Journal of Neurophysiology, Vol 70, Issue 5 1767-1776, Copyright © 1993 by APS

ARTICLES

Identification and characterization of a multifunction neuron contributing to defensive arousal in Aplysia

L. J. Cleary and J. H. Byrne
Department of Neurobiology and Anatomy, University of Texas Medical School at Houston 77225.

1. The tail withdrawal reflex is mediated by a monosynaptic circuit composed of tail sensory and motor neurons, but there appear to be additional neuronal elements that also contribute to the reflex. A newly identified interneuron, called LP117, was located in the pleural ganglion. This neuron formed a parallel excitatory pathway between sensory and motor neurons. The distinguishing feature of LP117 was its ability to elicit a long-lasting (5-100 s) excitatory postsynaptic potential (EPSP) in the motor neuron. 2. Intracellular labeling of LP117 revealed axons projecting to the cerebral and abdominal as well as the pedal ganglia. Simultaneous intracellular recordings confirmed the widely divergent output of LP117 to tentacle motor neurons in the cerebral ganglion, as well as to gill, siphon, and ink motor neurons in the abdominal ganglion. 3. Also receiving input were abdominal neurons L29, which excites LFs motor neurons and facilitates LE sensory neurons, and L25, which is part of the pattern-generating network underlying respiratory pumping. Thus LP117 appears to be a neural element important for the conduction of information about tail stimulation to ganglia that are not innervated by tail sensory neurons themselves. Moreover, the divergent outputs suggest that LP117 is an element of a neural circuit underlying defensive arousal. 4. LP117 produced slow EPSPs in several motor neurons. The long time course of the EPSP could prolong the burst in the motor neuron produced by LP117 itself as well as increase the effectiveness of coincident synaptic input. This suggests that an important function of this interneuron is to extend the duration of the response to tail stimulation in the motor neuron. This could account for the relatively long time course of the motor neuron response to tail stimulation compared with that of the sensory neuron. 5. Sensitization is a form of nonassociative learning that produces changes in the amplitude and duration of reflex responses. It seems unlikely that all of these changes can be attributed to enhanced amplitude of the sensory-motor synapse, however. Therefore LP117 may itself be a site of plasticity for reflexes elicited by tail stimulation.

This article has been cited by other articles:

				X. Ye, J. L. Shobe, S. K. Sharma, A. Marina, and T. J. Carew Small G proteins exhibit pattern sensitivity in MAPK activation during the induction of memory and synaptic facilitation in Aplysia PNAS, December 23, 2008; 105(51): 20511 - 20516. [Abstract] [Full Text] [PDF]

				X. Gasull, X. Liao, M. F. Dulin, C. Phelps, and E. T. Walters Evidence That Long-Term Hyperexcitability of the Sensory Neuron Soma Induced by Nerve Injury in Aplysia Is Adaptive J Neurophysiol, September 1, 2005; 94(3): 2218 - 2230. [Abstract] [Full Text] [PDF]

				A. S. Bristol and T. J. Carew Differential role of inhibition in habituation of two independent afferent pathways to a common motor output Learn. Mem., January 1, 2005; 12(1): 52 - 60. [Abstract] [Full Text] [PDF]

				M. A. Sutton, M. W. Bagnall, S. K. Sharma, J. Shobe, and T. J. Carew Intermediate-Term Memory for Site-Specific Sensitization in Aplysia Is Maintained by Persistent Activation of Protein Kinase C J. Neurosci., April 7, 2004; 24(14): 3600 - 3609. [Abstract] [Full Text] [PDF]

				A. S. Bristol, M. A. Sutton, and T. J. Carew Neural Circuit of Tail-Elicited Siphon Withdrawal in Aplysia. I. Differential Lateralization of Sensitization and Dishabituation J Neurophysiol, February 1, 2004; 91(2): 666 - 677. [Abstract] [Full Text] [PDF]

				G. A. Phares, E. G. Antzoulatos, D. A. Baxter, and J. H. Byrne Burst-Induced Synaptic Depression and Its Modulation Contribute to Information Transfer at Aplysia Sensorimotor Synapses: Empirical and Computational Analyses J. Neurosci., September 10, 2003; 23(23): 8392 - 8401. [Abstract] [Full Text] [PDF]

				D. Barbas, L. DesGroseillers, V. F. Castellucci, T. J. Carew, and S. Marinesco Multiple Serotonergic Mechanisms Contributing to Sensitization in Aplysia: Evidence of Diverse Serotonin Receptor Subtypes Learn. Mem., September 1, 2003; 10(5): 373 - 386. [Abstract] [Full Text] [PDF]

				S. Marinesco, K. L Duran, and W. G Wright Evolution of learning in three aplysiid species: differences in heterosynaptic plasticity contrast with conservation in serotonergic pathways J. Physiol., July 1, 2003; 550(1): 241 - 253. [Abstract] [Full Text] [PDF]

				M. A. Sutton and T. J. Carew Behavioral, Cellular, and Molecular Analysis of Memory in Aplysia I: Intermediate-Term Memory Integr. Comp. Biol., August 1, 2002; 42(4): 725 - 735. [Abstract] [Full Text] [PDF]

				M. L. Wainwright, H. Zhang, J. H. Byrne, and L. J. Cleary Localized Neuronal Outgrowth Induced by Long-Term Sensitization Training in Aplysia J. Neurosci., May 15, 2002; 22(10): 4132 - 4141. [Abstract] [Full Text] [PDF]

				W. N. Frost, T. A. Hoppe, J. Wang, and L.-M. Tian Swim Initiation Neurons in Tritonia diomedea Integr. Comp. Biol., August 1, 2001; 41(4): 952 - 961. [Abstract] [Full Text] [PDF]

				S. A. Prescott and R. Chase Sites of Plasticity in the Neural Circuit Mediating Tentacle Withdrawal in the Snail Helix aspersa: Implications for Behavioral Change and Learning Kinetics Learn. Mem., July 1, 1999; 6(4): 363 - 380. [Abstract] [Full Text]

				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]

				S. A. Prescott Interactions between Depression and Facilitation within Neural Networks: Updating the Dual-Process Theory of Plasticity Learn. Mem., November 1, 1998; 5(6): 446 - 466. [Abstract] [Full Text]

				L. J. Cleary, W. L. Lee, and J. H. Byrne Cellular Correlates of Long-Term Sensitization in Aplysia J. Neurosci., August 1, 1998; 18(15): 5988 - 5998. [Abstract] [Full Text] [PDF]

				S. A. Prescott, N. Gill, and R. Chase Neural Circuit Mediating Tentacle Withdrawal in Helix aspersa, With Specific Reference to the Competence of the Motor Neuron C3 J Neurophysiol, December 1, 1997; 78(6): 2951 - 2965. [Abstract] [Full Text] [PDF]

				J. R. Lieb Jr. and W. N. Frost Realistic Simulation of the Aplysia Siphon-Withdrawal Reflex Circuit: Roles of Circuit Elements in Producing Motor Output J Neurophysiol, March 1, 1997; 77(3): 1249 - 1268. [Abstract] [Full Text] [PDF]

				M. Stopfer, X. Chen, Y.-T. Tai, G. S. Huang, and T. J. Carew Site Specificity of Short-Term and Long-Term Habituation in the Tail-Elicited Siphon Withdrawal Reflex of Aplysia J. Neurosci., August 15, 1996; 16(16): 4923 - 4932. [Abstract] [Full Text] [PDF]

				M. Stopfer and T. J. Carew Heterosynaptic Facilitation of Tail Sensory Neuron Synaptic Transmission during Habituation in Tail-Induced Tail and Siphon Withdrawal Reflexes of Aplysia J. Neurosci., August 15, 1996; 16(16): 4933 - 4948. [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]