Journal of Neurophysiology, Vol 74, Issue 4 1444-1462, Copyright © 1995 by APS

ARTICLES

Identification and characterization of cerebral ganglion neurons that induce swimming and modulate swim-related pedal ganglion neurons in Aplysia brasiliana

G. N. Gamkrelidze, P. J. Laurienti and J. E. Blankenship
Marine Biomedical Institute, University of Texas Medical Branch, Galveston 77555-1069, USA.

1. We have identified and characterized a family of several pairs of neurons in the cerebral ganglion of Aplysia brasiliana that are capable of inducing, maintaining, or modulating a motor program that underlies swim locomotion in this marine mollusk. We have operationally defined these cells as command neurons (CNs) for swimming. 2. The command cells occur in bilateral pairs in the cerebral ganglion and make direct and indirect outputs to neurons in the pedal ganglia, including motor neurons, a central pattern generator circuit, and modulatory neurons that enhance muscle contractions during swimming. Several of the CNs are sufficient individually to induce the swim motor program (SMP), all receive sensory feedback from the periphery, and several interconnect with other swim-related CNs. 3. Tonic discharges of approximately 10 Hz in CN types 1-3 (CN1-CN3) are capable of eliciting the oscillatory, phasic SMP as recorded in peripheral nerves that innervate the swim appendages, the parapodia. CN1, CN2, and CN3 make monosynaptic excitatory connections onto ipsilateral, contralateral, and bilateral pedal swim-modulatory neurons [parapodial opener-phase (POP) cells], respectively; and each command cell type activates the pedal central pattern generator (CPG), leading to sustained phasic output of motor neurons and POP cells. 4. Tonic firing of CN4 causes weak activation of the SMP contralaterally. These neurons occur as two pairs of neurons in each cerebral hemiganglion, with mutual electrical and chemical synaptic interconnections. CN4 cells also excite CN1 and CN2 cells. Thus CN4 is classified as a higher-order swim command cell type. 5. Command cells classified as types 5-8 (CN5-CN8), although not capable of inducing the SMP individually, nonetheless have strong synaptic connections with pedal POP cells and/or with other command neurons. These command cells may excite or inhibit follower cells on the same or opposite sides of the preparation and modulate the swim output. 6. All the command cells tested received strong input from mechanical stimulation, either stretch or pinching, of either parapodium. Mechanosensory input from the parapodia was shown to depend on the presence of the pedal ganglion, but not the pleural. Sensory stimulation activated command cells and motor neurons, but POP cells received input from sensory stimuli only through the cerebral ganglion, probably via command cells. The effects of applied mechanosensory stimuli could be entirely mimicked by motor neuron-induced contractions of the parapodia.

This article has been cited by other articles:

				N. J. Spencer and T. K. Smith Mechanosensory S-neurons rather than AH-neurons appear to generate a rhythmic motor pattern in guinea-pig distal colon J. Physiol., July 15, 2004; 558(2): 577 - 596. [Abstract] [Full Text] [PDF]

				J. M. Newcomb and W. H. Watson III Modulation of swimming in the gastropod Melibe leonina by nitric oxide J. Exp. Biol., February 1, 2002; 205(3): 397 - 403. [Abstract] [Full Text] [PDF]

				P. S. Katz, D. J. Fickbohm, and C. P. Lynn-Bullock Evidence that the Central Pattern Generator for Swimming in Tritonia Arose from a Non-Rhythmic Neuromodulatory Arousal System: Implications for the Evolution of Specialized Behavior Integr. Comp. Biol., August 1, 2001; 41(4): 962 - 975. [Abstract] [Full Text] [PDF]

				B. Yu, G. N. Gamkrelidze, P. J. Laurienti, and J. E. Blankenship Serotonin Directly Increases a Calcium Current in Swim Motoneurons of Aplysia brasiliana Integr. Comp. Biol., August 1, 2001; 41(4): 1009 - 1025. [Abstract] [Full Text] [PDF]

				W. H. Watson III,, K. A. Lawrence, and J. M. Newcomb Neuroethology of Melibe leonina Swimming Behavior Integr. Comp. Biol., August 1, 2001; 41(4): 1026 - 1035. [Abstract] [Full Text] [PDF]

				R. Aharonov-Barki, T. Beker, and E. Ruppin Emergence of Memory-Driven Command Neurons in Evolved Artificial Agents Neural Comput., March 1, 2001; 13(3): 691 - 716. [Abstract] [Full Text]

				J. Jing and R. Gillette Central Pattern Generator for Escape Swimming in the Notaspid Sea Slug Pleurobranchaea californica J Neurophysiol, February 1, 1999; 81(2): 654 - 667. [Abstract] [Full Text] [PDF]

				P. J. Laurienti and J. E. Blankenship Serotonergic Modulation of a Voltage-Gated Calcium Current in Parapodial Swim Muscle From Aplysia brasiliana J Neurophysiol, March 1, 1997; 77(3): 1496 - 1502. [Abstract] [Full Text] [PDF]