Abstract
MOTOR circuits are often thought to be physically separate from their neuromodulatory systems1,2. We report here a counter example, where neurons within a circuit appear to modulate synaptic properties of that same circuit during its normal operation. The dorsal swim interneurons (DSIs) are members of the central pattern generator circuit for escape swimming in the mollusc Tritonia diomedea3. However, DSI stimulation also rapidly enhances the synaptic potentials evoked by another neuron in the same circuit onto its follower cells. This modulatory action appears to be mediated by serotonin (5-hydroxytryptamine); the DSIs are serotonin-immunoreactive4, and bath-application of serotonin mimics and occludes the effect of DSIs. These results indicate that during the escape swim, circuit connection strengths are dynamically controlled by the activity of neurons within the circuit itself. This 'intrinsic neuromodulation' may be important for the animal's initial decision to swim, the generation of the swim motor programme itself, and certain types of learning.
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References
Harris-Warrick, R. M. & Marder, E. A. Rev. Neurosci. 14, 39–57 (1991).
Kaczmarek, L. K. & Levitan, I. B. Neuromodulation: The Biochemical Control of Neuronal Excitability (Oxford Univ. Press, New York, 1987).
Getting, P. A., Lennard, P. R. & Hume, R. I. J. Neurophysiol. 44, 151–164 (1980).
Getting, P. A., McClellan, A. D. & Li, M. Soc. Neurosci. Abstr. 11, 1023 (1985).
Getting, P. A. & Dekin, M. S. in Model Neural Networks and Behavior (ed. Selverston, A. I.) 3–20 (Plenum, New York, 1985).
Frost, W. N. & Getting, P. A. Soc. Neurosci. Abstr. 15, 1118 (1989).
Getting, P. A. J. Neurophysiol. 46, 65–79 (1981).
Katz, P. S. & Frost, W. N. Soc. Neurosci. Abstr. 19, 1700 (1993).
Getting, P. A. in Symposia of the Society for Experimental Biology No. 37; Neural Origin of Rhythmic Movements (eds Roberts, A. & Roberts, B. L.) 89–128 (Cambridge Univ. Press, New York, 1983).
Getting, P. A. & Dekin, M. S. J. Neurophysiol. 53, 466–480 (1985).
Getting, P. A. A. Rev. Neurosci. 12, 185–204 (1989).
Abraham, F. D. & Willows, A. O. D. Comm. Behav. Biol. 6, 271–280 (1971).
Frost, W. N., Brown, G. & Getting, P. A. Soc. Neurosci. Abstr. 14, 607 (1988).
Katz, P. S. & Harris-Warrick, R. M. Trends Neurosci. 13, 367–373 (1990).
Harris-Warrick, R. M. in Neural Control of Rhythmic Movements in Vertebrates (eds Cohen, A. H., Rossignol, S. & Grillner, S.) 285–331 (Wiley, New York, 1988).
Jordan, L. M., Brownstone, R. M. & Noga, B. R. Curr. Opin. Neurobiol. 2, 794–801 (1992).
Hawkins, R. D., Castellucci, V. F. & Kandel, E. R. J. Neurophysiol. 45, 315–326 (1981).
Cropper, E. C. et al. Proc. natn. Acad. Sci. U.S.A. 84, 3486–3490 (1987).
Whim, M. D. & Lloyd, P. E. J. Neurosci. 10, 3313–3322 (1990).
Bishop, C. A., Wine, J. J., Nagy, F. & O'Shea, M. R. J. Neurosci. 7, 1769–1779 (1987).
Katz, P. S. & Harris-Warrick, R. M. J. Neurophysiol. 62, 571–581 (1989).
Chiel, H. J., Weiss, K. R. & Kupfermann, I. Trends Neurosci. 13, 223–227 (1990).
Nusbaum, M. P., Weimann, J. M., Golowasch, J. & Marder, E. J. Neurosci. 12, 2706–2714 (1992).
Taghert, P. H. & Willows, A. O. D. J. comp. Physiol. 123, 253–259 (1978).
Willows, A. O. D., Dorsett, D. A. & Hoyle, G. J. Neurobiol. 4(3), 207–237 (1973).
Hume, R. I., Getting, P. A. & Del Beccaro, M. A. J. Neurophysiol. 47, 60–74 (1982).
Hume, R. I., Getting, P. A. J. Neurophysiol. 47, 75–90 (1982).
Brown, G. D. & Willows, A. O. D. Soc. Neurosci. Abstr. 17, 549 (1991).
Weinreich, D., McCaman, M. W., McCaman, R. E. & Vaughn, J. E. J. Neurochem. 20, 969–976 (1973).
Croll, R. P. & Chiasson, B. J. J. comp. Neurol. 280, 122–142 (1989).
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Katz, P., Getting, P. & Frost, W. Dynamic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit. Nature 367, 729–731 (1994). https://doi.org/10.1038/367729a0
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DOI: https://doi.org/10.1038/367729a0
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