelty response” in an electric fish: response properties and habituation. Physiol Behav 68(1–2):115–128CrossRefGoogle Scholar
  87. Postlethwaite CM, Psemeneki TM, Selimkhanov J et al (2009) Optimal movement in the prey strikes of weakly electric fish: a case study of the interplay of body plan and movement capability. J Royal Soc Interface 6(34):417–433.  https://doi.org/10.1098/rsif.2008.0286CrossRefGoogle Scholar
  88. Poteser M, Kral K (1995) Visual distance discrimination between stationary targets in praying-mantis - an index of the use of motion parallax. J Exp Biol 198(10):2127–2137PubMedGoogle Scholar
  89. Prechtl JC, von der Emde G, Wolfart J et al (1998) Sensory processing in the pallium of a mormyrid fish. J Neurosci 18(18):7381–7393CrossRefGoogle Scholar
  90. Rasnow B (1996) The effects of simple objects on the electric field of Apteronotus. J Comp Physiol A 78(3):397–411.  https://doi.org/10.1007/BF00193977
  91. Rochefort C, Lefort J, Rondi-Reig L (2013) The cerebellum: a new key structure in the navigation system. Front Neural Circuits 7:1–12.  https://doi.org/10.3389/fncir.2013.00035CrossRefGoogle Scholar
  92. Rodriguez F, Durán E, Vargas JP et al (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.  https://doi.org/10.3758/BF03209160CrossRefGoogle Scholar
  93. Rodríguez F, López JC, Vargas JP et al (2002) Conservation of spatial memory function in the pallial forebrain of reptiles and ray-finned fishes. J Neurosci 22(7):2894–2903CrossRefGoogle Scholar
  94. Rodriguez F, Broglio C, Durán E et al (2006) Neural mechanisms of learning in teleost fish. In: Brown C, Laland K, Krause J (eds) Fish cognition and behavior. Blackwell Publishing Ltd., pp 243–277Google Scholar
  95. Rojas R, Moller P (2002) Multisensory contributions to the shelter-seeking behavior of a mormyrid fish, Gnathonemus petersii Günther (mormyridae, teleostei): the role of vision, and the passive and active electrosenses. Brain Behav Evol 59(4):211–221.  https://doi.org/10.1159/000064908
  96. Rolls ET (2016) Pattern separation, completion, and categorisation in the hippocampus and neocortex. Neurobiol Learn Mem 129:4–28.  https://doi.org/10.1016/j.nlm.2015.07.008CrossRefPubMedGoogle Scholar
  97. Rooney DJ, New JG, Szabo T et al (1989) Central connections of the olfactory bulb in the weakly electric fish, Gnathonemus petersii. Cell Tissue Res 257(2):423–436.  https://doi.org/10.1007/BF00261845CrossRefGoogle Scholar
  98. Rowin J, Meriggioli MN (2007) Proprioception, touch, and vibratory sensation. In: Textbook of clinical neurology. Elsevier, pp 343–361.  https://doi.org/10.1016/B978-141603618-0.10019-0CrossRefGoogle Scholar
  99. Salas C, Broglio C, Rodríguez F et al (1996a) Telencephalic ablation in goldfish impairs performance in a “spatial constancy” problem but not in a cued one. Behav Brain Res 79(1–2):193–200CrossRefGoogle Scholar
  100. Salas C, Rodríguez F, Vargas JP et al (1996b) Spatial learning and memory deficits after telencephalic ablation in goldfish trained in place and turn maze procedures. Behav Neurosci 110(5):965–980.  https://doi.org/10.1037/0735-7044.110.5.965CrossRefPubMedGoogle Scholar
  101. 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.  https://doi.org/10.1159/000072438CrossRefPubMedGoogle Scholar
  102. Salas C, Broglio C, Durán E et al (2006) Neuropsychology of learning and memory in teleost fish. Zebrafish 3(2):157–171.  https://doi.org/10.1089/zeb.2006.3.157CrossRefPubMedGoogle Scholar
  103. Salazar VL, Krahe R, Lewis JE (2013) The energetics of electric organ discharge generation in gymnotiform weakly electric fish. J Exp Biol 216(13):2459–2468.  https://doi.org/10.1242/jeb.082735CrossRefGoogle Scholar
  104. Sas E, Maler L, Weld M (1993) Connections of the olfactory bulb in the gymnotiform fish, Apteronotus leptorhynchus. J Comp Neurol 335(4):486–507.  https://doi.org/10.1002/cne.903350403CrossRefGoogle Scholar
  105. Schumacher S, Burt de Perera T, Thenert J et al (2016) Cross-modal object recognition and dynamic weighting of sensory inputs in a fish. PNAS 113(27):7638–7643.  https://doi.org/10.1073/pnas.1603120113CrossRefPubMedGoogle Scholar
  106. Schumacher S, von der Emde G, Burt de Perera T (2017) Sensory influence on navigation in the weakly electric fish Gnathonemus petersii. Anim Behav 132:1–12.  https://doi.org/10.1016/j.anbehav.2017.07.016CrossRefGoogle Scholar
  107. Sim M, Kim D (2011) Electrolocation based on tail-bending movements in weakly electric fish. J Exp Biol 214(Pt 14):2443–2450.  https://doi.org/10.1242/jeb.052308CrossRefPubMedGoogle Scholar
  108. Snyder JB, Nelson ME, Burdick JW et al (2007) Omnidirectional sensory and motor volumes in electric fish. PLoS Biol 5(11):e301.  https://doi.org/10.1371/journal.pbio.0050301CrossRefPubMedPubMedCentralGoogle Scholar
  109. Sokolov EN (1990) The orienting response, and future directions of its development. Pavlov J Biol Sci 25(3):142–150PubMedGoogle Scholar
  110. Stanford TR, Quessy S, Stein BE (2005) Evaluating the operations underlying multisensory integration in the cat superior colliculus. J Neurosci 13(25):6499–6508.  https://doi.org/10.1523/JNEUROSCI.5095-04.2005CrossRefGoogle Scholar
  111. Taube JS (2007) The head direction signal: origins and sensory-motor integration. Annu Rev Neurosci 30(1):181–207.  https://doi.org/10.1146/annurev.neuro.29.051605.112854CrossRefPubMedGoogle Scholar
  112. Torres B, Luque MA, Pérez-Pérez MP et al (2005) Visual orienting response in goldfish: a multidisciplinary study. Brain Res Bull 66(4–6):376–380.  https://doi.org/10.1016/j.brainresbull.2005.02.002CrossRefPubMedGoogle Scholar
  113. Trinh AT, Harvey-Girard E, Teixeira F et al (2016) Cryptic laminar and columnar organization in the dorsolateral pallium of a weakly electric fish. J Comp Neurol 524(2):408–428.  https://doi.org/10.1002/cne.23874CrossRefPubMedGoogle Scholar
  114. Vargas JP, López JC, Portavella M (2009) What are the functions of fish brain pallium? Brain Res Bull 79(6):436–440.  https://doi.org/10.1016/j.brainresbull.2009.05.008CrossRefPubMedGoogle Scholar
  115. von der Emde G, Bleckmann H (1998) Finding food: senses involved in foraging for insect larvae in the electric fish Gnathonemus petersii. J Exp Biol 201(1):969–980Google Scholar
  116. von der Emde G, Prechtl JC (1999) Anatomical connections of auditory and lateral line areas of the dorsal telencephalon (Dm) in the osteoglossomorph teleost, Gnathonemus petersii. Brain Res 818(2):355–367Google Scholar
  117. von der Emde G, Schwarz S (2002) Imaging of objects through active electrolocation in Gnathonemus petersii. J Physiol Paris 96(5–6):431–444.  https://doi.org/10.1016/S0928-4257(03)00021-4CrossRefGoogle Scholar
  118. von der Emde G, Schwarz S, Gomez L et al (1998) Electric fish measure distance in the dark. Nature 395(6705):890–894.  https://doi.org/10.1038/27655CrossRefPubMedGoogle Scholar
  119. von der Emde G, Behr K, Bouton B et al (2010) 3-dimensional scene perception during active electrolocation in a weakly electric pulse fish. Front Behav Neurosci 4(26):1–13.  https://doi.org/10.3389/fnbeh.2010.00026CrossRefGoogle Scholar
  120. Vonderschen K, Bleckmann H, Hofmann MH (2002) A direct projection from the cerebellum to the telencephalon in the goldfish, Carassius auratus. Neurosci Lett 320(1–2):37–40.  https://doi.org/10.1016/S0304-3940(02)00022-8CrossRefGoogle Scholar
  121. Wallace DG, Hines DJ, Pellis SM et al (2002) Vestibular information is required for dead reckoning in the rat. J Neurosci 22(22):10009–10017CrossRefGoogle Scholar
  122. Wallach A, Harvey-Girard E, Jun JJ et al (2018) A time-stamp mechanism may provide temporal information necessary for egocentric to allocentric spatial transformations. elife;7:e36769. https://doi.org/10.7554/eLife.36769
  123. Walton AG, Moller P (2010) Maze learning and recall in a weakly electric fish, Mormyrus rume proboscirostris Boulenger (Mormyridae, Teleostei). Ethology 116(10):904–919.  https://doi.org/10.1111/j.1439-0310.2010.01807.xCrossRefGoogle Scholar
  124. Wolpert DM, Landy MS (2012) Motor control is decision-making. Curr Opin Neurobiol 22(6):996–1003.  https://doi.org/10.1016/j.conb.2012.05.003CrossRefPubMedPubMedCentralGoogle Scholar
  125. Wullimann MF, Mueller T (2004) Teleostean and mammalian forebrains contrasted: evidence from genes to behavior. J Comp Neurol 475(2):143–162.  https://doi.org/10.1002/cne.20183CrossRefPubMedGoogle Scholar
  126. Wullimann MF, Northcutt RG (1990) Visual and electrosensory circuits of the diencephalon in mormyrids: an evolutionary perspective. J Comp Neurol 297(4):537–552.  https://doi.org/10.1002/cne.902970407CrossRefPubMedGoogle Scholar
  127. Wullimann MF, Rooney DJ (1990) A direct cerebello-telencephalic projection in an electrosensory mormyrid fish. Brain Res 520(1–2):354–357.  https://doi.org/10.1016/0006-8993(90)91730-5CrossRefPubMedGoogle Scholar
  128. Yamamoto K, Bloch S, Vernier P (2017) New perspective on the regionalization of the anterior forebrain in Osteichthyes. Develop Growth Differ 59(4):175–187.  https://doi.org/10.1111/dgd.12348CrossRefGoogle Scholar
  129. Yassa MA, Stark CEL (2011) Pattern separation in the hippocampus. Trends Neurosci 34(10):515–525.  https://doi.org/10.1016/j.tins.2011.06.006CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.AG Active Sensing, University of Bielefeld, UHG W3-268BielefeldGermany
  2. 2.AG Active Sensing and Center of Excellence Cognitive Interaction TechnologyUniversity of Bielefeld, UHG W3-268BielefeldGermany

Personalised recommendations