Experimental Brain Research

, Volume 109, Issue 2, pp 361–365 | Cite as

Control of locomotion in the marine mollusc Clione limacina

XI. Effects of serotonin
  • Y. V. Panchin
  • Y. I. Arshavsky
  • T. G. Deliagina
  • G. N. Orlovsky
  • L. B. Popova
  • A. I. Selverston
Research Note

Abstract

The locomotor activity in the marine mollusc Clione limacina has been found to be strongly excited by serotonergic mechanisms. In the present study putative serotonergic cerebropedal neurons were recorded simultaneously with pedal locomotor motoneurons and interneurons. Stimulation of serotonergic neurons produced acceleration of the locomotor rhythm and strengthening of motoneuron discharges. These effects were accompanied by depolarization of motoneurons, while depolarization of the generator interneurons was considerably lower (if it occurred at all). Effects of serotonin application on isolated locomotor and non-locomotor pedal neurons were studied. Serotonin (5×10-7 to 1×10-6 M) affected most pedal neurons. All locomotor neurons were excited by serotonin. This suggests that serotonergic command neurons exert direct influence on locomotor neurons. Effects of serotonin on nonlocomotor neurons were diverse, most neurons being inhibited by serotonin. Some effects of serotonin on locomotor neurons could not be reproduced by neuron depolarization. This suggests that, along with depolarization, serotonin modulates voltage-sensitive membrane properties of the neurons. As a result, serotonin promotes the endogenous rhythmical activity in neurons of the C. limacina locomotor central pattern generator.

Key words

Locomotion Central pattern generator Serotonin Modulation Pteropod mollusc 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arshavsky YI, Orlovsky GN, Panchin YV, Pavlova GA (1982) Generation of locomotor rhythm in pedal ganglia of Clione limacina (in Russian). Neirofiziologia 14: 102–104Google Scholar
  2. Arshavsky YI, Beloozerova IN, Orlovsky GN, Panchin YV, Pavlova GA (1985a) Control of locomotion in marine mollusc Clione limacina. 1. Efferent activity during actual and fictitious swimming. Exp Brain Res 58: 255–262Google Scholar
  3. Arshavsky YI, Beloozerova IN, Orlovsky GN, Panchin YV, Pavlova GA (1985b) Control of locomotion in marine mollusc Clione limacina. 2. Rhythmic neurons of pedal ganglia. Exp Brain Res 58: 263–272Google Scholar
  4. Arshavsky YI, Beloozerova IN, Orlovsky GN, Panchin YV, Pavlova GA (1985c) Control of locomotion in marine mollusc Clione limacina. 3. On the origin of locomotory rhythm. Exp Brain Res 58: 273–284Google Scholar
  5. Arshavsky YI, Deliagina TG, Orlovsky GN, Panchin YV, Pavlova GA, Popova LB (1986) Control of locomotion in marine mollusc Clione limacina. 6. Activity of isolated neurons of pedal ganglia. Exp Brain Res 63: 106–112Google Scholar
  6. Arshavsky YI, Deliagina TG, Orlovsky GN, Panchin YV, Pavlova GA, Popova LB (1991) Locomotion of Clione limacina in relation to various types of behavior. In: Sakharov DA, Winlow W (eds) Simpler nervous systems. Manchester University Press, Manchester, UK, pp 290–315Google Scholar
  7. Harris-Warrick RM, Marder E, Selverston AI, Moulins M (1992) The stomatogastric nervous system. MIT Press, Cambridge, MAGoogle Scholar
  8. Hochman S, Jordan LM, MacDonald LF (1994a) N-methyl-d-aspartate receptor-mediated voltage oscillations in neurons surrounding the central canal in slices of rat spinal cord. J Neurophysiol 72: 565–577Google Scholar
  9. Hochman S, Jordan LM, Schmidt BJ (1994b) TTX-resistant NMDA receptor-mediated voltage oscillations in mammalian lumbar motoneurons. J Neurophysiol 72: 2559–2562Google Scholar
  10. Kabotyansky EA, Milosevic I, Sakharov DA (1990) Neuronal correlates of 5-hydroxytryptophan-induced sustained swimming in Aplysia fasciata. Comp Biochem Physiol [C] 95: 39–44Google Scholar
  11. Katz PS, Getting PA, Frost WN (1994) Dynamic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit. Nature 367: 729–731Google Scholar
  12. Mackey S, Carew TJ (1983) Locomotion in Aplysia: triggering by serotonin and modulation by bag cell extract. J Neurosci 3:1469–1477Google Scholar
  13. McClellan AD, Brown GD, Getting PA (1994) Modulation of swimming in Tritonia: excitatory and inhibitory effects of serotonin. J Comp Physiol [A] 174: 257–266Google Scholar
  14. McPherson DR, Blankenship JE (1991) Neural control of swimming in Aplysia brasiliana. 3. Serotonergic modulatory neurons. J Neurophysiol 66:1366–1379Google Scholar
  15. Panchin YV, Arshavsky YI, Selverston AI, Cleland TA (1993) Lobster stomatogasric neurons in primary culture. 1. Basic characteristics. J Neurophysiol 69:1976–1992Google Scholar
  16. Panchin YV, Gamkrelidze GN, Popova LB, Deliagina TG, Orlovsky GN, Arshavsky YI (1994) Neuronal basis of hunting and feeding behavior in the pteropod mollusc Clione limacina. Neth J Zool 44: 170–183Google Scholar
  17. Panchin YV, Popova LB, Deliagina TG, Orlovsky GN, Arshavsky YI (1995a) Control of locomotion in marine mollusc Clione limacina. 8. Cerebro-pedal neurons. J Neurophysiol 73: 1912–1923Google Scholar
  18. Panchin YV, Sadreev RI, Arshavsky YI (1995b) Control of locomotion in marine mollusc Clione limacina. 10. Effects of acetylcholine antagonists. Exp Brain Res 106: 135–144Google Scholar
  19. Parsons DW, Pinsker HM (1989) Swimming in Aplysia brasiliana: Behavioral and cellular effects of serotonin. J Neurophysiol 62: 1163–1176Google Scholar
  20. Sakharov DA, Kabotyansky EA (1986) Integration of behavior of the pteropod mollusc by dopamine and serotonin (in Russian). Zh Obsch Biol 47: 234–245Google Scholar
  21. Sakharov DA, Milosevic I, Salimova N (1989) Drug-induced locomotor stereotypes in Aplysia. Comp Biochem Physiol [C] 93:161–166Google Scholar
  22. Satterlie RA (1985) Reciprocal inhibition and postinhibitory rebound produce reverberation in a locomotor pattern generation. Science 229: 402–404Google Scholar
  23. Satterlie RA (1991) Neural control of speed changes in an opisthobranch locomotory system. Biol Bull 180: 228–233Google Scholar
  24. Satterlie RA (1995) Serotonergic modulation of swimming speed in the pteropod mollusc Clione limacina. 2. Peripheral modulatory neurons. J Exp Biol 198: 905–916Google Scholar
  25. Satterlie RA, Norekian TP (1995) Serotonergic modulation of swimming speed in the pteropod mollusc Clione limacina. 3. Cerebral neurons. J Exp Biol 198: 917–930Google Scholar
  26. Satterlie RA, Spencer AN (1985) Swimming in the pteropod mollusc Clione limacina. 2. Physiology. J Exp Biol 116: 205–222Google Scholar
  27. Satterlie RA, LaBarbera M, Spencer AN (1985) Swimming in the pteropod mollusc Clione limacina. 1. Behavior and morphology. J Exp Biol 116: 189–204Google Scholar
  28. Satterlie RA, Norekian TP, Jordan S, Kazilek CJ (1995) Serotonergic modulation of swimming speed in the pteropod mollusc Clione limacina. 1. Serotonin immunoreactivity in the central nervous system and wings. J Exp Biol 198: 895–904Google Scholar
  29. Selverston AI, Moulins M (1987) The crustacean stomatogastric system. Springer, Berlin Heidelberg New YorkGoogle Scholar
  30. Stewart WW (1978) Functional connections between cells revealed by dye-coupling with a high fluorescent naphthalimide tracer. Cell 14: 741–759Google Scholar
  31. Tell F, Jean A (1993) Ionic basis for endogenous rhythmic patterns induced by activation of N-methyl-d-aspartate receptors in eurons of the rat nucleus tractus solitarii. J Neurophysiol 70:2379–2390Google Scholar
  32. Wagner N (1885) Die Wirbellosen des Weissen Meeres. Engelmann, LeipzigGoogle Scholar
  33. Wallen P, Grillner S (1987) N-methyl-d-aspartate receptors induced, inherent oscillatory activity in neurons active during fictive locomotion in the lamprey. J Neurosci 7: 2745–2755Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • Y. V. Panchin
    • 1
    • 2
    • 4
  • Y. I. Arshavsky
    • 1
    • 4
  • T. G. Deliagina
    • 2
    • 3
  • G. N. Orlovsky
    • 2
    • 3
  • L. B. Popova
    • 2
  • A. I. Selverston
    • 4
  1. 1.Institute of Problems of Information Transmission, Academy of Science of RussiaMoscowRussia
  2. 2.A. N. Belozersky Institute of Physico-Chemical Biology, Moscow State UniversityMoscowRussia
  3. 3.Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska InstitutetStockholmSweden
  4. 4.Department of Biology 0357University of CaliforniaSan Diego, La JollaUSA

Personalised recommendations