Advertisement

Brain Structure and Function

, Volume 223, Issue 9, pp 3975–4003 | Cite as

Immediate early gene expression related to learning and retention of a visual discrimination task in bamboo sharks (Chiloscyllium griseum)

  • Theodora FussEmail author
  • Vera Schluessel
Original Article
  • 107 Downloads

Abstract

Using the expression of the immediate early gene (IEG) egr-1 as a neuronal activity marker, brain regions potentially involved in learning and long-term memory functions in the grey bamboo shark were assessed with respect to selected visual discrimination abilities. Immunocytochemistry revealed a significant up-regulation of egr-1 expression levels in a small region of the telencephalon of all trained sharks (i.e., ‘early’ and ‘late learners’, ‘recallers’) when compared to three control groups (i.e., ‘controls’, ‘undisturbed swimmers’, ‘constant movers’). There was also a well-defined difference in egr-1 expression patterns between the three control groups. Additionally, some staining was observed in diencephalic and mesencephalic sections; however, staining here was weak and occurred only irregularly within and between groups. Therefore, it could have either resulted from unintentional cognitive or non-cognitive inducements (i.e., relating to the mental processes of perception, learning, memory, and judgment, as contrasted with emotional and volitional processes) rather than being a training effect. Present findings emphasize a relationship between the training conditions and the corresponding egr-1 expression levels found in the telencephalon of Chiloscyllium griseum. Results suggest important similarities in the neuronal plasticity and activity-dependent IEG expression of the elasmobranch brain with other vertebrate groups. The presence of the egr-1 gene seems to be evolutionarily conserved and may therefore be particularly useful for identifying functional neural responses within this group.

Keywords

Immediate early gene (IEG) egr-1 Immunocytochemistry Shark Learning Memory retention 

Notes

Acknowledgements

We would like to thank Dr. N. Krützfeldt and K. Stehr laboratory support and S. Braun for animal care taking and maintenance. We specifically thank C. Scharff and A. Nshdejan as well as T. Ruhl for help with the IEG protocols and procedures. We would also like to thank the anonymous reviewers for their expert comments, which helped to improve our manuscript. The research reported herein was performed under the guidelines established by the current German animal protection law and had been approved by the Landesamt für Natur, Umwelt und Verbraucherschutz NRW (Approval number 8.87-50.10.37.09.198). Funding was provided by a grant of the Deutsche Forschungsgemeinschaft (DFG) to Dr. Vera Schluessel (Grant number SCHL 1919/4-1).

Funding

Funding was provided by a grant of the Deutsche Forschungsgemeinschaft (DFG) to Dr. Vera Schluessel (Grant number SCHL 1919/4-1).

Compliance with ethical standards

Conflict of interest

Dr. Theodora Fuss declares that she has no conflict of interest. Dr. Vera Schluessel declares that she has no conflict of interest.

Research involving human participants and/or animals

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors. There were no experiments involving humans or human material. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The research reported on bamboo sharks was performed under the guidelines established by the current German animal protection law and had been approved by the Landesamt für Natur, Umwelt und Verbraucherschutz NRW (Approval number 8.87-50.10.37.09.198).

Informed consent

This article does not contain any studies with human participants performed by any of the authors. There were no experiments involving humans or human material.

References

  1. Abraham WC, Demmer J, Richardson CL, Williams JM, Lawlor PA, Mason SE et al (1993) Correlation between immediate early gene induction and persistence of LTP. Neuroscience 56:717–727PubMedGoogle Scholar
  2. Alcock J (2006) Animal behavior—an evolutionary approach, 8th edn. Elsevier, Munich, pp 88–89Google Scholar
  3. Anadón R, Rodríguez-Moldes I, Adrio F (2013) Glycine-immunoreactive neurons in the brain of a shark (Scyliorhinus canicula L.). J Comp Neurol 521(13):3057–3082PubMedGoogle Scholar
  4. Anokhin K, Mileusnic R, Shamakina I, Rose S (1991) Effects of early experience on c-fos gene expression in the chick forebrain. Brain Res 544(1):101–107PubMedGoogle Scholar
  5. Baraban S, Taylor M, Castro P, Baier H (2005) Pentylenetetrazole induced changes in zebrafish behavior, neural activity and c-fos expression. Neuroscience 131(3):759–768PubMedGoogle Scholar
  6. Baumgärtel K, Genoux D, Welzl H, Tweedie-Cullen RY, Koshibu K, Livingstone-Zatchej M, Mamie C, Mansuy IM (2008) Control of the establishment of aversive memory by calcineurin and Zif268. Nat Neurosci 11(5):572–578PubMedGoogle Scholar
  7. Beckmann AM, Wilce PA (1997) Egr transcription factors in the nervous system. Neurochem Int 31:477–510PubMedGoogle Scholar
  8. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361(6407):31–39Google Scholar
  9. Bodznick D (1990) Elasmobranch vision: multimodal integration in the brain. J Exp Zool 256(S5):108–116Google Scholar
  10. Bolhuis JJ, Zijlstra GO, den Boer-Visser AM, Van der Zee EA (2000) Localised neuronal activation in the zebra finch brain is related to the strength of song learning. Proc Natl Acad Sci USA 97:2282–2285PubMedGoogle Scholar
  11. Bosch TJ, Maslam S, Roberts BL (1995) A polyclonal antibody against mammalian FOS can be used as a cytoplasmic neuronal-activity marker in a teleost fish. J Neurosci Methods 58:173–179PubMedGoogle Scholar
  12. Bosch TJ, Maslam S, Roberts BL (2001) Fos-like immunohistochemical identification of neurons active during the startle response of the rainbow trout. J Comp Neurol 439:306–314PubMedGoogle Scholar
  13. Bozon B, Davis S, Laroche S (2002) Regulated transcription of the immediate-early gene Zif268: mechanisms and gene dosage-dependent function in synaptic plasticity and memory formation. Hippocampus 12(5):570–577PubMedGoogle Scholar
  14. Bozon B, Davis S, Laroche S (2003a) A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval. Neuron 40(4):695–701PubMedGoogle Scholar
  15. Bozon B, Kelly A, Josselyn SA, Silva AJ, Davis S, Laroche S (2003b) MAPK, CREB and zif268 are all required for the consolidation of recognition memory. Philos Trans R Soc B Biol Sci 358(1432):805–814Google Scholar
  16. Brown TH, Chattarji S (1994) Hebbian synaptic plasticity: evolution of the contemporary concept. In: Domany PE, Hemmen PD, Schulten PK (eds) Models of neural networks, physics of neural networks. Springer, New York, pp 287–314Google Scholar
  17. Burmeister SS, Fernald RD (2005) Evolutionary conservation of the egr-1 immediate-early gene response in a teleost. J Comp Neurol 481(2):220–232PubMedGoogle Scholar
  18. Burmeister S, Jarvis E, Fernald R (2005) Rapid behavioral and genomic responses to social opportunity. PLoS Biol 3(11):e363PubMedPubMedCentralGoogle Scholar
  19. Cao XM, Koski RA, Gashler A, McKiernan M, Morris CF, Gaffney R, Hay RV, Sukhatme VP (1990) Identification and characterization of the Egr-1 gene product, a DNA-binding zinc finger protein induced by differentiation and growth signals. Mol Cell Biol 10(5):1931–1939PubMedPubMedCentralGoogle Scholar
  20. Carrera I, Molist P, Anadón R, Rodríguez-Moldes I (2008) Development of the serotoninergic system in the central nervous system of a shark, the lesser spotted dogfish Scyliorhinus canicula. J Comp Neurol 511(6):804–831PubMedGoogle Scholar
  21. Clark E (1959) Instrumental conditioning of lemon sharks. Science 130(3369):217–218PubMedGoogle Scholar
  22. Clayton DF (1997) Role of gene regulation in song circuit development and song learning. J Neurobiol 33:549–571PubMedGoogle Scholar
  23. Collin SP (2012) The neuroecology of cartilaginous fishes: sensory strategies for survival. Brain Behav Evol 80:80–96PubMedGoogle Scholar
  24. Crino P, Khodakhah K, Becker K, Ginsberg S, Hemby S, Eberwine J (1998) Presence and phosphorylation of transcription factors in developing dendrites. Proc Natl Acad Sci 95(5):2313–2318PubMedGoogle Scholar
  25. Davis S, Bozon B, Laroche S (2003) How necessary is the activation of the immediate early gene zif268 in synaptic plasticity and learning? Behav Brain Res 142(1–2):17–30PubMedGoogle Scholar
  26. Day ML, Fahrner TJ, Aykent S, Milbrandt J (1990) The zinc finger protein NGFI-A exists in both nuclear and cytoplasmic forms in nerve growth factor-stimulated PC12 cells. J Biol Chem 265(25):15253–15260PubMedGoogle Scholar
  27. Ding L, Perkel DJ (2004) Long-term potentiation in an avian basal ganglia nucleus essential for vocal learning. J Neurosci 24(2):488–494PubMedGoogle Scholar
  28. Dragunow M (1996) A role for immediate early transcription factors in learning and memory. Behav Genet 20:293–299Google Scholar
  29. Dragunow M, Faull R (1989) The use of c-fos as metabolic marker in neuronal pathway tracing. J Neurosci Methods 29:261–265PubMedGoogle Scholar
  30. Dragunow M, Robertson HA (1987a) Generalized seizures induce c-fos protein(s) in mammalian neurons. Neurosci Lett 82:157–161PubMedGoogle Scholar
  31. Dragunow M, Robertson HA (1987b) Kindling stimulation induces c-fos protein(s) in granule cells of the rat dentate gyrus. Nature 329:441–442PubMedGoogle Scholar
  32. Dragunow M, Robertson HA, Robertson GS (1988) Amygdala kindling and c-fos protein. Exp Neurol 102(2):261–263PubMedGoogle Scholar
  33. Ebbesson SOE (1972) New insights into the organization of the shark brain. Comp Biochem Physiol 42:121–129Google Scholar
  34. Ebbesson SOE (1980) On the organization of the telencephalon in elasmobranchs. In: Ebbesson SOE (ed) Comparative neurology of the telencephalon. Springer, Boston, MAGoogle Scholar
  35. Ebbesson SOE, Heimer L (1970) Projections of the olfactory tract fibers in the nurse sharks (Ginglymostoma cirratum). Brain Res 17:47–55PubMedGoogle Scholar
  36. Ebbesson SOE, Schroeder DM (1971) Connections of the nurse shark’s telencephalon. Science 173:254–256PubMedGoogle Scholar
  37. Eichenbaum H (2000) A cortical–hippocampal system for declarative memory. Nat Rev Neurosci 1(1):41PubMedGoogle Scholar
  38. Ferreiro-Galve S, Carrera I, Candal E, Villar-Cheda B, Anadón R, Mazan S, Rodríguez-Moldes I (2008) The segmental organization of the developing shark brain based on neurochemical markers, with special attention to the prosencephalon. Brain Res Bull 75(2):236–240PubMedGoogle Scholar
  39. Fiebig E, Bleckmann H (1989) Cell groups afferent to the telencephalon in a cartilaginous fish (Platyrhinoidis triseriata). A WGA-HRP study. Neurosci Lett 105:57–62PubMedGoogle Scholar
  40. Frankland PW, Bontempi B (2005) The organization of recent and remote memories. Nat Rev Neurosci 6(2):119–130PubMedPubMedCentralGoogle Scholar
  41. Frey U, Krug M, Reymann KG, Matthies H (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452(1–2):57–65PubMedGoogle Scholar
  42. Fujikawa Y, Kozono K, Esaka M, Iijima N, Nagamatsu Y, Yoshida M, Uematsu K (2006) Molecular cloning and effect of c-fos mRNA on pharmacological stimuli in the goldfish brain. Comp Biochem Physiol D Genom Proteom 1(2):253–259Google Scholar
  43. Fuss T, Schluessel V (2015) Something worth remembering: visual discrimination in sharks. Anim Cogn 18(2):463–471PubMedGoogle Scholar
  44. Fuss T, Bleckmann H, Schluessel V (2014a) The shark Chiloscyllium griseum can orient using turn responses before and after partial telencephalon ablation. J Comp Physiol A 200:19–35Google Scholar
  45. Fuss T, Bleckmann H, Schluessel V (2014b) Place learning prior to and after telencephalon ablation in bamboo and coral cat sharks (Chiloscyllium griseum and Atelomycterus marmoratus). J Comp Physiol A 200:37–52Google Scholar
  46. Fuss T, Bleckmann H, Schluessel V (2014c) Visual discrimination abilities in grey bamboo sharks (Chiloscyllium griseum). Zoology 117:104–111PubMedGoogle Scholar
  47. Fuss T, Bleckmann H, Schluessel V (2014d) The brain creates illusions not just for us: turns out sharks (Chiloscyllium griseum) can ‘see the magic’ as well. Front Neural Circuits 8:24.  https://doi.org/10.3389/fncir.2014.00024 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Gashler AL, Swaminathan SOWMYA, Sukhatme VP (1993) A novel repression module, an extensive activation domain, and a bipartite nuclear localization signal defined in the immediate-early transcription factor Egr-1. Mol Cell Biol 13(8), 4556–4571PubMedPubMedCentralGoogle Scholar
  49. Glanzman DL (1995) The cellular basis of classical conditioning in Aplysia californica—it’s less simple than you think. Trends Neurosci 18(1):30–36PubMedGoogle Scholar
  50. Goelet P, Castellucci VF, Schacher S, Kandel ER (1986) The long and the short of long-term memory—a molecular framework. Nature 322(6078):419–422PubMedGoogle Scholar
  51. Graeber RC, Ebbesson SO (1972) Visual discrimination learning in normal and tectal-ablated nurse sharks (Ginglymostoma cirratum). Comp Biochem Physiol 42:131–139Google Scholar
  52. Graeber RC, Ebbesson SO, Jane JA (1978) Visual discrimination following partial telencephalic ablations in nurse sharks (Ginglymostoma cirratum). J Comp Neurol 180:325–344PubMedGoogle Scholar
  53. Graeber RC, Ebbesson SO, Jane JA (1973) Visual discrimination in sharks without optic tectum. Science 180(4084):413–415PubMedGoogle Scholar
  54. Gruber SH (1967) A behavioral measurement of dark adaptation in the lemon shark, Negaprion brevirostris. In: Gilbert PW, Mathewson RF, Rall DP (eds) Sharks, skates and rays. Johns Hopkins Press, Baltimore, pp 479–790Google Scholar
  55. Guttridge TL, Brown C (2014) Learning and memory in the Port Jackson shark, Heterodontus portusjacksoni. Anim Cogn 17:415–425PubMedGoogle Scholar
  56. Guzowski JF, Setlow B, Wagner EK, McGaugh JL (2001) Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J Neurosci 21(14):5089–5098PubMedGoogle Scholar
  57. Harvey-Girard E, Tweedle J, Ironstone J, Cuddy M, Ellis W, Maler L (2010) Long-term recognition memory of individual conspecifics is associated with telencephalic expression of Egr-1 in the electric fish Apteronotus leptorhynchus. J Comp Neurol 518(14):2666–2692PubMedGoogle Scholar
  58. Herrero L, Rodríguez F, Salas C, Torres B (1998) Tail and eye movements evoked by electrical microstimulation of the optic tectum in goldfish. Exp Brain Res 120(3):291–305PubMedGoogle Scholar
  59. Heurteaux C, Messier C, estrade C, Lazdunski M (1993) Memory processing and apamin induce immediate early gene expression in mouse brain. Mol Brain Res 3:17–22Google Scholar
  60. Hofmann MH, Northcutt RG (2012) Forebrain organization in elasmobranchs. Brain Behav Evolut 80(2):142–151Google Scholar
  61. Hughes P, Dragunow M (1995) Induction of immediate-early genes and the control of neurotransmitter-regulated gene expression within the nervous system. Pharmacol Rev 47:133–178PubMedGoogle Scholar
  62. Ito H, Vanegas H (1984) Visual receptive thalamopetal neurons in the optic tectum of teleosts (Holocentridae). Brain Res 290(2):201–210PubMedGoogle Scholar
  63. Jarvis ED, Ribeiro S, Da Silva ML, Ventura D, Vielliard J, Mello CV (2000) Behaviorally driven gene expression reveals song nuclei in humming- bird brain. Nature 406:628–632PubMedPubMedCentralGoogle Scholar
  64. Jones MW, Errington ML, French PJ, Fine A, Bliss TVP, Garel S, Charnay P, Bozon B, Laroche S, Davis S (2001) A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci 4(3):289–296PubMedGoogle Scholar
  65. Jones EG, Peters A (eds) (2013) Comparative structure and evolution of cerebral cortex, vol 8. Springer Science & Business Media, Berlin, HeidelbergGoogle Scholar
  66. Kimber JA, Sims DW, Bellamy PH, Gill AB (2014) Elasmobranch cognitive ability: using electroreceptive foraging behaviour to demonstrate learning, habituation and memory in a benthic shark. Anim Cogn 17(1):55–65PubMedGoogle Scholar
  67. Kinoshita M, Hosokawa T, Urano A, Ito E (2004) Long-term potentiation in the optic tectum of rainbow trout. Neurosci Lett 370(2–3):146–150PubMedGoogle Scholar
  68. Knapska E, Kaczmarek L (2004) A gene for neuronal plasticity in the mammalian brain: Zif268/Egr-1/NGFI-A/Krox-24/TIS8/ZENK? Prog Neurobiol 74(4):183–211PubMedGoogle Scholar
  69. Koyano K, Kuba K, Minota S (1985) Long-term potentiation of transmitter release induced by repetitive presynaptic activities in bull-frog sympathetic ganglia. J Physiol 359(1):219–233PubMedPubMedCentralGoogle Scholar
  70. Krug M, Lössner B, Ott T (1984) Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats. Brain Res Bull 13(1):39–42PubMedGoogle Scholar
  71. Lanahan A, Worley P (1998) Immediate-early genes and synaptic function. Neurobiol Learn Mem 70:37–43PubMedGoogle Scholar
  72. Larson JR, Lynch G (1985) Long-term potentiation in lizard cerebral cortex. Soc Neurosci Abstr 11:777Google Scholar
  73. Lau BYB, Mathur P, Gould GG, Guo S (2011) Identification of a brain center whose activity discriminates a choice behavior in zebrafish. Proc Natl Acad Sci USA 108(6):2581–2586PubMedGoogle Scholar
  74. Lee I, Yoganarasimha D, Rao G, Knierim JJ (2004) Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 430(6998):456–459PubMedGoogle Scholar
  75. Lewis D, Teyler TJ (1986) Anti-S-100 serum blocks long-term potentiation in the hippocampal slice. Brain Res 383(1–2):159–164PubMedGoogle Scholar
  76. Luiten P (1981a) Two visual pathways to the telencephalon in the nurse shark (Ginglymostoma cirratum). I. Retinal projections. J Comp Neurol 196:531–538PubMedGoogle Scholar
  77. Luiten P (1981b) Two visual pathways to the telencephalon in the nurse shark (Ginglymostoma cirratum). II. Ascending thalamo-telencephalic connections. J Comp Neurol 196:539–548PubMedGoogle Scholar
  78. Mack K, Day M, Milbrandt J, Gottlieb DI (1990) Localization of the NGFI-A protein in the rat brain. Mol Brain Res 8(2):177–180PubMedGoogle Scholar
  79. Malenka RC, Nicoll RA (1993) NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trends Neurosci 16(12):521–527PubMedGoogle Scholar
  80. Malkani S, Wallace KJ, Donley MP, Rosen JB (2004) An egr-1 (zif268) antisense oligodeoxynucleotide infused into the amygdala disrupts fear conditioning. Learn Mem 11(5):617–624PubMedPubMedCentralGoogle Scholar
  81. Manso M, Anadón R (1993) Golgi study of the telencephalon of the small-spotted dogfish Scyliorhinus canicula L. J Comp Neurol 333(4):485–502PubMedGoogle Scholar
  82. Mansour-Robaey S, Pinganaud G (1996) Development of retino-tectal arborizations in the trout. Anat Embryol 194(3):279–287PubMedGoogle Scholar
  83. Maruska KP, Zhang A, Neboori A, Fernald RD (2013) Social opportunity causes rapid transcriptional changes in the social behaviour network of the brain in an African cichlid fish. J Neuroendocrinol 25(2):145–157PubMedPubMedCentralGoogle Scholar
  84. Matheny C, Day ML, Milbrandt J (1994) The nuclear localization signal of NGFI-A is located within the zinc finger DNA binding domain. J Biol Chem 269(11):8176–8181PubMedGoogle Scholar
  85. Matsuoka I, Fuyuki K, Shoji T, Kurihara K (1998) Identification of c-fos related genes and their induction by neural activation in rainbow trout brain. Biochim Biophys Acta 1395:220–227PubMedGoogle Scholar
  86. Mayer U, Pecchia T, Bigman VP, Flore M, Vallortigara G (2015) Hippocampus and medial striatum dissociation during goal navigation by geometry or features in the domestic chick: an immediate early gene study. Hippocampus 14:1–14Google Scholar
  87. Mello CV, Clayton DF (1994) Song-induced ZENK gene expression in auditory pathways of songbird brain and its relation to the song control system. J Neurosci 14:6652–6666PubMedGoogle Scholar
  88. Mello CV, Vicario DS, Clayton DF (1992) Song presentation induces gene expression in the songbird forebrain. Proc Natl Acad Sci USA 89:6818–6822PubMedGoogle Scholar
  89. Myrberg AA, Banner A, Richard JD (1969) Shark attraction using a video-acoustic system. Mar Biol 2:264–276Google Scholar
  90. Nam RH, Kim W, Lee CJ (2004) NMDA receptor-dependent long-term potentiation in the telencephalon of the zebrafish. Neurosci Lett 370(2–3):248–251PubMedGoogle Scholar
  91. Nguyen PV, Kandel ER (1996) A macromolecular synthesis-dependent late phase of long-term potentiation requiring cAMP in the medial perforant pathway of rat hippocampal slices. J Neurosci 16(10):3189–3198PubMedGoogle Scholar
  92. Nicoll RA (2017) A brief history of long-term potentiation. Neuron 93(2):281–290PubMedGoogle Scholar
  93. Nikolaev E, Werka T, Kaczmarek L (1992) c-Fos protooncogene expression in rat brain after long-term training of two-way active avoidance reaction. Behav Brain Res 48:91–94PubMedGoogle Scholar
  94. Nikonorov SI (1983) Electrophysiological analysis of convergent relations between the olfactory and visual analyzers in the forebrain of Squalus acanthias. J Evol Biochem Physiol 18:268–273Google Scholar
  95. Nikonorov SI, Lukyanov AS (1980) Electrophysiological investigations of visual afferent pathways in the forebrain of Squalus acanthias. J Evol Biochem Physiol 16:132–139Google Scholar
  96. Northcutt RG (1977) Elasmobranch central nervous system organization and its possible evolutionary significance. Integr Comp Biol 17(2):411–429Google Scholar
  97. Northcutt RG (1978) Brain organization in the cartilaginous fishes. In: Hodgson ES, Mathewson RF (eds) Sensory biology of sharks, skates and rays. Office of Naval Research, Arlington, pp 117–193Google Scholar
  98. Northcutt RG, Wathey JC (1979) Some connections of the skate dorsal and medial pallia. Neurosci Abstr 5:145Google Scholar
  99. Okuyama T, Suehiro Y, Imada H, Shimada A, Naruse K, Takeda H, Kubo T, Takeuchi H (2011) Induction of c-fos transcription in the medaka brain (Oryzias latipes) in response to mating stimuli. Biochem Biophys Res Commun 404(1):453–457PubMedGoogle Scholar
  100. Otani S, Abraham WC (1989) Inhibition of protein synthesis in the dentate gyrus, but not the entorhinal cortex, blocks maintenance of long-term potentiation in rats. Neurosci Lett 106(1–2):175–180PubMedGoogle Scholar
  101. Perry B (2002) Childhood experience and the expression of genetic potential: what childhood neglect tells us about nature and nurture. Brain Mind 3:79–100Google Scholar
  102. Poirier R, Cheval H, Mailhes C, Garel S, Charnay P, Davis S, Laroche S (2008) Distinct functions of egr gene family members in cognitive processes. Front Neurosci 2:2Google Scholar
  103. Quintana-Urzainqui I, Sueiro C, Carrera I, Ferreiro-Galve S, Santos-Durán G, Pose-Méndez S, Mazan S, Candal E, Rodríguez-Moldes I (2012) Contributions of developmental studies in the dogfish Scyliorhinus canicula to the brain anatomy of elasmobranchs: in-sights on the basal ganglia. Brain Behav Evol 80:127–141PubMedGoogle Scholar
  104. Rajan KE, Ganesh A, Dharaneedharan S, Radhakrishnan K (2011) Spatial learning-induced egr-1 expression in telencephalon of gold fish Carassius auratus. Fish Physiol Biochem 37(1):153–159PubMedGoogle Scholar
  105. Renaudineau S, Poucet B, Laroche S, Davis S, Save E (2009) Impaired long-term stability of CA1 place cell representation in mice lacking the transcription factor zif268/egr1. Proc Natl Sci 106(28):11771–11775Google Scholar
  106. Rodríguez-Moldes I (2009) A developmental approach to forebrain organization in elasmobranchs: new perspectives on the regionalization of the telencephalon. Brain Behav Evol 74:20–29PubMedGoogle Scholar
  107. Rogan MT, Stäubli UV, LeDoux JE (1997) Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390(6660):604–607PubMedPubMedCentralGoogle Scholar
  108. Rose S (1991) How chicks make memories: the cellular cascade from c-fos to dendritic remodelling. Trends Neurosci 14(9):390–397PubMedGoogle Scholar
  109. Satou M, Anzai S, Huruno M (2005) Long-term potentiation and olfactory memory formation in the carp (Cyprinus carpio L.) olfactory bulb. J Comp Physiol A 191(5):421–434Google Scholar
  110. Schluessel V (2015) Who would have thought that ‘Jaws’ also has brains? Cognitive functions in elasmobranchs. Anim Cogn 18(1):19–37PubMedGoogle Scholar
  111. Schluessel V, Bleckmann H (2012) Spatial learning and memory retention in the grey bamboo shark (Chiloscyllium griseum). Zool 115(6):346–353Google Scholar
  112. Schroeder D, Ebbesson SOE (1974) Nonolfactory telencephalic afferents in the nurse shark (Ginglymostoma cirratum). Brain Behav Evol 9:121–155PubMedGoogle Scholar
  113. Schwarze S, Bleckmann H, Schluessel V (2013) Avoidance conditioning in bamboo sharks (Chiloscyllium griseum and C. punctatum): behavioral and neuroanatomical aspects. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 199:843–856.  https://doi.org/10.1007/s00359-013-0847-1 CrossRefPubMedGoogle Scholar
  114. Schwassmann HO (1968) Visual projection upon the optic tectum in foveate marine teleosts. Vis Res 8(10):1337-N2Google Scholar
  115. Schweitzer J (1983) The physiological and anatomical localization of two electroreceptive diencephalic nuclei in the thornback ray, Platyrhinoidis triseriata. J Comp Physiol A 153:331–341Google Scholar
  116. Schweitzer J, Lowe D (1984) Mesencephalic and diencephalic cobalt-lysine injections in an elasmobranch: evidence for two parallel electrosensory pathways. Neurosci Lett 44:317–322PubMedGoogle Scholar
  117. Scott TRD, Bennett MR (1993) The effect of ions and second messengers on long-term potentiation of chemical transmission in avian ciliary ganglia. Br J Pharmacol 110(1):461–469PubMedPubMedCentralGoogle Scholar
  118. Shiflett MW, Tomaszycki ML, Rankin AZ, DeVoogd TJ (2004) Long-term memory for spatial locations in a food-storing bird (Poecile atricapilla) requires activation of NMDA receptors in the hippocampal formation during learning. Behav Neurosci 118(1):121–130PubMedGoogle Scholar
  119. Shors TJ, Matzel LD (1997) Long-term potentiation: what’s learning got to do with it? Behav Brain Sci 20(4):597–614PubMedGoogle Scholar
  120. Shuttleworth TJ (ed) (1988) Physiology of elasmobranch fishes. Springer-Verlag, New York, USAGoogle Scholar
  121. Smeets W, Boord R (1985) Connections of the lobus inferior hypothalami of the clearnose skate Raja eglanteria (Chondrichthyes). J Comp Neurol 234:380–392PubMedGoogle Scholar
  122. Smeets WJ, Northcutt RG (1987) At least one thalamotelencephalic pathway in cartilaginous fishes projects to the medial pallium. Neurosci Lett 78:277–282PubMedGoogle Scholar
  123. Smeets WJAJ, Nieuwenhuys R, Roberts BL (1983) The central nervous system of cartilaginous fishes. Springer, BerlinGoogle Scholar
  124. Staubli U, Xu FB (1995) Effects of 5-HT3 receptor antagonism on hippocampal theta rhythm, memory, and LTP induction in the freely moving rat. J Neurosci 15(3):2445–2452PubMedGoogle Scholar
  125. Tischmeyer W, Kaczmarek L, Strauss M, Jork R, Matthies H (1990) Accumulation of c-fos mRNA in rat hippocampus during acquisition of a brightness discrimination. Behav Neural Biol 54:165–171PubMedGoogle Scholar
  126. Tokarev K, Tiunova A, Scharff C, Anokhin K (2011) Food for song: expression of C-Fos and ZENK in the zebra finch song nuclei during food aversion learning. PLoS One 6(6):e21157PubMedPubMedCentralGoogle Scholar
  127. Van-Eyk SM, Siebeck UE, Champ CM, Marshall J, Hart NS (2011) Behavioural evidence for colour vision in an elasmobranch. J Exp Biol 214:4186–4192PubMedGoogle Scholar
  128. Vollmann H, Wölfel S, Ohneseit P, Stransky E, Vonthein R, Wick W et al (2007) Differential expression of egr1 and activation of microglia following irradiation in the rat brain. Strahlenther Onkol 183(5):248–255PubMedGoogle Scholar
  129. Wada K, Howard JT, McConnell P, Whitney O, Lints T, Rivas M, Horita H, Patterson MA, White SA, Sharff C, Haesler S, Zhao S, Sakaguchi H, Hagiwara M, Shiraki T, Horizane-Kishikawa T, Skene P, Hayashizali Y, Carninci P, Jarvis ED (2006) A molecular neuroethological approach for identifying and characterizing a cascade of behaviorally regulated genes. PNAS 103(45):15212–15217PubMedGoogle Scholar
  130. Wai MS, Lorke DE, Webb SE, Yew DT (2005) The pattern of c-fos activation in the CNS is related to behavior in the mudskipper, Periophthalmus cantonensis. Behav Brain Res 167(2):318–327PubMedGoogle Scholar
  131. Walker DL, Toufexis DJ, Davis M (2003) Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur J Pharm 463(1–3):199–216Google Scholar
  132. Walters ET, Byrne JH (1985) Long-term enhancement produced by activity-dependent modulation of Aplysia sensory neurons. J Neurosci 5(3):662–672PubMedGoogle Scholar
  133. Waters CM, Hancock DC, Evan GI (1990) Identification and characterisation of the egr-1 gene product as an inducible, short-lived, nuclear phosphoprotein. Oncogene 5(5):669–674PubMedGoogle Scholar
  134. Wood L, Desjardins J, Fernald R (2011) Effects of stress and motivation on performing a spatial task. Neurobiol Learn Mem 95(3):277–285PubMedGoogle Scholar
  135. Yang XD, Korn H, Faber DS (1990) Long-term potentiation of electrotonic coupling at mixed synapses. Nature 348(6301):542–545PubMedGoogle Scholar
  136. Yopak KE (2012a) Neuroecology of cartilaginous fishes: the functional implications of brain scaling. J Fish Biol 80(5):1968–2023PubMedGoogle Scholar
  137. Yopak KE (2012b) The nervous system of cartilaginous fishes. Brain Behav Evol 80:77–79PubMedGoogle Scholar
  138. Zangenehpour S, Chaudhuri A (2002) Differential induction and decay curves of c-fos and zif268 revealed through dual activity maps. Mol Brain Res 109:221–225PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of ZoologyRheinische Friedrich-Wilhelms-University BonnBonnGermany

Personalised recommendations