Journal of Neurophysiology, Vol 62, Issue 5 1113-1126, Copyright © 1989 by APS

ARTICLES

Chemically and electrically coupled interneurons mediate respiratory pumping in Aplysia

J. Koester
Center for Neurobiology and Behavior, College of Physicians and Surgeons, Columbia University, New York, New York.

1. Respiratory pumping in Aplysia consists of synchronous, brief contractions of the mantle organs that can occur spontaneously and also can be triggered by tactile or noxious stimulation. It has been shown previously to be driven in part by a cluster of electrically coupled interneurons, called the L25 cells, located in the left hemiabdominal ganglion. This paper describes a second class of interneurons, the R25 cells, that also plays an important role in the control of respiratory pumping. 2. The R25 cells are a cluster of approximately 14 interneurons located in the right hemiabdominal ganglion, roughly symmetrical to the L25 cells. The R25 cells are electrically coupled to each other and to the L25 cells. Some R25 and L25 cells also produce chemically mediated fast excitation and slow inhibition of other neurons in the R25/L25 network. 3. Three lines of evidence demonstrate that the R25 cells play a role in mediating respiratory pumping: 1) They fire in a synchronous burst each time the behavior occurs. 2) They make direct chemical synaptic connections to motoneurons that mediate the behavior; and 3) Firing a single R25 cell can trigger the entire behavior, by recruiting synchronous bursts of activity in all of the other R25 and L25 neurons. Individual R25 and L25 cells can act both as trigger cells (exciting the other interneurons) and as relay cells (projecting directly to motoneurons). 4. Burst initiation within the R25/L25 network appears to have two phases: 1) There is an initial phase when the R25 and L25 cells fire at a relatively low frequency. This phase can be driven either by endogenous pacemaker activity of the R25/L25 cells or by afferent synaptic input from sensory pathways; and 2) The late, high-frequency phase of the burst results largely from reverberation within the network, as activity in each cell contributes positive feedback via the excitatory chemical and electrical connections between R25 and L25 cells. 5. Synchronization of the different motor outputs that make up the pumping behavior is achieved by three mechanisms: 1) When pumping occurs spontaneously, the electrical coupling between the cells of the R25/L25 network ensures that these cells will all be near spike threshold at the end of each interburst period.(ABSTRACT TRUNCATED AT 400 WORDS)

This article has been cited by other articles:

				I. Hurwitz, A. Ophir, A. Korngreen, J. Koester, and A. J. Susswein Currents Contributing to Decision Making in Neurons B31/B32 of Aplysia J Neurophysiol, February 1, 2008; 99(2): 814 - 830. [Abstract] [Full Text] [PDF]

				R. D. Hawkins, G. A. Clark, and E. R. Kandel Operant Conditioning of Gill Withdrawal in Aplysia J. Neurosci., March 1, 2006; 26(9): 2443 - 2448. [Abstract] [Full Text] [PDF]

				A. J. Susswein, I. Hurwitz, R. Thorne, J. H. Byrne, and D. A. Baxter Mechanisms Underlying Fictive Feeding in Aplysia: Coupling Between a Large Neuron With Plateau Potentials Activity and a Spiking Neuron J Neurophysiol, May 1, 2002; 87(5): 2307 - 2323. [Abstract] [Full Text] [PDF]

				M. Levy and A. J. Susswein Separate Effects of a Classical Conditioning Procedure on Respiratory Pumping, Swimming, and Inking in Aplysia fasciata Learn. Mem., January 1, 1999; 6(1): 21 - 36. [Abstract] [Full Text]

				I. Hurwitz, I. Kupfermann, and A. J. Susswein Different Roles of Neurons B63 and B34 That Are Active During the Protraction Phase of Buccal Motor Programs in Aplysia californica J Neurophysiol, September 1, 1997; 78(3): 1305 - 1319. [Abstract] [Full Text] [PDF]

				G. A. Phares and P. E. Lloyd Immunocytological and Biochemical Localization and Biological Activity of the Newly Sequenced Cerebral Peptide 2 in Aplysia J. Neurosci., December 15, 1996; 16(24): 7841 - 7852. [Abstract] [Full Text] [PDF]

				L J Cleary, J H Byrne, and W N Frost Role of interneurons in defensive withdrawal reflexes in Aplysia. Learn. Mem., January 1, 1995; 2(3-4): 133 - 151. [PDF]

				J. Wu, L. Cohen, and C. Falk Neuronal activity during different behaviors in Aplysia: a distributed organization? Science, February 11, 1994; 263(5148): 820 - 823. [Abstract] [PDF]