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Journal of Neurophysiology, Vol 74, Issue 6 2281-2294, Copyright © 1995 by APS
ARTICLES |
P. S. Katz and W. N. Frost
Department of Neurobiology and Anatomy, University of Texas Medical School, Houston 77030, USA.
1. Neuromodulation has previously been shown to be intrinsic to the central pattern generator (CPG) circuit that generates the escape swim of the nudibranch mollusk Tritonia diomedea; the dorsal swim interneurons (DSIs) make conventional monosynaptic connections and evoke neuromodulatory effects within the swim motor circuit. The conventional synaptic potentials evoked by a DSI onto cerebral neuron 2 (C2) and onto the dorsal flexion neurons (DFNs) consist of a fast excitatory postsynaptic potential (EPSP) followed by a prolonged slow EPSP. In their neuromodulatory role, the DSIs produce an enhancement of the monosynaptic connections made by C2 onto other CPG circuit interneurons and onto efferent flexion neurons. Previous work showed that the DSIs are immunoreactive for serotonin. Here we provide evidence that both the neurotransmission and the neuromodulation evoked by the DSIs are produced by serotonin, and that these effects may be pharmacologically separable. 2. Previously it was shown that bath-applied serotonin both mimics and occludes the modulation of the C2 synapses by the DSIs. Here we find that pressure-applied puffs of serotonin mimic both the fast and slow EPSPs evoked by a DSI onto a DFN, whereas high concentrations of bath-applied serotonin occlude both of these synaptic components. 3. Consistent with the hypothesis that serotonin mediates the actions of the DSIs, the serotonin reuptake inhibitor imipramine prolongs the duration of the fast DSI-DFN EPSP, increases the amplitude of the slow DSI-DFN EPSP, and increases both the amplitude and duration of the modulation of the C2-DFN synapse by the DSIs. 4.Two serotonergic antagonists were found that block the actions of the DSIs. Gramine blocks the fast DSI-DFN EPSP, and has far less of an effect on the slow EPSP and the modulation. Gramine also diminishes the depolarization evoked by pressure-applied serotonin, showing that it is a serotonin antagonist in this system. In contrast, methysergide greatly reduces both the slow EPSP and the modulation evoked by the DSIs, but has mixed effects on the fast EPSP. Methysergide also blocks the ability of exogenous serotonin to enhance the C2-DFN EPSP, demonstrating that it antagonizes the serotonin receptors responsible for this modulation. 5. Taken together with previous work, these results indicate that serotonin is likely to be responsible for all three actions of the DSIs that were examined: the fast and slow DSI-DFN EPSPs and the neuromodulation of the C2-DFN synapse. These results also indicate that the conventional and neuromodulatory effects of the DSIs may be pharmacologically separable. In future work it may be possible to determine the functional role of each in the swim circuit.
This article has been cited by other articles:
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  E. V. Megalou, C. J. Brandon, and W. N. Frost Evidence That the Swim Afferent Neurons of Tritonia diomedea Are Glutamatergic Biol. Bull., April 1, 2009; 216(2): 103 - 112. [Abstract] [Full Text] [PDF]
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 J. M Newcomb and P. S Katz Different functions for homologous serotonergic interneurons and serotonin in species-specific rhythmic behaviours Proc R Soc B, January 7, 2009; 276(1654): 99 - 108. [Abstract] [Full Text] [PDF]
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 E. S. Hill, A. Sakurai, and P. S. Katz Transient Enhancement of Spike-Evoked Calcium Signaling by a Serotonergic Interneuron J Neurophysiol, November 1, 2008; 100(5): 2919 - 2928. [Abstract] [Full Text] [PDF]
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R. J. Calin-Jageman, M. J. Tunstall, B. D. Mensh, P. S. Katz, and W. N. Frost Parameter Space Analysis Suggests Multi-Site Plasticity Contributes to Motor Pattern Initiation in Tritonia J Neurophysiol, October 1, 2007; 98(4): 2382 - 2398. [Abstract] [Full Text] [PDF]
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G. E. Serrano, C. Martinez-Rubio, and M. W. Miller Endogenous Motor Neuron Properties Contribute to a Program-Specific Phase of Activity in the Multifunctional Feeding Central Pattern Generator of Aplysia J Neurophysiol, July 1, 2007; 98(1): 29 - 42. [Abstract] [Full Text] [PDF]
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E. S. Hill and P. S. Katz Role of Membrane Potential in Calcium Signaling During Rhythmic Bursting in Tritonia Swim Interneurons J Neurophysiol, March 1, 2007; 97(3): 2204 - 2214. [Abstract] [Full Text] [PDF]
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G. E. Serrano and M. W. Miller Conditional Rhythmicity and Synchrony in a Bilateral Pair of Bursting Motor Neurons in Aplysia J Neurophysiol, October 1, 2006; 96(4): 2056 - 2071. [Abstract] [Full Text] [PDF]
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L.-M. Tian, R. Kawai, and T. Crow Serotonin-Immunoreactive CPT Interneurons in Hermissenda: Identification of Sensory Input and Motor Projections J Neurophysiol, July 1, 2006; 96(1): 327 - 335. [Abstract] [Full Text] [PDF]
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S. P. Lieske and J.-M. Ramirez Pattern-Specific Synaptic Mechanisms in a Multifunctional Network. II. Intrinsic Modulation by Metabotropic Glutamate Receptors J Neurophysiol, March 1, 2006; 95(3): 1334 - 1344. [Abstract] [Full Text] [PDF]
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M. A. Calvino, I. R. Iscla, and L. Szczupak Selective Serotonin Reuptake Inhibitors Induce Spontaneous Interneuronal Activity in the Leech Nervous System J Neurophysiol, May 1, 2005; 93(5): 2644 - 2655. [Abstract] [Full Text] [PDF]
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M. Diaz-Rios and M. W. Miller Rapid Dopaminergic Signaling by Interneurons That Contain Markers for Catecholamines and GABA in the Feeding Circuitry of Aplysia J Neurophysiol, April 1, 2005; 93(4): 2142 - 2156. [Abstract] [Full Text] [PDF]
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 A. Sakurai and P. S. Katz Spike Timing-Dependent Serotonergic Neuromodulation of Synaptic Strength Intrinsic to a Central Pattern Generator Circuit J. Neurosci., November 26, 2003; 23(34): 10745 - 10755. [Abstract] [Full Text] [PDF]
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S. Clemens and P. S. Katz G Protein Signaling in a Neuronal Network is Necessary for Rhythmic Motor Pattern Production J Neurophysiol, February 1, 2003; 89(2): 762 - 772. [Abstract] [Full Text] [PDF]
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W. H. Watson III, J. M. Newcomb, and S. Thompson Neural Correlates of Swimming Behavior in Melibe leonina Biol. Bull., October 1, 2002; 203(2): 152 - 160. [Abstract] [Full Text] [PDF]
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 T. Nagayama Serotonergic modulation of nonspiking local interneurones in the terminal abdominal ganglion of the crayfish J. Exp. Biol., October 1, 2002; 205(19): 3067 - 3076. [Abstract] [Full Text] [PDF]
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I. R. Popescu and W. N. Frost Highly Dissimilar Behaviors Mediated by a Multifunctional Network in the Marine Mollusk Tritonia diomedea J. Neurosci., March 1, 2002; 22(5): 1985 - 1993. [Abstract] [Full Text] [PDF]
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P. T. Morgan, J. Jing, F. S. Vilim, and K. R. Weiss Interneuronal and Peptidergic Control of Motor Pattern Switching in Aplysia J Neurophysiol, January 1, 2002; 87(1): 49 - 61. [Abstract] [Full Text] [PDF]
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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]
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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]
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G. D. Brown The Role of Serotonin in Tritonia diomedea Integr. Comp. Biol., August 1, 2001; 41(4): 976 - 982. [Abstract] [Full Text] [PDF]
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S. Clemens and P. S. Katz Identified Serotonergic Neurons in the Tritonia Swim CPG Activate Both Ionotropic and Metabotropic Receptors J Neurophysiol, January 1, 2001; 85(1): 476 - 479. [Abstract] [Full Text] [PDF]
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P. T. Morgan, R. Perrins, P. E. Lloyd, and K. R. Weiss Intrinsic and Extrinsic Modulation of a Single Central Pattern Generating Circuit J Neurophysiol, September 1, 2000; 84(3): 1186 - 1193. [Abstract] [Full Text] [PDF]
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D. J. Fickbohm and P. S. Katz Paradoxical Actions of the Serotonin Precursor 5-hydroxytryptophan on the Activity of Identified Serotonergic Neurons in a Simple Motor Circuit J. Neurosci., February 15, 2000; 20(4): 1622 - 1634. [Abstract] [Full Text] [PDF]
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 B. D. Burrell and C. L. Sahley Serotonin Depletion Does Not Prevent Intrinsic Sensitization in the Leech Learn. Mem., September 1, 1999; 6(5): 509 - 520. [Abstract] [Full Text]
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B. D. Burrell and C. L. Sahley Generalization of Habituation and Intrinsic Sensitization in the Leech Learn. Mem., November 1, 1998; 5(6): 405 - 419. [Abstract] [Full Text]
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S. Clemens, J.-C. Massabuau, A. Legeay, P. Meyrand, and J. Simmers In Vivo Modulation of Interacting Central Pattern Generators in Lobster Stomatogastric Ganglion: Influence of Feeding and Partial Pressure of Oxygen J. Neurosci., April 1, 1998; 18(7): 2788 - 2799. [Abstract] [Full Text] [PDF]
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P. S. Katz and W. N. Frost Removal of Spike Frequency Adaptation via Neuromodulation Intrinsic to the Tritonia Escape Swim Central Pattern Generator J. Neurosci., October 15, 1997; 17(20): 7703 - 7713. [Abstract] [Full Text] [PDF]
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E. M. Quinlan, B. C. Arnett, and A. D. Murphy Feeding Stimulants Activate an Identified Dopaminergic Interneuron That Induces the Feeding Motor Program in Helisoma J Neurophysiol, August 1, 1997; 78(2): 812 - 824. [Abstract] [Full Text] [PDF]
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M. Bartos and M. P. Nusbaum Intercircuit Control of Motor Pattern Modulation by Presynaptic Inhibition J. Neurosci., April 1, 1997; 17(7): 2247 - 2256. [Abstract] [Full Text] [PDF]
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