Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1987 May;84(10):3486–3490. doi: 10.1073/pnas.84.10.3486

Multiple neuropeptides in cholinergic motor neurons of Aplysia: evidence for modulation intrinsic to the motor circuit.

E C Cropper, P E Lloyd, W Reed, R Tenenbaum, I Kupfermann, K R Weiss
PMCID: PMC304896  PMID: 3472218

Abstract

Changes in Aplysia biting responses during food arousal are partially mediated by the serotonergic metacerebral cells (MCCs). The MCCs potentiate contractions of a muscle utilized in biting, the accessory radula closer (ARCM), when contractions are elicited by stimulation of either of the two cholinergic motor neurons B15 or B16 that innervate the muscle. We have now shown that ARCM contractions may also be potentiated by peptide cotransmitters in the ARCM motor neurons. We found that motor neuron B15 contains small cardioactive peptides A and B (SCPA and SCPB)--i.e., whole B15 neurons were bioactive on the SCP-sensitive Helix heart, as were reverse-phase HPLC fractions of B15 neurons that eluted like synthetic SCPA and SCPB. Furthermore, [35S]methionine-labeled B15 peptides precisely coeluted with synthetic SCPA and SCPB. SCPB-like immunoreactivity was associated with dense-core vesicles in the soma of B15 and in neuritic varicosities and terminals in the ARCM. B16 motor neurons did not contain SCPA or SCPB but contained an unidentified bioactive peptide. RP-HPLC of [35S]methionine-labeled B16s resulted in one major peak of radioactivity that did not coelute with either SCP and which, when subject to Edman degradation, yielded [35S]methionine in positions where there is no methionine in the SCPs. Exogenously applied B16 peptide potentiated ARCM contractions elicited by stimulation of B15 or B16 neurons. Thus, in this system there appear to be two types of modulation; one type arises from the MCCs and is extrinsic to the motor system, whereas the second type arises from the motor neurons themselves and hence is intrinsic.

Full text

PDF
3486

Images in this article

3488Image
on p.3488

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams M. E., O'Shea M. Peptide cotransmitter at a neuromuscular junction. Science. 1983 Jul 15;221(4607):286–289. doi: 10.1126/science.6134339. [DOI] [PubMed] [Google Scholar]
  2. Beltz B., Eisen J. S., Flamm R., Harris-Warrick R. M., Hooper S. L., Marder E. Serotonergic innervation and modulation of the stomatogastric ganglion of three decapod crustaceans (Panulirus interruptus, Homarus americanus and Cancer irroratus). J Exp Biol. 1984 Mar;109:35–54. doi: 10.1242/jeb.109.1.35. [DOI] [PubMed] [Google Scholar]
  3. Bendayan M., Zollinger M. Ultrastructural localization of antigenic sites on osmium-fixed tissues applying the protein A-gold technique. J Histochem Cytochem. 1983 Jan;31(1):101–109. doi: 10.1177/31.1.6187796. [DOI] [PubMed] [Google Scholar]
  4. Cohen J. L., Weiss K. R., Kupfermann I. Motor control of buccal muscles in Aplysia. J Neurophysiol. 1978 Jan;41(1):157–180. doi: 10.1152/jn.1978.41.1.157. [DOI] [PubMed] [Google Scholar]
  5. Evans P. D., O'Shea M. An octopaminergic neurone modulates neuromuscular transmission in the locust. Nature. 1977 Nov 17;270(5634):257–259. doi: 10.1038/270257a0. [DOI] [PubMed] [Google Scholar]
  6. Hoyle G. A function for neurons (DUM) neurosecretory on skeletal muscle of insects. J Exp Zool. 1974 Sep;189(3):401–406. doi: 10.1002/jez.1401890313. [DOI] [PubMed] [Google Scholar]
  7. Kravitz E. A., Glusman S., Harris-Warrick R. M., Livingstone M. S., Schwarz T., Goy M. F. Amines and a peptide as neurohormones in lobsters: actions on neuromuscular preparations and preliminary behavioural studies. J Exp Biol. 1980 Dec;89:159–175. doi: 10.1242/jeb.89.1.159. [DOI] [PubMed] [Google Scholar]
  8. Kuhlman J. R., Li C., Calabrese R. L. FMRF-amide-like substances in the leech. II. Bioactivity on the heartbeat system. J Neurosci. 1985 Sep;5(9):2310–2317. doi: 10.1523/JNEUROSCI.05-09-02310.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kupfermann I. Feeding behavior in Aplysia: a simple system for the study of motivation. Behav Biol. 1974 Jan;10(1):1–26. doi: 10.1016/s0091-6773(74)91644-7. [DOI] [PubMed] [Google Scholar]
  10. Kupfermann I., Weiss K. R. Activity of an identified serotonergic neuron in free moving Aplysia correlates with behavioral arousal. Brain Res. 1982 Jun 10;241(2):334–337. doi: 10.1016/0006-8993(82)91072-1. [DOI] [PubMed] [Google Scholar]
  11. Lloyd P. E., Kupfermann I., Weiss K. R. Evidence for parallel actions of a molluscan neuropeptide and serotonin in mediating arousal in Aplysia. Proc Natl Acad Sci U S A. 1984 May;81(9):2934–2937. doi: 10.1073/pnas.81.9.2934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lloyd P. E., Mahon A. C., Kupfermann I., Cohen J. L., Scheller R. H., Weiss K. R. Biochemical and immunocytological localization of molluscan small cardioactive peptides in the nervous system of Aplysia californica. J Neurosci. 1985 Jul;5(7):1851–1861. doi: 10.1523/JNEUROSCI.05-07-01851.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Mahon A. C., Lloyd P. E., Weiss K. R., Kupfermann I., Scheller R. H. The small cardioactive peptides A and B of Aplysia are derived from a common precursor molecule. Proc Natl Acad Sci U S A. 1985 Jun;82(11):3925–3929. doi: 10.1073/pnas.82.11.3925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Matthews M. R., Cuello A. C. Substance P-immunoreactive peripheral branches of sensory neurons innervate guinea pig sympathetic neurons. Proc Natl Acad Sci U S A. 1982 Mar;79(5):1668–1672. doi: 10.1073/pnas.79.5.1668. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Morris H. R., Panico M., Karplus A., Lloyd P. E., Riniker B. Elucidation by FAB-MS of the structure of a new cardioactive peptide from Aplysia. Nature. 1982 Dec 16;300(5893):643–645. doi: 10.1038/300643a0. [DOI] [PubMed] [Google Scholar]
  16. Ono J. K., McCaman R. E. Identification of additional histaminergic neurons in Aplysia: improvement of single cell isolation techniques for in tandem physiological and chemical studies. Neuroscience. 1980;5(5):835–840. doi: 10.1016/0306-4522(80)90152-9. [DOI] [PubMed] [Google Scholar]
  17. Orchard I., Lange A. B. Evidence for octopaminergic modulation of an insect visceral muscle. J Neurobiol. 1985 May;16(3):171–181. doi: 10.1002/neu.480160303. [DOI] [PubMed] [Google Scholar]
  18. Pickel V. M., Reis D. J., Leeman S. E. Ultrastructural localization of substance P in neurons of rat spinal cord. Brain Res. 1977 Feb 25;122(3):534–540. doi: 10.1016/0006-8993(77)90463-2. [DOI] [PubMed] [Google Scholar]
  19. Rosen S. C., Kupfermann I., Goldstein R. S., Weiss K. R. Lesion of a serotonergic modulatory neuron in Aplysia produces a specific defect in feeding behavior. Brain Res. 1983 Jan 31;260(1):151–155. doi: 10.1016/0006-8993(83)90778-3. [DOI] [PubMed] [Google Scholar]
  20. Takami K., Kawai Y., Uchida S., Tohyama M., Shiotani Y., Yoshida H., Emson P. C., Girgis S., Hillyard C. J., MacIntyre I. Effect of calcitonin gene-related peptide on contraction of striated muscle in the mouse. Neurosci Lett. 1985 Sep 30;60(2):227–230. doi: 10.1016/0304-3940(85)90248-4. [DOI] [PubMed] [Google Scholar]
  21. Thompson E. B., Schwartz J. H., Kandel E. R. A radioautographic analysis in the light and electron microscope of identified Aplysia neurons and their processes after intrasomatic injection of L-(3H)fucose. Brain Res. 1976 Aug 13;112(2):251–281. doi: 10.1016/0006-8993(76)90283-3. [DOI] [PubMed] [Google Scholar]
  22. Weiss K. R., Cohen J. L., Kupfermann I. Modulatory control of buccal musculature by a serotonergic neuron (metacerebral cell) in Aplysia. J Neurophysiol. 1978 Jan;41(1):181–203. doi: 10.1152/jn.1978.41.1.181. [DOI] [PubMed] [Google Scholar]
  23. Weiss K. R., Mandelbaum D. E., Schonberg M., Kupfermann I. Modulation of buccal muscle contractility by serotonergic metacerebral cells in Aplysia: evidence for a role of cyclic adenosine monophosphate. J Neurophysiol. 1979 May;42(3):791–803. doi: 10.1152/jn.1979.42.3.791. [DOI] [PubMed] [Google Scholar]
  24. Willard A. L. Effects of serotonin on the generation of the motor program for swimming by the medicinal leech. J Neurosci. 1981 Sep;1(9):936–944. doi: 10.1523/JNEUROSCI.01-09-00936.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES