Identification of a Novel Retrieval-Dependent Memory Process in the Crab Neohelice granulata
Abstract
Fully consolidated associative memories may be altered by alternative retrieval dependent memory processes. While a brief exposure to the conditioned stimulus (CS) can trigger reconsolidation of the original memory, a prolonged CS exposure will trigger memory extinction. The conditioned response is maintained after reconsolidation, but is inhibited after extinction, presumably by the formation of a new inhibitory memory trace. In rats and humans, it has been shown that CS exposure of intermediate duration leave the memory in an insensitive or limbo state. Limbo is characterised by the absence of reconsolidation or extinction. Here we investigated the evolutionary conserved nature of limbo using a contextual Pavlovian conditioning (CPC) memory paradigm in the crab Neohelice granulata . In animals with fully consolidated CPC memory, systemic administration of the protein synthesis inhibitor cycloheximide after 1 CS presentation disrupted the memory, presumably by interfering with memory reconsolidation. The same intervention given after 320 CSs prevented CPC memory extinction. Cycloheximide had no behavioural effect when administered after 80 CS presentations, a protocol that failed to extinguish CPC memory. Also, we observed that a stronger CPC memory engaged reconsolidation after 80 CS instead of limbo, indicating that memory strength affects the parametrical conditions to engage either reconsolidation or limbo. Altogether, these results indicate that limbo is an evolutionary conserved memory process segregating reconsolidation from extinction in the number of CSs space. Limbo appears as an intrinsic component of retrieval dependent memory processing, with a key function in the transition from memory maintenance to inhibition. Author statement (CRediT Roles): Santiago A. Merlo: Conceptualization, Data curation, Formal Analysis, Investigation, Software, Validation, Visualization, Writing – original draft, Writing – review & editing. Jimena Santos: Investigation, Writing – review & editing. Maria Eugenia Pedreira: Conceptualization, Funding acquisition, Project administration, Resources, Supervision, Validation, Writing – original draft, Writing – review & editing. Emiliano Merlo: Conceptualization, Funding acquisition, Project administration, Resources, Supervision, Validation, Writing – original draft, Writing – review & editing.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Protein synthesis inhibition did not affect conditioned responding when administered after an intermediate number of CS re-exposures in the crab Neohelice granulatus.
“protein synthesis inhibition, a “gold standard” amnestic manipulation, did not affect conditioned responding when administered after an intermediate number of CS re-exposures in the crab Neohelice granulatus (Merlo et al., 2019).”
From Retrieval-Dependent Mechanisms Affecting Emotional Memory Persistence: Reconsolidation, Extinction, and the Space in Between (2020) · cites this paper as Merlo et al., 2019
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Context and Behavioral Processes in Extinction: Table 1.
Bouton, M. E. (2004) · Learning & Memory · doi:10.1101/lm.78804 · Cited by 1,808 · see citing works
Memory Reconsolidation and Extinction Have Distinct Temporal and Biochemical Signatures
Suzuki, A., Josselyn, S. A., Frankland, P. W., Masushige, S., Silva, A. J., & Kida, S. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5491-03.2004 · Cited by 1,127 · see citing works
Statistical Evidence in Experimental Psychology: An Empirical Comparison Using 855 <i>t</i> Tests
Wetzels, R., Matzke, D., Lee, M. D., Rouder, J. N., Iverson, G. J., & Wagenmakers, E.-J. (2011) · Perspectives on Psychological Science · doi:10.1177/1745691611406923 · Cited by 945 · see citing works
The Consolidation and Transformation of Memory
Dudai, Y., Karni, A., & Born, J. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.004 · Cited by 741 · see citing works
Stability of retrieved memory: Inverse correlation with trace dominance
Eisenberg, M., Kobilo, T., Berman, D. E., & Dudai, Y. (2003) · Science · doi:10.1126/science.1086881 · Cited by 518 · see citing works
Reconsolidation and Extinction of Conditioned Fear: Inhibition and Potentiation
Lee, J. L. C., Milton, A. L., & Everitt, B. J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2466-06.2006 · Cited by 479 · see citing works
Protein Synthesis Subserves Reconsolidation or Extinction Depending on Reminder Duration
Pedreira, M. E., & Maldonado, H. (2003) · Neuron · doi:10.1016/s0896-6273(03)00352-0 · Cited by 406 · see citing works
Self-citationPedreira, M. E., Pérez-Cuesta, L. M., & Maldonado, H. (2004) · Learning & Memory · doi:10.1101/lm.76904 · Cited by 367 · see citing works
Self-citationDeep homology of arthropod central complex and vertebrate basal ganglia.
Strausfeld, N. J., & Hirth, F. (2013) · Science · doi:10.1126/science.1231828 · Cited by 354 · see citing works
Merlo, E., Milton, A. L., Goozée, Z. Y., Theobald, D. E., & Everitt, B. J. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.4001-13.2014 · Cited by 242 · see citing works
Self-citationPrediction error demarcates the transition from retrieval, to reconsolidation, to new learning
Sevenster, D., Beckers, T., & Kindt, M. (2014) · Learning & Memory · doi:10.1101/lm.035493.114 · Cited by 161 · see citing works
Memory Reconsolidation Mediates the Updating of Hippocampal Memory Content
Lee, J. L. C. (2010) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2010.00168 · Cited by 153 · see citing works
Reconsolidation in humans opens up declarative memory to the entrance of new information
Forcato, C., Rodríguez, M. L. C., Pedreira, M. E., & Maldonado, H. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.08.006 · Cited by 147 · see citing works
Self-citationControl of the establishment of aversive memory by calcineurin and Zif268
Baumgärtel, K., Genoux, D., Welzl, H., Tweedie‐Cullen, R. Y., Koshibu, K., Livingstone-Zatchej, M., Mamie, C., & Mansuy, I. M. (2008) · Nature Neuroscience · doi:10.1038/nn.2113 · Cited by 130 · see citing works
Psychological and Neural Mechanisms of Experimental Extinction: A Selective Review
Delamater, A., & Westbrook, R. F. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.09.016 · Cited by 110 · see citing works
Frenkel, L., Maldonado, H., & Delorenzi, A. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04373.x · Cited by 98 · see citing works
Enhancement of fear memory by retrieval through reconsolidation
Fukushima, H., Zhang, Y., Archbold, G., Ishikawa, R., Nader, K., & Kida, S. (2014) · eLife · doi:10.7554/elife.02736 · Cited by 97 · see citing works
The vascular circulation in the brain, optic lobes and thoracic ganglia of the crab Carcinus
Sandeman, D. C. (1967) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1967.0052 · Cited by 92 · see citing works
Repeated Labilization-Reconsolidation Processes Strengthen Declarative Memory in Humans
Forcato, C., Rodríguez, M. L. C., & Pedreira, M. E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023305 · Cited by 90 · see citing works
Self-citationMeyer, F., & Louilot, A. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00118 · Cited by 84 · see citing works
Cycloheximide inhibits context memory and long-term habituation in the crab Chasmagnathus
Pedreira, M. E., Dimant, B., Tomsic, D., Quesada-Allué, L. A., & Maldonado, H. (1995) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)00124-f · Cited by 74 · see citing works
Self-citationAbsence of Blood-Brain Barrier in a Crustacean, Carcinus maenas L.
ABBOTT, J. (1970) · Nature · doi:10.1038/225291b0 · Cited by 73 · see citing works
Alfei, J. M., Ferrer Monti, R. I., Molina, V. A., Bueno, A. M., & Urcelay, G. P. (2015) · Learning & Memory · doi:10.1101/lm.038513.115 · Cited by 71 · cited 1× · see citing works
“In this case, limbo was found using GABA enhancer midazolam (Alfei et al., 2015; Franzen et al., 2019) or NMDAR antagonist MK-801 (Cassini et al.”
MethodReconsolidation and extinction of an appetitive pavlovian memory
Flavell, C. R., & Lee, J. L. C. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.04.009 · Cited by 53 · see citing works
Pereyra, P., Portino, E. G., & Maldonado, H. (2000) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1999.3945 · Cited by 48 · see citing works
On the transition from reconsolidation to extinction of contextual fear memories
Cassini, L. F., Flavell, C. R., Amaral, O. B., & Lee, J. L. C. (2017) · Learning & Memory · doi:10.1101/lm.045724.117 · Cited by 47 · see citing works
Catecholamine degradation in the hemolymph of the Chinese crab, Eriocheir Sinensis
Hoeger, U., & Florey, E. (1989) · Comparative Biochemistry and Physiology Part C Comparative Pharmacology · doi:10.1016/0742-8413(89)90062-5 · Cited by 41 · see citing works
Merlo, E., Milton, A. L., & Everitt, B. J. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.3273-17.2018 · Cited by 41 · see citing works
Self-citationDisrupting Reconsolidation of Fear Memory in Humans by a Noradrenergic β-Blocker
Kindt, M., Soeter, M., & Sevenster, D. (2014) · Journal of Visualized Experiments · doi:10.3791/52151 · Cited by 33 · see citing works
Franzen, J. M., Giachero, M., & Bertoglio, L. J. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.03.035 · Cited by 26 · see citing works
López, M. A., Santos, M. J., Cortasa, S. A., Fernández, R. S., Tano, M. C., & Pedreira, M. E. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.10.016 · Cited by 25 · see citing works
Self-citationContextual Pavlovian conditioning in the crab Chasmagnathus
Fustiñana, M. S., Tano, M. C., Romano, A. G., & Pedreira, M. E. (2012) · Animal Cognition · doi:10.1007/s10071-012-0570-2 · Cited by 20 · see citing works
Self-citationKinase and phosphatase engagement is dissociated between memory formation and extinction
Pagani, M. R., & Merlo, E. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00038 · Cited by 14 · see citing works
Self-citationDisrupting Reconsolidation of Fear Memory in Humans by a Noradrenergic β-Blocker
Kindt, M., Soeter, M., & Sevenster, D. (2014) · Journal of Visualized Experiments · doi:10.3791/52151-v · Cited by 3 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [17]17. Jeffreys, H. (1961). Theory of probability (3d ed.). Oxford,: Clarendon Press.
Cited by
Sorted by citations
Vaverková, Z., Milton, A. L., & Merlo, E. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.574358 · Cited by 27 · see citing works
“As extinction relies on the formation of a new inhibitory memory, many mechanisms supporting extinction acquisition and consolidation have common and distinctive partners compared to the consolidation of the CS-US memory (for a review see Pagani and Merlo, 2019).”
BackgroundInfluentialSelf-citationMemory persistence: from fundamental mechanisms to translational opportunities
Merlo, S. A., Belluscio, M., Pedreira, M. E., & Merlo, E. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-02808-z · Cited by 32 · see citing works
“Memory age and strength modulate the relationship between PE, memory maintenance and inhibition, with older and stronger memories requiring longer PE signals to undergo memory reconsolidation or extinction [46, 56] (for a review see [15]).”
BackgroundSelf-citationOver the Edge: Extending the duration of a reconsolidation intervention for spider fear
Filmer, A. I., Peters, J., Bridge, L. A., Visser, R. M., & Kindt, M. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02020-x · Cited by 9 · see citing works
Turel, Z. B., Prados, J., & Urcelay, G. P. (2020) · Behavioural Processes · doi:10.1016/j.beproc.2020.104197 · Cited by 8 · see citing works
O'Neill, O. S., & Winters, B. D. (2025) · Neuroscience · doi:10.1016/j.neuroscience.2025.12.038 · Cited by 4 · see citing works
Gonzalez, H., Bloise, L., Maza, F. J., Molina, V. A., & Delorenzi, A. (2020) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2020.01.014 · Cited by 6 · see citing works
Maza, F. J., Urbano, F. J., & Delorenzi, A. (2022) · Scientific Reports · doi:10.1038/s41598-022-15502-1 · Cited by 5 · see citing works
- Authors
- Merlo, S. A., Santos, M. J., Pedreira, M. E., & Merlo, E.
- ORCID
- Merlo, Emiliano
- Publisher
- openRxiv
- Published
- 2019-12-19
- Semantic Scholar
- 11383631ca06e2fb862ace19205e4f0694a20b2c
- References
- 0
- Type
- Preprint
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
