Reversal of synaptic depression by serotonin at Aplysia sensory neuron synapses involves activation of adenylyl cyclase.
Open accessAbstract
Facilitation of the monosynaptic connection between siphon sensory neurons and gill and siphon motor neuron contributes to sensitization and dishabituation of the gill and siphon withdrawal reflex in Aplysia. The facilitatory transmitter serotonin (5-HT) initiates two mechanisms that act in parallel to increase transmitter release from siphon sensory neurons. 5-HT acts, at least partly through cAMP, to broaden the presynaptic action potential. 5-HT also initiates a second process that facilitates depressed sensory neuron synapses by a mechanism independent of changes in action potential duration. Recent experiments indicated that either of two protein kinases, cAMP-dependent protein kinase A and protein kinase C, are capable of effectively activating this second facilitatory mechanism, restoring synaptic transmission in depressed synapses. We have used the adenylyl cyclase inhibitor SQ 22,536 [9-(tetrahydro-2-furyl)adenine or THFA] to explore the contribution of cAMP to the reversal of synaptic depression. THFA effectively inhibited both adenylyl cyclase activity in vitro and known cyclase-mediated effects in intact sensory neurons. THFA also completely blocked facilitation of depressed synapses by 5-HT. These results suggest that adenylyl cyclase plays a critical role in the reversal of synaptic depression that contributes to dishabituation in this system.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The text we found for this paper looks like another document, so the self-check wasn’t run.
Cites
The molecular heterogeneity of protein kinase C and its implications for cellular regulation
Nishizuka, Y. (1988) · Nature · doi:10.1038/334661a0 · Cited by 4,213 · see citing works
Habituation: a model phenomenon for the study of neuronal substrates of behavior
Thompson, R. F., & Spencer, W. A. (1966) · Psychological Review · doi:10.1037/h0022681 · Cited by 2,608 · see citing works
Protein Kinase C Contains a Pseudosubstrate Prototope in Its Regulatory Domain
House, C. M., & Kemp, B. E. (1987) · Science · doi:10.1126/science.3686012 · Cited by 1,008 · see citing works
Serotonin and cyclic AMP close single K+ channels in Aplysia sensory neurones
Siegelbaum, S. A., Camardo, J. S., & Kandel, E. R. (1982) · Nature · doi:10.1038/299413a0 · Cited by 655 · see citing works
A potent synthetic peptide inhibitor of the cAMP-dependent protein kinase.
Cheng, H., Kemp, B. E., Pearson, R. B., Smith, A. J., Misconi, L. Y., Patten, S. M. V., & Walsh, D. A. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)36041-6 · Cited by 592 · see citing works
HABITUATION OF THE AROUSAL REACTION
Sharpless, S. K., & Jasper, H. H. (1956) · Brain · doi:10.1093/brain/79.4.655 · Cited by 532 · see citing works
Brunelli, M., Castellucci, V. F., & Kandel, E. R. (1976) · Science · doi:10.1126/science.186870 · Cited by 522 · see citing works
Klein, M. E., & Kandel, E. R. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.11.6912 · Cited by 366 · see citing works
Klein, M. E., Camardo, J. S., & Kandel, E. R. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.18.5713 · Cited by 347 · see citing works
Glanzman, D. L., Mackey, S. L., Hawkins, R. D., Dyke, A. M., Lloyd, P. E., & Kandel, E. R. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-12-04200.1989 · Cited by 287 · see citing works
Shuster, M. J., Camardo, J. S., Siegelbaum, S. A., et al. (1985) · Nature · doi:10.1038/313392a0 · Cited by 263 · see citing works
cAMP Evokes Long-Term Facilitation in Aplysia Sensory Neurons That Requires New Protein Synthesis
Schacher, S., Castellucci, V. F., & Kandel, E. R. (1988) · Science · doi:10.1126/science.2454509 · Cited by 260 · see citing works
Abrams, T. W., Castellucci, V. F., Camardo, J. S., Kandel, E. R., & Lloyd, P. E. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.24.7956 · Cited by 254 · see citing works
Self-citationBernier, L., Castellucci, V. F., Kandel, E. R., & Schwartz, J. H. (1982) · Journal of Neuroscience · doi:10.1523/jneurosci.02-12-01682.1982 · Cited by 212 · see citing works
Mackey, S. L., Kandel, E., & Hawkins, R. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-12-04227.1989 · Cited by 193 · see citing works
Synaptic Plasticity and the Modulation of the Ca2+ Current
Klein, M., Shapiro, E., & Kandel, E. R. (1980) · Journal of Experimental Biology · doi:10.1242/jeb.89.1.117 · Cited by 187 · see citing works
Gingrich, K. J., & Byrne, J. H. (1985) · Journal of Neurophysiology · doi:10.1152/jn.1985.53.3.652 · Cited by 180 · see citing works
Hochner, B., Klein, M., Schacher, S., & Kandel, E. R. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.22.8794 · Cited by 168 · see citing works
Braha, O., Dale, N., Hochner, B., et al. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.5.2040 · Cited by 166 · see citing works
Parallel processing of short‐term memory for sensitization in Aplysia
Frost, W. N., Clark, G. A., & Kandel, E. R. (1988) · Journal of Neurobiology · doi:10.1002/neu.480190402 · Cited by 155 · see citing works
Sweatt, J. D., & Kandel, E. R. (1989) · Nature · doi:10.1038/339051a0 · Cited by 132 · see citing works
Intracellular Injection of cAMP Induces a Long-Term Reduction of Neuronal K + Currents
Scholz, K. P., & Byrne, J. H. (1988) · Science · doi:10.1126/science.2837826 · Cited by 130 · see citing works
Contributions of Two Types of Calcium Channels to Synaptic Transmission and Plasticity
Edmonds, B. W., Klein, M., Dale, N., et al. (1990) · Science · doi:10.1126/science.2174573 · Cited by 128 · see citing works
Serotonergic modulation of two potassium currents in the pleural sensory neurons of Aplysia
Baxter, D. A., & Byrne, J. H. (1989) · Journal of Neurophysiology · doi:10.1152/jn.1989.62.3.665 · Cited by 128 · see citing works
Ocorr, K. A., & Byrne, J. H. (1985) · Neuroscience Letters · doi:10.1016/0304-3940(85)90004-7 · Cited by 115 · see citing works
Sensitizing stimuli cause translocation of protein kinase C in Aplysia sensory neurons.
Sacktor, T. C., & Schwartz, J. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.5.2036 · Cited by 100 · see citing works
Davies, N. W., Lux, H. D., & Morad, M. (1988) · The Journal of Physiology · doi:10.1113/jphysiol.1988.sp017116 · Cited by 99 · see citing works
Dixon, D. B., & Atwood, H. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-12-04246.1989 · Cited by 97 · see citing works
Ke, K., Sossin, W., Sacktor, T. C., et al. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-08-02303.1991 · Cited by 86 · see citing works
Inhibition of adenylate cyclase in human blood platelets by 9-substituted adenine derivatives.
Dn, H., Mm, A., Mb, P., Goldenberg, H. J., & Mj, A. (1979) · PubMed · Cited by 84 · see citing works
Dishabituation and sensitization emerge as separate processes during development in Aplysia
Rankin, C. H., & Carew, T. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-01-00197.1988 · Cited by 77 · see citing works
Blumenfeld, H., Spiral, M. E., Kandel, E. R., et al. (1990) · Neuron · doi:10.1016/0896-6273(90)90088-w · Cited by 67 · see citing works
Schacher, S., Montarolo, P. G., & Kandel, E. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-10-03286.1990 · Cited by 48 · see citing works
Structural studies on a family of cAMP-binding proteins in the nervous system of Aplysia.
Eppler, C. M., Bayley, H., Greenberg, S. M., & Schwartz, J. H. (1986) · The Journal of Cell Biology · doi:10.1083/jcb.102.1.320 · Cited by 37 · see citing works
Dubuc, B., & Castellucci, V. F. (1991) · Journal of Experimental Biology · doi:10.1242/jeb.156.1.315 · Cited by 35 · see citing works
Yovell, Y., Kandel, E. R., Dudai, Y., et al. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.24.9285 · Cited by 31 · see citing works
Distribution of cAMP and cAMP-dependent protein kinases in Aplysia sensory neurons
Greenberg, S., Bernier, L., & Schwartz, J. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-01-00291.1987 · Cited by 29 · see citing works
Belardetti, F., Biondi, C., Brunelli, M., et al. (1983) · Brain Research · doi:10.1016/0006-8993(83)90084-7 · Cited by 20 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Computational design of enhanced learning protocols
Zhang, Y., Liu, R.-Y., Heberton, G. A., Smolen, P., Baxter, D. A., Cleary, L. J., & Byrne, J. H. (2012) · Nature Neuroscience · doi:10.1038/nn.2990 · Cited by 80 · see citing works
- Authors
- Goldsmith, B. A., & Abrams, T. W.
- Affiliations
- University of Pennsylvania (US)
- ORCID
- Abrams, T W
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1991-10-15
- Volume
- 88
- Issue
- 20
- Pages
- 9021-9025
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC52643
- OpenAlex
- W2054343388
- Cited by
- 118
- References
- 38
- Citations by year
- 2024: 1 · 2023: 1 · 2016: 1 · 2014: 1
- FWCI
- 1.83
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Whitehall Foundation
- National Institutes of Health (5r01ns025788-05)
- National Institute of Neurological Disorders and Stroke (NS 25788)
- 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
- synaptic depression, serotonin, adenylate cyclase, Aplysia, cyclic AMP, dishabituation, presynaptic action potential, protein kinase C, protein kinase A, synaptic transmission
- MeSH terms
- Adenylyl Cyclase Inhibitors, Adenine, Adenylyl Cyclases, Animals, Aplysia, Enzyme Activation, Evoked Potentials, Ganglia, Kinetics, Neurons, Afferent, Serotonin, Synapses, Phorbol 12,13-Dibutyrate, In Vitro Techniques
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