Skip to main content
Log in

Increase in serotonin precursor levels reinstates the context memory during reconsolidation

  • Original Article
  • Published:
Invertebrate Neuroscience

Abstract

In the present study, we tested possible ways of modification of the context long-term memory using the reconsolidation as a tool. Recently, using a depletion of the serotonin content, it was shown that the reinforcing neurotransmitter serotonin is necessary for successful repeated reconsolidation of context memory in terrestrial snails Helix lucorum (Balaban et al. in Sci Rep 6:36933, 2016), and in the present study, we investigated effects of serotonin increase in memory maintenance by injection of the serotonin precursor 5-hydroxytryptophan (5-HTP). We studied reinstatement of the context memory after its impairment during reconsolidation with a protein synthesis blocker anisomycin (ANI) or with a specific inhibitor of protein-kinase Mζ (ZIP). It was observed that applications of 5-HTP alone, known to increase the release of serotonin, or reactivation of memory alone did not restore the ZIP- or ANI-impaired context memory, while combination of the 5-HTP + reactivation of memory effectively reinstated the context memory. The data obtained confirmed the assumption that serotonin/reinforcing transmitter is a part of successful reconsolidation necessary for memory maintenance, demonstrated possible ways of long-term memory regulation during the reconsolidation process.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alberini CM, Kandel ER (2014) The regulation of transcription in memory consolidation. Cold Spring Harb Perspect Biol 7(1):a021741

    Article  PubMed  Google Scholar 

  • Andrianov VV, Bogodvid TK, Deryabina IB, Golovchenko AN, Muranova LN, Tagirova RR et al (2015) Modulation of defensive reflex conditioning in snails by serotonin. Front Behav Neurosci 9:1–12

    Article  Google Scholar 

  • Balaban P (1993) Behavioral neurobiology of learning in terrestrial snails. Prog Neurobiol 41:1–19

    Article  CAS  PubMed  Google Scholar 

  • Balaban PM (2002) Cellular mechanisms of behavioral plasticity in terrestrial snail. Neurosci Biobehav Rev 26:597–630

    Article  CAS  PubMed  Google Scholar 

  • Balaban PM (2017) Molecular mechanisms of memory modification. Zhurnal Vysshei Nervnoi Deyatelnosti Imeni I.P Pavlova 67:131–140

    Google Scholar 

  • Balaban P, Bravarenko N (1993) Long-term sensitization and environmental conditioning in terrestrial snails. Exp Brain Res 96:487–493

    Article  CAS  PubMed  Google Scholar 

  • Balaban PM, Vehovszky A, Maximova OA, Zakharov IS (1987) Effect of 5,7-dihydroxytryptamine on the food-aversive conditioning in the snail Helix Lucorum L. Brain Res 404:201–210

    Article  CAS  PubMed  Google Scholar 

  • Balaban PM, Roshchin M, Timoshenko AKh, Zuzina AB, Lemak M, Ierusalimsky VN et al (2015) Homolog of protein kinase Mzeta maintains context aversive memory and underlying long-term facilitation in terrestrial snail Helix. Front Cell Neurosci 9:222

    Article  PubMed  PubMed Central  Google Scholar 

  • Balaban PM, Vinarskaya AK, Zuzina AB, Ierusalimsky VN, Malyshev AY (2016) Impairment of the serotonergic neurons underlying reinforcement elicits extinction of the repeatedly reactivated context memory. Sci Rep 6:36933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bauer EP (2015) Serotonin in fear conditioning processes. Behav Brain Res 277:68–77

    Article  CAS  PubMed  Google Scholar 

  • Bogodvid TK, Andrianov VV, Deryabina IB, Muranova LN, Silantyeva DI, Vinarskaya A et al (2017) Responses of withdrawal interneurons to serotonin applications in naïve and learned snails are different. Front Cell Neurosci 11:403

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen S, Cai D, Pearce K, Sun PY, Roberts AC, Glanzman DL (2014) Reinstatement of long-term memory following erasure of its behavioral and synaptic expression in Aplysia. ELife 3:e03896

    Article  PubMed  PubMed Central  Google Scholar 

  • Colwill RM, Absher RA, Roberts ML (1988) Context-US learning in Aplysia californica. J Neurosci 8:4434–4439

    Article  CAS  PubMed  Google Scholar 

  • Cottrell GA, Powell B (1971) Formation of serotonin by isolated serotonin-containing neurons and by isolated non-amine-containing neurons. J Neurochem 18(9):1695–1697

    Article  CAS  PubMed  Google Scholar 

  • Debiec J, LeDoux JE, Nader K (2002) Cellular and systems reconsolidation in the hippocampus. Neuron 36:527–538

    Article  CAS  PubMed  Google Scholar 

  • Dyakonova VE, Chistopolsky IA, Dyakonova TL, Vorontsov DD, Sakharov DA (2009) Direct and decarboxylation-dependent effects of neurotransmitter precursors on firing of isolated monoaminergic neurons. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 195:515–527

    Article  CAS  PubMed  Google Scholar 

  • Fickbohm DJ, Katz PS (2000) Paradoxical actions of the serotonin precursor 5-hydroxytryptophan on the activity of identified serotonergic neurons in a simple motor circuit. J Neurosci 20(4):1622–1634

    Article  CAS  PubMed  Google Scholar 

  • Fickbohm DJ, Spitzer N, Katz PS (2005) Pharmacological manipulation of serotonin levels in the nervous system of the opisthobranch mollusc Tritonia diomedea. Biol Bull 209(1):67–74

    Article  CAS  PubMed  Google Scholar 

  • Gainutdinova TKh, Tagirova RR, Ismailova AI, Muranova LN, Gainutdinov KhL, Balaban PM (2006) Protein synthesis-dependent reactivation of a contextual conditioned reflex in the common snail. Neurosci Behav Physiol 36:203–207

    Article  PubMed  Google Scholar 

  • Gartside SE, Cowen PJ, Sharp T (1992) Effect of 5-hydroxy-l-tryptophan on the release of 5-HT in rat hypothalamus in vivo as measured by microdialysis. Neuropharmacology 31:9–14

    Article  CAS  PubMed  Google Scholar 

  • Guan Z, Giustetto M, Lomvardas S, Kim JH, Miniaci MC, Schwartz JH et al (2002) Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell 111(4):483–493

    Article  CAS  PubMed  Google Scholar 

  • Haney J, Lukowiak K (2001) Context learning and the effect of context on memory retrieval in Lymnaea. Learn Mem 8:35–43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynn-Bullock CP, Welshhans K, Pallas SL, Katz PS (2004) The effect of oral 5-HTP administration on 5-HTP and 5-HT immunoreactivity in monoaminergic brain regions of rats. J Chem Neuroanat 27(2):129–138

    Article  CAS  PubMed  Google Scholar 

  • Marinesco S, Wickremasinghe N, Kolkman KE, Carew TJ (2004) Serotonergic modulation in aplysia. II. Cellular and behavioral consequences of increased serotonergic tone. J Neurophysiol 92:2487–2496

    Article  CAS  PubMed  Google Scholar 

  • McCaman MW, Ono JK, McCaman RE (1984) 5-Hydroxytryptamine measurements in molluscan ganglia and neurons using a modified radioenzymatic assay. J Neurochem 43(1):91–99

    Article  CAS  PubMed  Google Scholar 

  • Meneses A (2015) Serotonin, neural markers, and memory. Front Pharmacol 6:143

    Article  PubMed  PubMed Central  Google Scholar 

  • Nader K, Hardt O (2009) A single standard for memory: the case for reconsolidation. Nat Rev Neurosci 10:224–234

    Article  CAS  PubMed  Google Scholar 

  • Pearce K, Cai D, Roberts AC, Glanzman DL (2017) Role of protein synthesis and DNA methylation in the consolidation and maintenance of long-term memory in Aplysia. Elife 6:e18299

    Article  PubMed  PubMed Central  Google Scholar 

  • Pratelli M, Migliarini S, Pelosi B, Napolitano F, Usiello A, Pasqualetti M (2017) Perturbation of serotonin homeostasis during adulthood affects serotonergic neuronal circuitry. eNeuro 4(2):1–13

    Article  Google Scholar 

  • Sacktor TC (2011) How does PKMzeta maintain long-term memory? Nat Rev Neurosci 12:9–15

    Article  CAS  PubMed  Google Scholar 

  • Sacktor T (2012) Memory maintenance by PKMζ — an evolutionary perspective. Mol Brain 5:31–41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sara SJ (2000) Strengthening the shaky trace through retrieval. Nat Rev Neurosci 1:212–213

    Article  CAS  PubMed  Google Scholar 

  • Tsyganov VV (2010) Coordination between locomotor and respiratory rhythms in the great ramshorn snail Planorbarius corneus: transmitter-dependent modifications. Izv Akad Nauk Ser Biol 3:355–362

    Google Scholar 

Download references

Acknowledgements

This study was supported by Russian Foundation for Basic Research Grants 17-04-01175, 17-00-00216, Grant of Russian Science Foundation 19-75-10067.

Author information

Authors and Affiliations

Authors

Contributions

ABZ, AKV and PMB contributed equally.

Corresponding author

Correspondence to Pavel M. Balaban.

Ethics declarations

Conflict of interests

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving snails were in accordance with the ethical standards and approved (#012 from 10.10.2014) by Ethical Committee of the Institute of Higher Nervous Activity and Neurophysiology of Russian Academy of Sciences.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zuzina, A.B., Vinarskaya, A.K. & Balaban, P.M. Increase in serotonin precursor levels reinstates the context memory during reconsolidation. Invert Neurosci 19, 8 (2019). https://doi.org/10.1007/s10158-019-0227-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10158-019-0227-9

Keywords

Navigation