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Serotonin produces long-term changes in the excitability of Aplysia sensory neurons in culture that depend on new protein synthesis

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Dale, N, Kandel, ER, Schacher, S·1987·The Journal of Neuroscience
DOI 10.1523/jneurosci.07-07-02232.1987PMC PMC6568947
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Abstract

When isolated and grown in cell culture, the sensory and motor neurons of the gill withdrawal reflex of Aplysia readily form synaptic connections. Repeated exposures to 5-HT cause facilitation of the synaptic connections between co-cultured sensory and motor neurons lasting at least 24 hr. As a first step toward understanding the locus and the mechanisms underlying this long-term synaptic facilitation, we have examined the membrane excitability of the isolated presynaptic sensory neurons grown alone in dissociated cell culture. Four repeated applications of 1 microM 5-HT caused a significant increase in the excitability of sensory neurons, lasting at least 24 hr. This resembles the short-term changes in excitability seen in response to a single application of 5-HT. Unlike the short-term effect, this long-lasting change was blocked by exposure of the cells during the 5-HT treatment to 10 microM anisomycin, an inhibitor of protein synthesis. Thus, like the synaptic facilitation, the long-term change in excitability of the isolated presynaptic neurons differs from the short-term in requiring the synthesis of new protein. This finding suggests that the sensory neuron uses gene products to modulate membrane currents in its long- term response to repeated external stimuli that are not required in its short-term response to a single stimulus.

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Crossref · 10.1523/jneurosci.07-07-02232.1987

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Figure 1 Repeated application of 5-HT causes a long-term change in the excitability of sensory neurons in synaptic contact with L7 motor neurons. The excitability of a sensory neuron recorded before and 24 hr after 5-HT treatment.
Figure 1 Repeated application of 5-HT causes a long-term change in the excitability of sensory neurons in synaptic contact with L7 motor neurons. The excitability of a sensory neuron recorded before and 24 hr after 5-HT treatment.CC-BY-NC-SA · From the PDF
'-ens L- () ee e e ei o s es a o n " y s e o ei- set nt A2, Examples of the spike trains evoked by current injection corresponding to the numbered points on the graph. B, In a control sensory neuron, the excitability declines over 24 hr. Figure 2.
'-ens L- () ee e e ei o s es a o n " y s e o ei- set nt A2, Examples of the spike trains evoked by current injection corresponding to the numbered points on the graph. B, In a control sensory neuron, the excitability declines over 24 hr. Figure 2.CC-BY-NC-SA · From the PDF
Image 3
CC-BY-NC-SA · From the PDF
Figure 4 Long-term changes in excitability are blocked by the protein synthesis inhibitor anisomycin. A, In the presence of 10 μM anisomycin, 5-HT cannot evoke a long-ter change iette o id s e s e e o a e ey ie te o sto rn ie e rs s s n and 24 hr later ().
Figure 4 Long-term changes in excitability are blocked by the protein synthesis inhibitor anisomycin. A, In the presence of 10 μM anisomycin, 5-HT cannot evoke a long-ter change iette o id s e s e e o a e ey ie te o sto rn ie e rs s s n and 24 hr later ().CC-BY-NC-SA · From the PDF
Figure 5 Neither 5-HT plus anisomycin nor anisomycin alone causes significant long-term changes in the excitability of sensory neurons at any of the interpolated current levels.
Figure 5 Neither 5-HT plus anisomycin nor anisomycin alone causes significant long-term changes in the excitability of sensory neurons at any of the interpolated current levels.CC-BY-NC-SA · From the PDF
Figure 6 Short-term changes in excitability do not require protein synthesis. A, Recording from an isolated sensory neuron that has been exposed to 10 μm anisomycin for 2 hr. The injection of depolarizing current (bottom trace) evokes 2 action potentials. B, One minute after the application of 1 μM 5-HT, the same current pulse evokes a continuous train of pulses. Note how the afterpotentials following the depolarizing pulse have been altered by the 5-HT. C, After 2 min of washing, the same current pulse evokes only 3 action potentials. The membrane potential of the cell and the amplitude of the injected current pulse shown in D are the same as in A-C.
Figure 6 Short-term changes in excitability do not require protein synthesis. A, Recording from an isolated sensory neuron that has been exposed to 10 μm anisomycin for 2 hr. The injection of depolarizing current (bottom trace) evokes 2 action potentials. B, One minute after the application of 1 μM 5-HT, the same current pulse evokes a continuous train of pulses. Note how the afterpotentials following the depolarizing pulse have been altered by the 5-HT. C, After 2 min of washing, the same current pulse evokes only 3 action potentials. The membrane potential of the cell and the amplitude of the injected current pulse shown in D are the same as in A-C.CC-BY-NC-SA · From the PDF
Figure 7 Summary bar chart showing the mean difference in the maximum number of spikes before and 24 hr after the 4 treatments. Bars represent 1 SEM.
Figure 7 Summary bar chart showing the mean difference in the maximum number of spikes before and 24 hr after the 4 treatments. Bars represent 1 SEM.CC-BY-NC-SA · From the PDF

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  1. Frost, W. N., V. F. Castellucci, R. D. Hawkins, and E. R. Kandel (1985) The monosynaptic connections from the sensory neurons participate in the storage of long-term memory for sensitization of the gill-and siphon-withdrawal reflex in Aplysia. Proc. Natl. Acad. Sci. USA 82: 8266-8269.

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Metadata

Authors
Dale, N., Kandel, E., & Schacher, S.
Affiliations
Howard Hughes Medical Institute (US)
ORCID
Venue
The Journal of Neuroscience
Publisher
Society for Neuroscience
Published
1987-07-01
Volume
7
Issue
7
Pages
2232-2238
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
DOI
10.1523/jneurosci.07-07-02232.1987
PMC
PMC6568947
OpenAlex
W1625157937
Cited by
118
References
9
Citations by year
2026: 1 · 2024: 1 · 2023: 2 · 2022: 1 · 2021: 1 · 2020: 1 · 2019: 1 · 2018: 1 · 2017: 1 · 2016: 1 · 2014: 5 · 2013: 2 · 2012: 2
FWCI
3.06
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
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, sensory neuron excitability, Aplysia, gill-withdrawal reflex, synaptic facilitation, long-term synaptic plasticity, anisomycin, presynaptic neurons, membrane currents, sensory-motor synapses
MeSH terms
Action Potentials, Animals, Anisomycin, Aplysia, Cells, Cultured, Gills, Nerve Tissue Proteins, Neurons, Afferent, Serotonin

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