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Potential evidence of peripheral learning and memory in the arms of dwarf cuttlefish, Sepia bandensis

Abstract

CREB (cAMP response element-binding) transcription factors are conserved markers of memory formation in the brain and peripheral circuits. We provide immunohistochemical evidence of CREB phosphorylation in the dwarf cuttlefish, Sepia bandensis, following the inaccessible prey (IP) memory experiment. During the IP experiment, cuttlefish are shown prey enclosed in a transparent tube, and tentacle strikes against the tube decrease over time as the cuttlefish learns the prey is inaccessible. The cues driving IP learning are unclear but may include sensory inputs from arms touching the tube. The neural activity marker, anti-phospho-CREB (anti-pCREB) was used to determine whether IP training stimulated cuttlefish arm sensory neurons. pCREB immunoreactivity occurred along the oral surface of the arms, including the suckers and epithelial folds surrounding the suckers. pCREB increased in the epithelial folds and suckers of trained cuttlefish. We found differential pCREB immunoreactivity along the distal–proximal axis of trained arms, with pCREB concentrated distally. Unequal CREB phosphorylation occurred among the 4 trained arm pairs, with arm pairs 1 and 2 containing more pCREB. The resulting patterns of pCREB in trained arms suggest that the arms obtain cues that may be salient for learning and memory of the IP experiment.

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Availability of data and materials

All data are available in the manuscript and online supplemental information.

Code availability

Not applicable.

Abbreviations

CREB:

CAMP response element-binding

IP:

Inaccessible prey

LTM:

Long-term memory

PBS:

Phosphate buffered saline

pCREB:

Phosphorylated-CREB

pCREB-ir:

pCREB immunoreactivity

PFA:

Paraformaldehyde

STM:

Short-term memory

References

  1. Adamo SA, Ehgoetz K, Sangster C, Whitehorne I (2006) Signaling to the enemy? Body pattern expression and its response to external cues during hunting in the cuttlefish Sepia officinalis (Cephalopoda). Biol Bull 210:192–200. https://doi.org/10.2307/4134557

    Article  PubMed  Google Scholar 

  2. Agin V, Dickel L, Chichery R, Chichery MP (1998) Evidence for a specific short-term memory in the cuttlefish, Sepia. Behav Processes 43:329–334. https://doi.org/10.1016/S0376-6357(98)00019-9

    CAS  Article  PubMed  Google Scholar 

  3. Agin V, Chichery R, Maubert E, Chichery MP (2003) Time-dependent effects of cycloheximide on long-term memory in the cuttlefish. Pharmacol Biochem Behav 75:141–146. https://doi.org/10.1016/S0091-3057(03)00041-8

    CAS  Article  PubMed  Google Scholar 

  4. Agin V, Chichery R, Dickel L, Chichery MP (2006) The “prawn-in-the-tube” procedure in the cuttlefish: Habituation or passive avoidance learning? Learn Mem 13:97–101. https://doi.org/10.1101/lm.90106

    Article  PubMed  PubMed Central  Google Scholar 

  5. Alves C, Chichery R, Boal JG, Dickel L (2007) Orientation in the cuttlefish Sepia officinalis: response versus place learning. Anim Cogn 10:29–36. https://doi.org/10.1007/s10071-006-0027-6

    Article  PubMed  Google Scholar 

  6. Bellanger C, Dauphin F, Chichery M-P, Chichery R (2003) Changes in cholinergic enzyme activities in the cuttlefish brain during memory formation. Physiol Behav 79:749–756. https://doi.org/10.1016/s0031-9384(03)00188-4

    CAS  Article  PubMed  Google Scholar 

  7. Bellier JP, Xie Y, Farouk SM, Sakaue Y, Tooyama I, Kimura H (2017) Immunohistochemical and biochemical evidence for the presence of serotonin-containing neurons and nerve fibers in the octopus arm. Brain Struct Funct 222:3043–3061. https://doi.org/10.1007/s00429-017-1385-3

    CAS  Article  PubMed  Google Scholar 

  8. Benito E, Barco A (2010) CREB’s control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci 33:230–240. https://doi.org/10.1016/j.tins.2010.02.001

    CAS  Article  PubMed  Google Scholar 

  9. Billard P, Schnell AK, Clayton NS, Jozet-Alves C (2020) Cuttlefish show flexible and future-dependent foraging cognition. Biol Lett 16:1–5. https://doi.org/10.1098/rsbl.2019.0743

    Article  Google Scholar 

  10. Bleckmann SC, Blendy JA, Rudolph D, Monaghan AP, Schmid W, Schütz G (2002) Activating transcription factor 1 and CREB are important for cell survival during early mouse development. Mol Cell Biol 22:1919–1925. https://doi.org/10.1128/mcb.22.6.1919-1925.2002

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Bowers J, Nimi T, Wilson J, Wagner S, Amarie D, Sittaramane V (2020) Evidence of learning and memory in the juvenile dwarf cuttlefish Sepia bandensis. Learn Behav 48:420–431. https://doi.org/10.3758/s13420-020-00427-4

    Article  PubMed  Google Scholar 

  12. Boycott BB (1961) The functional organization of the brain of the cuttlefish Sepia officinalis. Proc R Soc Lond B 153:503–534. https://doi.org/10.1098/rspb.1961.0015

    Article  Google Scholar 

  13. Boycott BB, Young JZ (1955) A memory system in Octopus vulgaris Lamarck. Proc R Soc Lond B 143:449–480. https://doi.org/10.1098/rspb.1955.0024

    CAS  Article  PubMed  Google Scholar 

  14. Brightwell JJ, Smith CA, Neve RL, Colombo PJ (2007) Long-term memory for place learning is facilitated by expression of cAMP response element-binding protein in the dorsal hippocampus. Learn Mem 14:195–199. https://doi.org/10.1101/lm.395407

    Article  PubMed  Google Scholar 

  15. Brown ER, Piscopo S (2013) Synaptic plasticity in cephalopods; more than just learning and memory? Invert Neurosci 13:35–44. https://doi.org/10.1007/s10158-013-0150-4

    Article  PubMed  Google Scholar 

  16. Byrne RA, Kuba MJ, Meisel DV, Griebel U, Mather JA (2006) Does Octopus vulgaris have preferred arms? J Comp Psychol 120:198–204. https://doi.org/10.1037/0735-7036.120.3.198

    Article  PubMed  Google Scholar 

  17. Cartron L, Darmaillacq AS, Dickel L (2013) The “prawn-in-the-tube” procedure: what do cuttlefish learn and memorize? Behav Brain Res 240:29–32. https://doi.org/10.1016/j.bbr.2012.11.010

    Article  PubMed  Google Scholar 

  18. Casadio A, Martin KC, Giustetto M, Zhu H, Chen M, Bartsch D, Bailey CH, Kandel ER (1999) A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 99:221–237. https://doi.org/10.1016/S0092-8674(00)81653-0

    CAS  Article  PubMed  Google Scholar 

  19. Chichery MP, Chichery R (1987) The anterior basal lobe and control of prey-capture in the cuttlefish (Sepia officinalis). Physiol Behav 40:329–336. https://doi.org/10.1016/0031-9384(87)90055-2

    CAS  Article  PubMed  Google Scholar 

  20. Chichery MP, Chichery R (1988) Manipulative motor activity of the cuttlefish Sepia officinalis during prey-capture. Behav Processes 17:45–56. https://doi.org/10.1016/0376-6357(88)90049-6

    CAS  Article  PubMed  Google Scholar 

  21. Deisseroth K, Bito H, Tsien RW (1996) Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron 16:89–101. https://doi.org/10.1016/S0896-6273(00)80026-4

    CAS  Article  PubMed  Google Scholar 

  22. Deisseroth K, Heist EK, Tsien RW (1998) Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons. Nature 12:198–202. https://doi.org/10.1038/32448

  23. Di Poi C, Darmaillacq AS, Dickel L, Boulouard M, Bellanger C (2013) Effects of perinatal exposure to waterborne fluoxetine on memory processing in the cuttlefish Sepia officinalis. Aquat Toxicol 132–133:84–91. https://doi.org/10.1016/j.aquatox.2013.02.004

    CAS  Article  PubMed  Google Scholar 

  24. Dickel L, Chichery MP, Chichery R (1998) Time differences in the emergence of short- and long-term memory during post-embryonic development in the cuttlefish, Sepia. Behav Processes 44:81–86. https://doi.org/10.1016/S0376-6357(98)00024-2

    CAS  Article  PubMed  Google Scholar 

  25. Dickel L, Chichery MP, Chichery R (2001) Increase of learning abilities and maturation of the vertical lobe complex during postembryonic development in the cuttlefish, Sepia. Dev Psychobiol 39:92–98. https://doi.org/10.1002/dev.1033

    CAS  Article  PubMed  Google Scholar 

  26. Dickel L, Darmaillacq AS, Jozet-Alves C, Bellanger C (2013) Learning, memory, and brain plasticity in cuttlefish (Sepia officinalis). In: Menzel R, Benjamin PR (eds) Handbook of behavioral neuroscience. Elsevier, Amsterdam, pp 318–333

    Google Scholar 

  27. Efimova OI, Ierusalimskii VN, Anokhin KV, Balaban PM (2007) Immunohistochemical detection of the activation of CREB and c-Fos transcription factors in the nervous system of the terrestrial snail induced by pentylenetetrazole. Neurosci Behav Physiol 37:853–856. https://doi.org/10.1007/s11055-007-0092-6

    CAS  Article  PubMed  Google Scholar 

  28. Eisenhardt D, Friedrich A, Stollhoff N, Müller U, Kress H, Menzel R (2003) The AmCREB gene is an ortholog of the mammalian CREB/CREM family of transcription factors and encodes several splice variants in the honeybee brain. Insect Mol Biol 12:373–382. https://doi.org/10.1046/j.1365-2583.2003.00421.x

    CAS  Article  PubMed  Google Scholar 

  29. Fain GL, Matthews HR, Cornwall MC, Koutalos Y (2001) Adaptation in vertebrate photoreceptors. Physiol Rev 81:117–151. https://doi.org/10.1152/physrev.2001.81.1.117

    CAS  Article  PubMed  Google Scholar 

  30. Fiorito G, Affuso A, Basil J et al (2015) Guidelines for the care and welfare of cephalopods in research –A consensus based on an initiative by CephRes, FELASA and the Boyd Group. Lab Anim 49:1–90. https://doi.org/10.1177/0023677215580006

    Article  PubMed  Google Scholar 

  31. Freeman FM, Rose SPR (1999) Expression of Fos and Jun proteins following passive avoidance training in the day-old chick. Learn Mem 6:389–397. https://doi.org/10.1101/lm.6.4.389

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. Gallo FT, Katche C, Morici JF, Medina JH, Weisstaub NV (2018) Immediate early genes, memory and psychiatric disorders: focus on c-Fos, Egr1 and Arc. Front Behav Neurosci 12:79. https://doi.org/10.3389/fnbeh.2018.00079

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. Gleadall IG (2013) The effects of prospective anaesthetic substances on cephalopods: summary of original data and a brief review of studies over the last two decades. J Exp Mar Bio Ecol 447:23–30. https://doi.org/10.1016/j.jembe.2013.02.008

    CAS  Article  Google Scholar 

  34. Grasso FW (2008) Octopus sucker-arm coordination in grasping and manipulation. Am Malacol Bull 24:13–23. https://doi.org/10.4003/0740-2783-24.1.13

    Article  Google Scholar 

  35. Grasso FW (2014) The octopus with two brains: How are distributed and central representations integrated in the octopus central nervous system? In: Darmaillacq AS, Dickel L, Mather J (eds) Cephalopod cognition. Cambridge University Press, Cambridge, pp 94–122

    Chapter  Google Scholar 

  36. Grasso F, Wells M (2013) Tactile sensing in the octopus. Scholarpedia 8:7165. https://doi.org/10.4249/scholarpedia.7165

    Article  Google Scholar 

  37. Graziadei P (1964) Receptors in the sucker of the cuttlefish. Nature 203:384–386. https://doi.org/10.1038/203384a0

    CAS  Article  PubMed  Google Scholar 

  38. Graziadei P (1965) Muscle receptors in cephalopods. Proc R Soc Lond B 161:392–402. https://doi.org/10.1098/rspb.1965.0011

    Article  Google Scholar 

  39. Graziadei P (1971) The nervous system of the arm. In: Young JZ (ed) The anatomy of the nervous system of Octopus vulgaris. Clarendon Press, Oxford, pp 45–61

    Google Scholar 

  40. Graziadei PPC, Gagne HT (1976) Sensory innervation in the rim of the octopus sucker. J Morphol 150(3):639–679. https://doi.org/10.1002/jmor.1051500304

    CAS  Article  PubMed  Google Scholar 

  41. Guo CH, Senzel A, Li K, Feng ZP (2010) De novo protein synthesis of syntaxin-1 and dynamin-1 in long-term memory formation requires creb1 gene transcription in Lymnaea stagnalis. Behav Genet 40:680–693. https://doi.org/10.1007/s10519-010-9374-9

    Article  PubMed  Google Scholar 

  42. Gutfreund Y, Matzner H, Flash T, Hochner B (2006) Patterns of motor activity in the isolated nerve cord of the octopus arm. Biol Bull 211:212–222. https://doi.org/10.2307/4134544

    Article  PubMed  Google Scholar 

  43. Hanlon RT, Messenger JB (2018) Cephalopod behaviour. Cambridge University Press, Cambridge

    Book  Google Scholar 

  44. Hawk JD, Calvo AC, Liu P, Almoril-Porras A, Aljobeh A, Torruella-Suárez ML, Ren I, Cook N, Greenwood J, Luo L, Wang ZW, Samuel ADT, Colón-Ramos DA (2018) Integration of plasticity mechanisms within a single sensory neuron of C. elegans actuates a memory. Neuron 97:356-367.e4. https://doi.org/10.1016/j.neuron.2017.12.027

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. Hochner B, Brown ER, Langella M, Shomrat T, Fiorito G (2003) A learning and memory area in the Octopus brain manifests a vertebrate-like long-term potentiation. J Neurophysiol 90:3547–3554. https://doi.org/10.1152/jn.00645.2003

    Article  PubMed  Google Scholar 

  46. Huang YH, Lin Y, Brown TE, Han MH, Saal DB, Neve RL, Zukin RS, Sorg BA, Nestler EJ, Malenka RC, Dong Y (2008) CREB modulates the functional output of nucleus accumbens neurons: a critical role of N-methyl-D-aspartate glutamate receptor (NMDAR) receptors. J Biol Chem 283:2751–2760. https://doi.org/10.1074/jbc.M706578200

    CAS  Article  PubMed  Google Scholar 

  47. Izquierdo LA, Barros DM, Vianna MRM, Coitinho A, deDavid e Silva T, Choi H, Moletta B, Medina JH, Izquierdo I (2002) Molecular pharmacological dissection of short- and long-term memory. Cell Mol Neurobiol 22:269–287. https://doi.org/10.1023/A:1020715800956

    CAS  Article  PubMed  Google Scholar 

  48. Jereb P, Roper CFE (2005) Cephalopods of the world. An annotated and illustrated catalogue of cephalopod species known to date. Volume 1 chambered nautiluses and sepioids (Nautilidae, Sepiidae, Sepiolidae, Sepiadariidae, Idiosepiidae and Spirulidae). FAO Species Catalogue for Fishery Purposes. FAO, Rome

  49. Jozet-Alves C, Bertin M, Clayton NS (2013) Evidence of episodic-like memory in cuttlefish. Curr Biol 23:R1033–R1035. https://doi.org/10.1016/j.cub.2013.10.021

    CAS  Article  PubMed  Google Scholar 

  50. Karson MA, Boal JG, Hanlon RT (2003) Experimental evidence for spatial learning in cuttlefish (Sepia officinalis). J Comp Psychol 117:149–155. https://doi.org/10.1037/0735-7036.117.2.149

    Article  PubMed  Google Scholar 

  51. Kier WM (2016) The musculature of coleoid cephalopod arms and tentacles. Front Cell Dev Biol 4:10. https://doi.org/10.3389/fcell.2016.00010

    Article  PubMed  PubMed Central  Google Scholar 

  52. Kim J, Kwon JT, Kim HS, Han JH (2013) CREB and neuronal selection for memory trace. Front Neural Circuits 7:44. https://doi.org/10.3389/fncir.2013.00044

    Article  PubMed  PubMed Central  Google Scholar 

  53. Kitagawa H, Sugo N, Morimatsu M, Arai Y, Yanagida T, Yamamoto N (2017) Activity-dependent dynamics of the transcription factor of cAMP-response element binding protein in cortical neurons revealed by single-molecule imaging. J Neurosci 37:1–10. https://doi.org/10.1523/jneurosci.0943-16.2016

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  54. Kovach SJ, Price JA, Shaw CM, Theodorakis NG, McKillop IH (2006) Role of cyclic-AMP responsive element binding (CREB) proteins in cell proliferation in a rat model of hepatocellular carcinoma. J Cell Physiol 206:411–419. https://doi.org/10.1002/jcp.20474

    CAS  Article  PubMed  Google Scholar 

  55. Landeira BS, Santana TT, Araujo JA, Tabet EI, Tannous BA, Schroeder T, Costa MR (2018) Activity-independent effects of CREB on neuronal survival and differentiation during mouse cerebral cortex development. Cereb Cortex 28:537–548. https://doi.org/10.1093/cercor/bhw387

    Article  Google Scholar 

  56. Lee J-A, Lee S-H, Lee C, Chang D-J, Lee Y, Kim H, Cheang Y-H, Ko H-G, Lee Y-S, Jun H, Bartsch D, Kander ER, Kaang B-K (2006) PKA-activated ApAF-ApC/EBP heterodimer is a a key downstream effector of ApCREB and is necessary and sufficient for the consolidation of long-term facilation. J Cell Biol 174:827–838. https://doi.org/10.1083/jcb.200512066

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  57. Maksimovic S, Nakatani M, Baba Y, Nelson AM, Marshall KL, Wellnitz SA, Firozi P, Woo SH, Ranade S, Patapoutian A, Lumpkin EA (2014) Epidermal merkel cells are mechanosensory cells that tune mammalian touch receptors. Nature 509:617–621. https://doi.org/10.1038/nature13250

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  58. Mather JA (1991) Foraging, feeding and prey remains in middens of juvenile Octopus vulgaris (Mollusca, Cephalopoda). J Zool 224:27–39. https://doi.org/10.1111/j.1469-7998.1991.tb04786.x

    Article  Google Scholar 

  59. Mather JA, Dickel L (2017) Cephalopod complex cognition. Curr Opin Behav Sci 16:131–137. https://doi.org/10.1016/j.cobeha.2017.06.008

    Article  Google Scholar 

  60. Mather JA, Kuba MJ (2013) The cephalopod specialties: complex nervous system, learning, and cognition. Can J Zool 91:431–449. https://doi.org/10.1139/cjz-2013-0009

    Article  Google Scholar 

  61. Matsumoto Y, Matsumoto CS, Mizunami M (2018) Signaling pathways for long-term memory formation in the cricket. Front Psychol 9:1014. https://doi.org/10.3389/fpsyg.2018.01014

    Article  PubMed  PubMed Central  Google Scholar 

  62. McGann JP (2015) Associative learning and sensory neuroplasticity: how does it happen and what is it good for? Learn Mem 22:567–576. https://doi.org/10.1101/lm.039636.115

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  63. Messenger JB (1968) The visual attack of the cuttlefish, Sepia officinalis. Anim Behav 16:342–357. https://doi.org/10.2331/suisan.63.145

    CAS  Article  PubMed  Google Scholar 

  64. Messenger JB (1971) Two-stage recovery of a response in Sepia. Nature 232:202–203. https://doi.org/10.1038/232202a0

    CAS  Article  PubMed  Google Scholar 

  65. Messenger JB (1973) Learning in the cuttlefish, Sepia. Anim Behav 21:801–826. https://doi.org/10.1016/S0003-3472(73)80107-1

    Article  Google Scholar 

  66. Molliver DC, Cook SP, Carlsten JA, Wright DE, McCleskey EW (2002) ATP and UTP excite sensory neurons and induce CREB phosphorylation through the metabotropic receptor, P2Y2. Eur J Neurosci 16:1850–1860. https://doi.org/10.1046/j.1460-9568.2002.02253.x

    Article  PubMed  Google Scholar 

  67. Moon C, Sung YK, Reddy R, Ronnett GV (1999) Odorants induce the phosphorylation of the cAMP response element binding protein in olfactory receptor neurons. Proc Natl Acad Sci USA 96:14605–14610. https://doi.org/10.1073/pnas.96.25.14605

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  68. Moroz LL (2011) Aplysia. Curr Biol 21:R60–R61. https://doi.org/10.1016/j.cub.2010.11.028

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  69. Müller U (2000) Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron 27:159–168. https://doi.org/10.1016/S0896-6273(00)00017-9

    Article  PubMed  Google Scholar 

  70. Munger B (1977) Neural-epithelial interactions in sensory receptors. J Invest Dermatol 69:27–40. https://doi.org/10.1111/1523-1747.ep12497861

    CAS  Article  PubMed  Google Scholar 

  71. Nödl MT, Kerbl A, Walzl MG, Müller GB, Gert de Couet H (2016) The cephalopod arm crown: appendage formation and differentiation in the Hawaiian bobtail squid Euprymna scolopes. Front Zool 13:44. https://doi.org/10.1186/s12983-016-0175-8

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  72. Okamoto K, Yasumuro H, Mori A, Ikeda Y (2017) Unique arm-flapping behavior of the pharaoh cuttlefish, Sepia pharaonis: putative mimicry of a hermit crab. J Ethol 35:307–311. https://doi.org/10.1007/s10164-017-0519-7

    Article  PubMed  PubMed Central  Google Scholar 

  73. Packard A (1972) Cephalopods and fish: the limits of convergence. Biol Rev 47:241–307. https://doi.org/10.1111/j.1469-185x.1972.tb00975.x

    CAS  Article  Google Scholar 

  74. Pereira C (2015) Short-term and long-term learning and memory in snails (Achatina fulica). J Zool Stud 2:1–12

    Google Scholar 

  75. Purdy JE, Roberts AC, Garcia CA (1999) Sign tracking in cuttlefish (Sepia officinalis). J Comp Psychol 113:443–449. https://doi.org/10.1037/0735-7036.113.4.443

    CAS  Article  PubMed  Google Scholar 

  76. Purdy JE, Dixon D, Estrada A, Peters A, Riedlinger E, Suarez R (2006) Prawn-in-a-tube procedure: habituation or associative learning in cuttlefish? J Gen Psychol 133:131–152. https://doi.org/10.3200/GENP.133.2.131-152

    Article  PubMed  Google Scholar 

  77. Ribeiro MJ, Serfozo Z, Papp A, Kemenes I, O’Shea M, Yin JCP, Benjamin PR, Kemenes G (2003) Cyclic AMP response element-binding (CREB)-like proteins in a molluscan brain: cellular localization and learning-induced phosphorylation. Eur J Neurosci 18:1223–1234. https://doi.org/10.1046/j.1460-9568.2003.02856.x

    Article  PubMed  Google Scholar 

  78. Sakaue Y, Bellier JP, Kimura S, D’Este L, Takeuchi Y, Kimura H (2014) Immunohistochemical localization of two types of choline acetyltransferase in neurons and sensory cells of the octopus arm. Brain Struct Funct 219:323–341. https://doi.org/10.1007/s00429-012-0502-6

    CAS  Article  PubMed  Google Scholar 

  79. Sampaio E, Ramos CS, Bernardino BLM, Bleunven M, Augustin ML, Moura E, Lopes VM, Rosa R (2020) Neurally underdeveloped cuttlefish newborns exhibit social learning. Anim Cogn 24:23–32. https://doi.org/10.1007/s10071-020-01411-1

    Article  PubMed  Google Scholar 

  80. Sanders FK, Young JZ (1940) Learning and other functions of the higher nervous centres of Sepia. J Neurophysiol 3:501–526. https://doi.org/10.1152/jn.1940.3.6.501

    Article  Google Scholar 

  81. Scata G, Jozet-Alves C, Thomasse C, Josef N, Shashar N (2016) Spatial learning in the cuttlefish Sepia officinalis: preference for vertical over horizontal information. J Exp Biol 219:2928–2933. https://doi.org/10.1242/jeb.129080

    Article  PubMed  Google Scholar 

  82. Shigeno S, Andrews PLR, Ponte G, Fiorito G (2018) Cephalopod brains: an overview of current knowledge to facilitate comparison with vertebrates. Front Physiol 9:952. https://doi.org/10.3389/fphys.2018.00952

    Article  PubMed  PubMed Central  Google Scholar 

  83. Shinzato S, Yasumuro H, Ikeda Y (2018) Visual stimuli for the induction of hunting behavior in cuttlefish Sepia pharaonis. Biol Bull 234:106–115. https://doi.org/10.1086/697522

    Article  PubMed  Google Scholar 

  84. Shomrat T, Turchetti-Maia AL, Stern-Mentch N, Basil JA, Hochner B (2015) The vertical lobe of cephalopods: an attractive brain structure for understanding the evolution of advanced learning and memory systems. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 201:947–956. https://doi.org/10.1007/s00359-015-1023-6

    CAS  Article  PubMed  Google Scholar 

  85. Sirakov M, Zarrella I, Borra M, Rizzo F, Biffali E, Arnone MI, Fiorito G (2009) Selection and validation of a set of reliable reference genes for quantitative RT-PCR studies in the brain of the Cephalopod Mollusc Octopus vulgaris. BMC Mol Biol 10:70. https://doi.org/10.1186/1471-2199-10-70

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  86. Sumbre G, Gutfreund Y, Fiorito G, Flash T, Hochner B (2001) Control of Octopus arm extension by a peripheral motor program. Science 293:1845–1848. https://doi.org/10.1126/science.1060976

    CAS  Article  PubMed  Google Scholar 

  87. Turchetti-Maia A, Shomrat T, Hochner B (2019) The vertical lobe of cephalopods-a brain structure ideal for exploring the mechanisms of complex forms of learning and memory. In: Byrne JH (ed) The Oxford handbook of invertebrate neurobiology. Oxford University Press, New York, pp 558–574

    Google Scholar 

  88. Van Den Berg M, Verbaarschot P, Hontelez S, Vet LEM, Dicke M, Smid HM (2010) CREB expression in the brains of two closely related parasitic wasp species that differ in long-term memory formation. Insect Mol Biol 19:367–379. https://doi.org/10.1111/j.1365-2583.2010.00997.x

    CAS  Article  PubMed  Google Scholar 

  89. Van Leeuwen JL, Kier WM (1997) Functional design of tentacles in squid: linking sarcomere ultrastructure to gross morphological dynamics. Philos Trans R Soc Lond B Biol Sci 352:551–571. https://doi.org/10.1098/rstb.1997.0038

    Article  PubMed Central  Google Scholar 

  90. Villanueva R, Perricone V, Fiorito G (2017) Cephalopods as predators: a short journey among behavioral flexibilities, adaptions, and feeding habits. Front Physiol 8:598. https://doi.org/10.3389/fphys.2017.00598

    Article  PubMed  PubMed Central  Google Scholar 

  91. Warnke KM, Kaiser R, Hasselmann M (2012) First observations of a snail-like body pattern in juvenile Sepia bandensis (Cephalopoda: Sepiidae). A note. Neues Jahrb Fur Geol Und Palaontologie - Abhandlungen 266:51–57. https://doi.org/10.1127/0077-7749/2012/0259

    Article  Google Scholar 

  92. Wells MJ (1958) Factors affecting reactions to mysis by newly hatched Sepia. Behaviour 13:96–111. https://doi.org/10.1163/156853958X00055

    Article  Google Scholar 

  93. Wells MJ (1964) Tactile discrimination of shape by octopus. Q J Exp Psychol 16:156–162. https://doi.org/10.1080/17470216408416360

    Article  Google Scholar 

  94. Wells MJ (1978) Octopus: physiology and behaviour of an advanced invertebrate. Springer, Netherlands

    Book  Google Scholar 

  95. Wells MJ, Wells J (1957) The function of the brain of octopus in tactile discrimination. J Exp Biol 34:131–142. https://doi.org/10.1242/jeb.34.1.131

    Article  Google Scholar 

  96. Wen AY, Sakamoto KM, Miller LS (2010) The role of the transcription factor CREB in immune function. J Immunol 185:6413–6419. https://doi.org/10.4049/jimmunol.1001829

    CAS  Article  PubMed  Google Scholar 

  97. Woo SH, Lumpkin EA, Patapoutian A (2015) Merkel cells and neurons keep in touch. Trends Cell Biol 25:74–81. https://doi.org/10.1016/j.tcb.2014.10.003

    Article  PubMed  Google Scholar 

  98. Yin JCP, Del Vecchio M, Zhou H, Tully T (1995) CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in drosophila. Cell 81:107–115. https://doi.org/10.1016/0092-8674(95)90375-5

    CAS  Article  PubMed  Google Scholar 

  99. Young JZ (1971) The anatomy of the nervous system of Octopus vulgaris. Clarendon Press, Oxford

    Google Scholar 

  100. Young JZ (1983) The distributed tactile memory system of Octopus. Proc R Soc Lond B 218:135–176. https://doi.org/10.1098/rspb.1983.0032

    Article  Google Scholar 

  101. Yuan F, Xiong G, Cohen NA, Cohen AS (2017) Optimized protocol of methanol treatment for immunofluorescent staining in fixed brain slices. Appl Immunohistochem Mol Morphol 25:221–224. https://doi.org/10.1097/PAI.0000000000000293

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  102. Zarrella I (2012) Testing changes in gene expression profiles in Octopus vulgaris (Mollusca Cephalopoda). Doctoral dissertation, The Open University. 

  103. Zepeda EA, Veline RJ, Crook RJ (2017) Rapid associative learning and stable long-term memory in the squid Euprymna scolopes. Biol Bull 232:212–218. https://doi.org/10.1086/693461

    Article  PubMed  Google Scholar 

  104. Zhang L, Jin C, Lu X, Yang J, Wu S, Liu Q, Chen R, Bai C, Zhang D, Zheng L, Du Y, Cai Y (2014) Aluminium chloride impairs long-term memory and downregulates cAMP-PKA-CREB signalling in rats. Toxicology 323:95–108. https://doi.org/10.1016/j.tox.2014.06.011

    CAS  Article  PubMed  Google Scholar 

  105. Zullo L, Eichenstein H, Maiole F, Hochner B (2019) Motor control pathways in the nervous system of Octopus vulgaris arm. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 205:271–279. https://doi.org/10.1007/s00359-019-01332-6

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank Bedore’s lab (Dr. Christine Bedore, Theresa Gunn, and Matt Levendosky) for their valuable resource sharing and advice on cuttlefish husbandry. We would also like to thank Bret Grasse for his advice on cuttlefish rearing.

Funding

This research was funded by Georgia Southern faculty research seed award and Georgia Southern graduate student research award.

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JB and VS participated in the design of this study. JB, JW and TN performed all the experiments and data analyses. JB and VS wrote and revised the manuscript.

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Correspondence to Vinoth Sittaramane.

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Bowers, J., Wilson, J., Nimi, T. et al. Potential evidence of peripheral learning and memory in the arms of dwarf cuttlefish, Sepia bandensis. J Comp Physiol A 207, 575–594 (2021). https://doi.org/10.1007/s00359-021-01499-x

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Keywords

  • Cuttlefish
  • CREB
  • Learning
  • Memory
  • Sepia