Skip to main content
Log in

Innervation of buccal muscles by multifunctional MA1 neurons in Aplysia kurodai

  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Summary

  1. 1.

    Spikes in Aplysia MA1 neurons produced excitatory (EJPs), inhibitory (IJPs), and diphasic inhibitory-excitatory junction potentials in different fibers of the buccal muscles.

  2. 2.

    The IJPs following the MA1 spikes were recorded in the muscle fibers innervated by the jaw-closing motoneurons. The depolarization of muscle fibers produced by the motoneurons was largely suppressed by simultaneous MA1 firing, suggesting that the MA1 neurons make a direct connection to a part of the muscle fibers innervated by these motoneurons and inhibit them.

  3. 3.

    The excitatory and inhibitory components of the junction potentials produced by MA1 were reversibly blocked by hexamethonium and d-tubocurarine, respectively. In contrast, the EJPs produced by the jaw-closing motoneurons were blocked by an amino acid antagonist, suggesting that the MA1 neurons and the jaw-closing motoneurons use different transmitters in the nerve-muscle junctions.

  4. 4.

    The jaw movement produced by the jaw-closing motoneurons was suppressed by simultaneous MA1 firing, and the suppression was released by d-tubocurarine, suggesting that the IJPs produced by MA1 may contribute to the suppression of jaw movement. The firing of MA1 produced the vertical movement of the buccal muscles, which was blocked by hexamethonium, suggesting that the EJPs produced by MA1 may contribute to the vertical movement.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

2-APB :

2-amino-4-phosphonobutyric acid

APV :

2-amino-5-phosphonovaleric acid

ARC :

accessory radula closer muscle

ASW :

artificial seawater

DGG γ-d :

glutamylglycine

EJP :

excitatory junction potential

EPSP :

excitatory postsynaptic potential

GDEE :

l-glutamic acid diethyl ester

I 1 + I 3 :

intrinsic buccal muscles I1 and I3

IEJP :

diphasic inhibitory-excitatory junction potential

IJP :

inhibitory junction potential

IPSP :

inhibitory postsynaptic potential

JC1-JC3 :

jaw-closing motoneurons

JO1 :

jaw-opening motoneruon

MA1, MA2 :

prernotor neurons

References

  • Ascher P, Kehoe JS (1975) Amine and amino acid receptors in gastropod neurons. In: Iversen LL, Iversen SD, Synder SH (eds) Handbook of psychopharmacology, vol 4. Plenum, New York, pp 265–310

    Google Scholar 

  • Banks FW (1975) Inhibitory transmission at a molluscan neuromuscular junction. J Neurobiol 6:429–433

    Google Scholar 

  • Banks FW (1978) Central control of the lower extrinsic protractor muscle in the buccal ganglia of Aplysia. Comp Biochem Physiol 61 A:267–277

    Google Scholar 

  • Beltz B, Gelperin A (1980) Mechanism of peripheral modulation of salivary burster in Limax maximus: a presumptive sensorimotor neuron. J Neurophysiol 44:675–686

    Google Scholar 

  • Blankenship JE, Rock MK, Hill J (1977) Physiological properties of the penis retractor muscle of Aplysia. J Neurobiol 8:549–568

    Google Scholar 

  • Carew TJ, Pinsker H, Rubinson K, Kandel ER (1974) Physiological and biochemical properties of neuromuscular transmission between identified motoneurons and gill muscle in Aplysia. J Neurophysiol 37:1020–1040

    Google Scholar 

  • Carpenter DO, Swann JW, Yarowsky PJ (1977) Effect of curare on response to different putative neurotransmitters in Aplysia neurons. J Neurobiol 8:119–132

    Google Scholar 

  • Cohen JL, Weiss KR, Kupfermann I (1978) Motor control of buccal muscles in Aplysia. J Neurophysiol 41:157–180

    Google Scholar 

  • Cotman CW, Monaghan DT, Ottersen OP, Storm-Mathisen J (1987) Anatomical organization of excitatory amino acid receptors and their pathways. Trends Neurosci 10:273–280

    Google Scholar 

  • Gardner D (1971) Bilateral symmetry and interneuronal organization in the buccal ganglia of Aplysia. Science 173:550–553

    Google Scholar 

  • Gardner D (1977) Interconnections of identified multiaction interneurons in buccal ganglia of Aplysia. J Neurophysiol 40:349–361

    Google Scholar 

  • Gardner D, Kandel ER (1977) Physiological and kinetic properties of cholinergic receptors activated by multiaction interneurons in buccal ganglia of Aplysia. J Neurophysiol 40:333–348

    Google Scholar 

  • Harris EW, Ganong AH, Cotman CW (1984) Long-term potentiation in the hippocampus involves activation of N-methyl-d-aspartate receptors. Brain Res 323:132–137

    Google Scholar 

  • Howells HH (1942) The structure and function of the alimentary canal of Aplysia punctata. Q J Microsc Sci 83:357–397

    Google Scholar 

  • Jahan-Parwar B, Wilson AH Jr, Fredman SM (1983) Role of proprioceptive reflexes in control of feeding muscles of Aplysia. J Neurophysiol 49:1469–1480

    Google Scholar 

  • Kandel ER (1976) Cellular basis of behavior. Freeman, San Francisco

    Google Scholar 

  • Krogsgaad-Larsen P, Honore T (1983) Glutamate receptors and new glutamate agonists. Trend Pharmacol Sci 4:31–33

    Google Scholar 

  • Kurokawa M, Kuwasawa K (1988) Multimodal inhibitory innervation of the gill of Aplysia Juliana. J Comp Physiol A 162:533–541

    Google Scholar 

  • Marder E (1976) Cholinergic motor neurons in the stomatogastric system of the lobster. J Physiol 257:63–86

    Google Scholar 

  • Maynard DM, Selverston AI (1975) Organization of the stomatogastric ganglion of the spiny lobster. IV. The pyloric system. J Comp Physiol 100:161–182

    Google Scholar 

  • Nagahama T, Takata M (1987) Food-induced firing patterns in motoneurons innervating the pharynx of Aplysia kurodai. J Comp Physiol A 161:799–809

    Google Scholar 

  • Nagahama T, Takata M (1988) Food-induced firing patterns in motoneurons producing jaw movements in Aplysia kurodai. J Comp Physiol A 162:729–738

    Google Scholar 

  • Nagahama T, Takata M (1989) Neural mechanism generating firing patterns in jaw motoneurons during the food-induced response in Aplysia kurodai. I. Identification and characterization of premotor neurons. J Comp Physiol A 166:143–150

    Google Scholar 

  • Nagahama T, Takata M (1990) Neural mechanism generating firing patterns in jaw motoneurons during the food-induced response in Aplysia kurodai. II. Functional role of premotor neurons on generation of firing patterns in motoneurons. J Comp Physiol A 166:277–286

    Google Scholar 

  • Peters M, Altrup U (1984) Motor organization in pharynx of Helix pomatia. J Neurophysiol 52:389–409

    Google Scholar 

  • Rosen SC, Weiss KR, Cohen JL, Kupfermann I (1982) Interganglionic cerebral-buccal mechanoafferents of Aplysia: receptive fields and synaptic connections of different classes of neurons involved in feeding behavior. J Neurophysiol 48:271–288

    Google Scholar 

  • Sawada M, Gibson D, McAdoo DJ (1984) l-Glutamic acid, a possible neurotransmitter to anterior aorta of Aplysia. J Neurophysiol 51:375–386

    Google Scholar 

  • Segal MM, Koester J (1982) Convergent cholinergic neurons produce similar postsynaptic actions in Aplysia: implications for neural organization. J Neurophysiol 47:742–759

    Google Scholar 

  • Watkins JC (1981) Pharmacology of excitatory amino acid receptors. In: Roberts PJ, Storm-Mathisen J, Johnston GAR (eds) Glutamate: transmitter in the central nervous system. John Wiley, London, pp 1–24

    Google Scholar 

  • Watkins JC (1984) Excitatory amino acids and central synaptic transmission. Trends Pharmacol Sci 5:373–376

    Google Scholar 

  • Weiss KR, Cohen JL, Kupfermann I (1978) Modulatory control of buccal musculature by a serotonergic neuron (metacerebral cell) in Aplysia. J Neurophysiol 41:181–203

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nagahama, T., Takata, M. Innervation of buccal muscles by multifunctional MA1 neurons in Aplysia kurodai . J Comp Physiol A 167, 1–10 (1990). https://doi.org/10.1007/BF00192401

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00192401

Key words

Navigation