Differential Induction of Long-Term Synaptic Facilitation by Spaced and Massed Applications of Serotonin at Sensory Neuron Synapses of Aplysia californica

Mauelshagen, Juliane; Sherff, Carolyn M.; Carew, Thomas J.

doi:10.1101/lm.5.3.246

PreprintCited by 129Neuroscience and Neuropharmacology ResearchMemory and Neural MechanismsNeurobiology and Insect Physiology Research

Differential Induction of Long-Term Synaptic Facilitation by Spaced and Massed Applications of Serotonin at Sensory Neuron Synapses of Aplysia californica

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Mauelshagen, Juliane, Sherff, Carolyn M., Carew, Thomas J.·1998·Learning & Memory

DOI 10.1101/lm.5.3.246PMC PMC313806

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Abstract

Serotonin (5HT)-induced facilitation of synaptic transmission from tail sensory neurons (SNs) to motor neurons (MNs) in the marine mollusc Aplysia provides a cellular model of short- and long-term memory for behavioral sensitization of the tail withdrawal reflex. Synaptic facilitation at these synapses occurs in three temporal phases: short-term (STF, lasting minutes), intermediate-term (ITF, lasting more than an hour), and long-term (LTF, lasting >24 hr). STF, ITF, and LTF differ in their induction requirements: A single brief exposure of 5HT induces STF, whereas five applications are required for ITF and LTF. Moreover, STF and LTF can be induced independently. Different forms of memory often show differential sensitivity to the pattern of training trials. To begin to explore this effect at a cellular level, we examined ITF and LTF induced by one of two patterns of 5HT application: a spaced pattern (five 5-min exposures with an interval of 15 min) or a massed pattern (one continuous 25-min application). The spaced and massed patterns both induced ITF; however, spaced 5HT application was significantly more reliable at inducing LTF than was massed application. Thus, whereas induction of ITF and LTF require similar amounts of 5HT, the cellular mechanisms underlying the induction of LTF are more sensitive to the pattern of the induction trials. In the massed group, further analysis revealed a relationship between the expression of ITF and the subsequent expression of LTF, suggesting that these two processes may be mechanistically related.

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Spaced training leads to improved memory in invertebrates such as Aplysia californica, Drosophila melanogaster and bees, and in rodents and non-human primates.
“Spaced training also leads to improved memory in invertebrates, such as the mollusk Aplysia californica11–14, Drosophila melanogaster15,16 and bees17, and in rodents18,19 and non-human primates20,21.”
From The right time to learn: Mechanisms and optimization of spaced learning (2016) · cites this paper as [14]
The massed protocol result is consistent with data that massed 5-HT application fails to produce LTF.
“The simulations determined that, of these protocols, a massed protocol (FIG. 4b) produced the lowest peak value of inducer, consistent with data that massed 5-HT application fails to produce LTF14.”
From The right time to learn: Mechanisms and optimization of spaced learning (2016) · cites this paper as [14]
A massed training protocol (25 min continuous 5-HT) produced significantly less LTF than a spaced protocol (five 5-min pulses of 5-HT).
“However, the model described in Fig. 1a was also compatible with previous empirical results in which a massed training protocol (25 min continuous 5-HT) produced significantly less LTF than a spaced protocol (five, 5-min pulses of 5-HT)29.”
From Computational design of enhanced learning protocols (2012) · cites this paper as [29]

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Authors: Mauelshagen, J., Sherff, C. M., & Carew, T. J.
Affiliations: Yale University (US)
ORCID: Carew, Thomas J.
Venue: Learning & Memory
Publisher: Cold Spring Harbor Laboratory
Published: 1998-07-01
Volume: 5
Issue: 3
Pages: 246-256
ISSN: 1072-0502 (ISSN-L)
1549-5485
DOI: 10.1101/lm.5.3.246
PMC: PMC313806
OpenAlex: W2175525622
Cited by: 129
References: 50
Citations by year: 2026: 2 · 2024: 5 · 2023: 2 · 2022: 2 · 2021: 4 · 2020: 9 · 2019: 3 · 2018: 1 · 2017: 5 · 2016: 5 · 2015: 7 · 2014: 5 · 2013: 5 · 2012: 6
Type: posted content
Language: en
Open access: bronze
doi.org
Locations: Learning & Memory (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Science Foundation
Deutsche Forschungsgemeinschaft
National Institutes of Health
National Institute of Mental Health (MH41083, R01MH041083, R37MH041083, N01 MH012004)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
Keywords: serotonin, short-term facilitation, Aplysia californica, tail withdrawal reflex, behavioral sensitization, synaptic plasticity
MeSH terms: Animals, Aplysia, Motor Neurons, Neuronal Plasticity, Neurons, Afferent, Probability, Reflex, Serotonin, Synapses, Excitatory Postsynaptic Potentials

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Differential Induction of Long-Term Synaptic Facilitation by Spaced and Massed Applications of Serotonin at Sensory Neuron Synapses of Aplysia californica

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