Abstract
In contextual conditioning, a complex pattern of information is processed to associate the characteristics of a particular place with incentive or aversive reinforcements. This type of learning has been widely studied in mammals, but studies of other taxa are scarce. The context-signal memory (CSM) paradigm of the crab Chasmagnathus has been extensively used as a model of learning and memory. Although initially interpreted as habituation, some characteristics of contextual conditioning have been described. However, no anticipatory response has been detected for animals exposed to the training context. Thus, CSM could be interpreted either as an associative habituation or as contextual conditioning that occurs without a context-evoked anticipatory response. Here, we describe a training protocol developed for contextual Pavlovian conditioning (CPC). For each training trial, the context (conditioned stimulus, CS) was discretely presented and finished together with the unconditioned stimulus (US). In agreement with the CSM paradigm, a robust freezing response was acquired during the 15 training trials, and clear retention was found when tested with the US presentation after short (2 and 4 h) and long (1–4 days) delays. This CPC memory showed forward but not simultaneous presentation conditioning and was context specific and protein synthesis dependent. Additionally, a weak CPC memory was enhanced during consolidation. One day after training, CPC was extinguished by repeated CS presentation, while one presentation induced a memory labilisation–reconsolidation process. Finally, we found an anticipatory conditioned response (CR) during the CS presentation for both short-term (4 h) and long-term memory (24 h). These findings support the conditioning nature of the new paradigm.
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References
Alberini CM (2008) The role of protein synthesis during the labile phases of memory: revisiting the skepticism. Neurobiol Learn Mem 89:234–246
Anagnostaras SG, Gale GD, Fanselow MS (2001) Hippocampus and contextual fear conditioning: recent controversies and advances. Hippocampus 11:8–17
Anokhin KV, Tiunova AA, Rose SPR (2002) Reminder effects—reconsolidation or retrieval deficit? Pharmacological dissection with protein synthesis inhibitors following reminder for a passive-avoidance task in young chicks. Eur J Neurosci 15:1759–1765
Berón de Astrada M, Sztarker J, Tomsic D (2001) Visual interneurons of the crab Chasmagnathus studied by intracellular recordings in vivo. J Comp Physiol A 187:37–44
Boccia M, Freudenthal R, Blake M, de la Fuente V, Acosta G, Baratti C, Romano A (2007) Activation of hippocampal nuclear factor-kappa B by retrieval is required for memory reconsolidation. J Neurosci 27:13436–13445
Brembs B, Wiener J (2006) Context and occasion setting in Drosophila visual learning. Learn Mem 13:618–628
Burnovicz A, Hermitte G (2010) Conditioning of an autonomic response in Crustacea. Physiol Behav 101:168–175
Carbó Tano M, Molina VA, Maldonado H, Pedreira ME (2009) Memory consolidation and reconsolidation in an invertebrate model: the role of the GABAergic system. Neuroscience 158:387–401
de la Fuente V, Freudenthal R, Romano A (2011) Reconsolidation or extinction: transcription factor switch in the determination of memory course after retrieval. J Neurosci 31:5562–5573
Eisenberg M, Kobilo T, Berman DE, Dudai Y (2003) Stability of retrieved memory: inverse correlation with trace dominance. Science 301:1102–1104
Freudenthal R, Boccia MM, Acosta GB, Blake MG, Merlo E, Baratti CM, Romano A (2005) NF-kappaB transcription factor is required for inhibitory avoidance long-term memory in mice. Eur J Neurosci 21:2845–2852
Hall G (1994) Pavlovian conditioning: laws of association. In: Mackintosh NJ (ed) Animal learning and cognition, 2nd edn. Academic Press, New York, pp 12–43
Hawkins RD, Carew TJ, Kandel ER (1986) Effects of interstimulus interval and contingency on classical conditioning of the Aplysia siphon withdrawal reflex. J Neurosci 6:1695–1701
Hepp Y, Pérez-Cuesta LM, Maldonado H, Pedreira ME (2010) Extinction memory in the crab Chasmagnathus: recovery protocols and effects of multi-trial extinction training. Anim Cogn 13:391–403
Hoeger U, Florey E (1989) Catecholamine degradation in the hemolymph of the Chinese crab, Eriocheir Sinensis. Comp Biochem Physiol Part C Comp Pharmacol 92:323–327
Holland PC (1983) Occasion setting in Pavlovian feature positive discriminations. In Commons ML, Herrnstein RJ, Wagner AR (eds) Quantitative analyses of behavior: discrimination processes, vol 4. Ballinger, New York, pp 183–206
Howell DC (1987) Statistical methods of psychology, 2nd edn. Duxbury, Boston
Liu L, Wolf R, Ernst R, Heisenberg M (1999) Context generalization in Drosophila visual learning requires the mushroom bodies. Nature 400:753–756
Lozada M, Romano A, Maldonado H (1990) Long-term habituation to a danger stimulus in the crab Chasmagnathus granulatus. Physiol Behav 47:35–41
Lubin FD, Sweatt JD (2007) The IkappaB kinase regulates chromatin structure during reconsolidation of conditioned fear memories. Neuron 55:942–957
Maldonado H, Romano A, Tomsic D (1997) Long-term habituation (LTH) in the crab Chasmagnathus: a model for behavioral and mechanistic studies of memory. Braz J Med Biol Res 30:813–826
Meffert MK, Baltimore D (2005) Physiological functions for brain NF-kappaB. Trends Neurosci 28:37–43
Merlo E, Romano A (2008) Memory extinction entails the inhibition of the transcription factor NF-kappaB. PLoS ONE 3:e3687
Merlo E, Freudenthal R, Romano A (2002) The IkappaB kinase inhibitor sulfasalazine impairs long-term memory in the crab Chasmagnathus. Neuroscience 112:161–172
Merlo E, Freudenthal R, Maldonado H, Romano A (2005) Activation of the transcription factor NF-kappaB by retrieval is required for long-term memory reconsolidation. Learn Mem 12:23–29
Nader K, Schafe GE, LeDoux JE (2000) The labile nature of consolidation theory. Nat Rev Neurosci 1:216–219
Pedreira ME, Maldonado H (2003) Protein synthesis subserves reconsolidation or extinction depending on reminder duration. Neuron 38:863–869
Pedreira ME, Dimant B, Tomsic D, Quesada-Allue LA, Maldonado H (1995) Cycloheximide inhibits context memory and long-term habituation in the crab Chasmagnathus. Pharmacol Biochem Behav 52:385–395
Pedreira ME, Dimant B, Maldonado H (1996) Inhibitors of protein and RNA synthesis block context memory and long-term habituation in the crab Chasmagnathus. Pharmacol Biochem Behav 54:611–617
Pedreira ME, Romano A, Tomsic D, Lozada M, Maldonado H (1998) Massed and spaced training build up different components of long-term habituation in the crab Chasmagnathus. Anim Learn Behav 26:34–45
Pedreira ME, Pérez-Cuesta LM, Maldonado H (2002) Reactivation and reconsolidation of long-term memory in the crab Chasmagnathus: protein synthesis requirement and mediation by NMDA-type glutamatergic receptors. J Neurosci 22:8305–8311
Pedreira ME, Pérez-Cuesta LM, Maldonado H (2004) Mismatch between what is expected and what actually occurs triggers memory reconsolidation or extinction. Learn Mem 11:579–585
Pereyra P, González Portino E, Maldonado H (2000) Long-lasting and context-specific freezing preference is acquired after spaced repeated presentations of a danger stimulus in the crab Chasmagnathus. Neurobiol Learn Mem 74:119–134
Pérez-Cuesta LM, Maldonado H (2009) Memory reconsolidation and extinction in the crab: mutual exclusion or coexistence? Learn Mem 16:714–721
Pérez-Cuesta LM, Hepp Y, Pedreira ME, Maldonado H (2007) Memory is not extinguished along with CS presentation but within a few seconds after CS-offset. Learn Mem 14:101–108
Romano A, Lozada M, Maldonado H (1990) Effect of naloxone pretreatment on habituation in the crab Chasmagnathus granulatus. Behav Neural Biol 53:113–122
Romano A, Lozada M, Maldonado H (1991) Nonhabituation processes affect stimulus specificity of response habituation in the crab Chasmagnathus granulatus. Behav Neurosci 105:542–552
Romano A, Freudenthal R, Merlo E, Routtenberg A (2006a) Evolutionarily-conserved role of the NF-kappaB transcription factor in neural plasticity and memory. Eur J Neurosci 24:1507–1516
Romano A, Locatelli F, Freudenthal R, Merlo E, Feld M, Ariel P, Lemos D, Federman N, Fustiñana MS (2006b) Lessons from a crab: molecular mechanisms in different memory phases of Chasmagnathus. Biol Bull 210:280–288
Rosenthal R, Rosnow RL (1985) Contrast analysis focused comparisons in the analysis of variance. Cambridge University Press, Cambridge, UK
Sangha S, Scheibenstock A, Lukowiak K (2003) Reconsolidation of a long-term memory in Lymnaea requires new protein and RNA synthesis and the soma of right pedal dorsal 1. J Neurosci 23:8034–8040
Strausfeld NJ, Hansen L, Li Y, Gomez RS, Ito K (1998) Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn Mem 5:11–37
Suárez LD, Smal L, Delorenzi A (2010) Updating contextual information during consolidation as result of a new memory trace. Neurobiol Learn Mem 93:561–571
Suzuki A, Josselyn SA, Frankland PW, Masushige S, Silva AJ, Kida S (2004) Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J Neurosci 24:4787–4795
Sztarker J, Tomsic D (2011) Brain modularity in arthropods: individual neurons that support “what” but not “where” memories. J Neurosci 31:8175–8180
Tomsic D, Maldonado H, Rakitin A (1991) Morphine and GABA: effects on perception, escape response and long-term habituation to a danger stimulus in the crab Chasmagnathus. Brain Res Bull 26:699–706
Tomsic D, Romano A, Maldonado H (1998) Behavioral and mechanistic bases of long-term habituation in the crab Chasmagnathus. Adv Exp Med Biol 446:17–35
Tomsic D, de Astrada MB, Sztarker J, Maldonado H (2009) Behavioral and neuronal attributes of short- and long-term habituation in the crab Chasmagnathus. Neurobiol Learn Mem 92:176–182
Whitlow Jw, Wagner AR (1984) Memory and habituation, In Peeke HVS, Petrinovich L (eds) Habituation. sensitization and behavior. Academic Press, New York, pp 103–153
Acknowledgments
This work was supported by FONCYT (grant PICT-1492; grant PICT2006-01161), CONICET (grant PIP-11220100100169) and UBACYT (grant X-198). We thank Dr. Liliana Orelli for language correction and Angel Vidal for technical assistance.
Ethical standards
Experimental procedures are in compliance with the National Institutes of Health Guide for Care and Use of Laboratory Animals (USA), and the Argentinean guidelines on the ethical use of animals. All the experiments performed in this work were planned minimising the number of animals used and their suffering.
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The authors declare that they have no conflict of interest.
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María Sol Fustiñana and Martín Carbó Tano contributed equally to this paper.
Arturo Romano and María Eugenia Pedreira contributed equally to this paper.
In memoriam to our science mentor Héctor Maldonado. A true scientist who inspired us with his illimitable creativity.
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Fustiñana, M.S., Carbó Tano, M., Romano, A. et al. Contextual Pavlovian conditioning in the crab Chasmagnathus . Anim Cogn 16, 255–272 (2013). https://doi.org/10.1007/s10071-012-0570-2
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DOI: https://doi.org/10.1007/s10071-012-0570-2