Abstract
The effects of protein synthesis inhibitors on the reactivation of an associative skill consisting of refusing a particular food by common snails were studied. Animals were given single injections of a protein synthesis inhibitor (cycloheximide at 0.6 mg/snail or anisomycin at 0.4 mg) 24 h after three days of training, and were then presented with a “reminding” stimulus (the “conditioned reflex” food-banana) and tested for retention of the skill. Observations revealed an impairment of reproduction of the acquired skill 2.5 h after the “reminder, ” with spontaneous restoration at 4.5–5.5 h. Other snails were given single 1.8-mg doses of cycloheximide or three 0.6-mg doses with intervals of 2 h. “Reminders” were presented after each injection. In these conditions, impairment of reproduction of the conditioned reflex also appeared 2.5 h after the first “reminder, ” though amnesia lasted at least 30 days and repeat training of the animals produced only partial recovery of the skill. Thus, we have provided the first demonstration that recovery of a long-term memory “trace” on exposure to relatively low doses of protein synthesis inhibitors produces transient and short-lived amnesia, lasting 2–3 h, while long-term, irreversible amnesia occurrs after longer-lasting or more profound suppression of protein synthesis. These results suggest that the “reminding” process induces reconsolidation of the “ initial” memory, suppression of which by protein synthesis inhibitors leads to “erasure” of the memory “trace” and impairs consolidation on repeat training.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
T. Kh. Gainutdinova, R. R. Tagirova, A. I. Ismailova, L. N. Muranova, Kh. L. Gainutdinov, and P. M. Balaban, “Protein synthesis-dependent reactivation of a contextual conditioned reflex in the common snail,” Zh. Vyssh. Nerv. Deyat., 54, No. 6, 785–790 (2004).
K. V. Anokhin, A. A. Tiunova, and S. P. R. Rose, “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, No. 11, 1759–1765 (2002).
P. M. Balaban, “Declarative and procedural memory in animals with simple nervous systems,” in: Psychology at the Turn of the Millennium, C. Hofsten (ed.), Academic Press, Stockholm (2002), pp. 1–28.
B. Bozon, S. Davis, and S. Laroche, “A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval,” Neuron, 40, No. 4, 695–701 (2003).
F. M. Child, H. T. Epstein, A. M. Kuzirian, and D. L. Alkon, “Memory reconsolidation in Hermissenda,” Biol. Bull., 205, No. 2, 218–219 (2003).
H. P. Davis and L. R. Squire, “Protein synthesis and memory: a review,” Psychol. Bull., 96, No. 4, 519–559 (1984).
J. Debiec, J. E. LeDoux, and K. Nader, “Cellular and systems reconsolidation in the hippocampus,” Neuron, 36, No. 3, 527–538 (2002).
Y. Dudai and M. Eisenberg, “Rites of passage of the engram: reconsolidation and the lingering consolidation hypothesis,” Neuron, 44, No. 1, 93–100 (2004).
S. Duvarci and K. Nader, “Characterization of fear memory reconsolidation,” J. Neurosci., 24, No. 42, 9269–9275 (2004).
L. M. Igaz, M. R. M. Vianna, J. H. Medina, and I. Izquierdo, “Two time periods of hippocampal mRNA synthesis are required for memory consolidation of fear-motivated learning,” J. Neurosci., 22, No. 15, 6781–6789 (2002).
M. C. Inda, J. M. Delgado-Garcia, and A. M. Carrion, “Acquisition, consolidation, reconsolidation, and extinction of eyelid conditioning responses require de novo protein synthesis,” J. Neurosci., 25, No. 8, 2070–2080 (2005).
K. M. Lattal and T. Abel, “Behavioral impairments caused by injections of the protein synthesis inhibitor anisomycin after contextual retrieval reverse with time,” Proc. Natl. Acad. Sci. USA, 101, No. 13, 4667–4672 (2004).
P. G. Montarolo, P. Goelet, V. F. Castellucci, J. Morgan, E. R. Kandel, and S. Schasher, “A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia,” Science, 234, No. 4781, 1249–1254 (1986).
K. Nader, “Memory traces unbound,” Trends Neurosci., 26, No. 2, 65–72 (2003).
M. E. Pedreira, L. M. Perez-Cuesta, and H. Maldonado, “Reactivation and reconsolidation of long-term memory in the crab Chasmagnathus: protein synthesis requirement and mediation by NMDA-type glutamatergic receptors,” J. Neurosci., 22, No. 18, 8305–8311 (2002).
S. Sangha, A. Scheibenstock, and K. Lukowiak, “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, No. 22, 8034–8040 (2003).
S. J. Sara, “Retrieval and reconsolidation: toward a neurobiology of remembering,” Learn. Mem., 7, No. 2, 73–84 (2000).
M. J. Summer, S. F. Crowe, and K. T. Ng, “Memory retrieval in the day-old chick: a psychobiological approach,” Neurosci. Biobehav. Rev., 27, 219–231 (2003).
A. Suzuki, S. A. Josselyn, P. W. Frankland, S. Masushige, A. J. Silva, and S. Kida, “Memory reconsolidation and extinction have distinct temporal and biochemical signatures,” J. Neurosci., 24, No. 20, 4787–4795 (2004).
A. A. Tiunova, K. V. Anokhin, and S. P. Rose, “Two critical periods of protein and glycoprotein synthesis in memory consolidation for visual categorization learning in chick,” Learn. Mem., 4, No. 4, 401–410 (1998).
Author information
Authors and Affiliations
Corresponding author
Additional information
__________
Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 92, No. 9, 1058–1068. September, 2006.
Rights and permissions
About this article
Cite this article
Solntseva, S.V., Nikitin, V.P., Kozyrev, S.A. et al. Effects of protein synthesis inhibitors during reactivation of associative memory in the common snail induces reversible and irreversible amnesia. Neurosci Behav Physiol 37, 921–928 (2007). https://doi.org/10.1007/s11055-007-0100-x
Received:
Issue Date:
DOI: https://doi.org/10.1007/s11055-007-0100-x