 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
Volume 16, Number 24, Issue of December 15, 1996 pp. 8105-8114
Copyright ©1996 Society for NeuroscienceRelease of Peptide Cotransmitters in Aplysia: Regulation and Functional Implications
Received June 24, 1996; revised Sept. 20, 1996; accepted Sept. 24, 1996.
F. S. Vilim1, 3, E. C. Cropper3, D. A. Price2, I. Kupfermann1, and K. R. Weiss3 1 Center for Neurobiology and Behavior, College of Physicians and Surgeons, Columbia University, New York, New York 10032, 2 C. V. Whitney Laboratories, University of Florida, St. Augustine, Florida 32086, and 3 Department of Physiology and Biophysics, Mount Sinai School of Medicine, New York, New York 10029
To gain insights into the physiological role of cotransmission, we measured peptide release from cell B15, a motorneuron that utilizes ACh as its primary transmitter but also contains putative peptide cotransmitters, the small cardioactive peptides (SCPs) and the buccalins (BUCs). All stimulation parameters used were in the range in which B15 fires in freely moving animals. We stimulated neuron B15 in bursts and systematically varied the interburst interval, the intraburst frequency, and burst duration. Both peptides were preferentially released when B15 was stimulated at higher intra- or interburst frequencies or with longer burst durations. Across stimulation patterns, the amount of peptide released depended on the mean frequency of stimulation and was independent of the specific pattern of stimulation. The parameters of stimulation that produce a larger release of peptides correspond to those that evoke larger contractions. Large and frequent contractions are likely to fuse or summate, thus disrupting the rhythmic behavior mediated by the muscle innervated by motorneuron B15. Because the combined effect of the SCPs and BUCs is to accelerate the relaxation and shorten the duration of muscle contractions, these peptides reduce the probability of the disruptive fusion or summation of muscle contractions. Because these cotransmitters regulate an aspect of muscle contractions that is not controlled by acetylcholine (ACh), the primary transmitter of B15, we suggest that peptides and ACh form parallel but functionally distinct lines of transmission at the neuromuscular junction. Both types of transmission may be necessary to ensure that behavior remains efficient over a wide range of conditions.
Key words: neuropeptides; dense-core vesicles; peptide release; Aplysia; cotransmission; confocal immunocytochemistry; motorneuron; modulation; muscle contractions; feeding
This article has been cited by other articles:
H.-Y. Koh and K. R. Weiss
Activity-Dependent Peptidergic Modulation of the Plateau-Generating Neuron B64 in the Feeding Network of Aplysia
J Neurophysiol, February 1, 2007; 97(2): 1862 - 1867.
[Abstract] [Full Text] [PDF]
I. Hurwitz, A. Harel, S. Markowitz, O. Noy, and A. J. Susswein
Control of Feeding in Aplysia With Ad Libitum Access to Food: Presence of Food Increases the Intervals Between Feeding Bouts
J Neurophysiol, January 1, 2006; 95(1): 106 - 118.
[Abstract] [Full Text] [PDF]
J. T. Birmingham
Simple Mechanism for Stabilizing Motor Output. Focus on "Temperature Compensation of Neuromuscular Modulation in Aplysia"
J Neurophysiol, November 1, 2005; 94(5): 2997 - 2998.
[Full Text] [PDF]
Y. Zhurov and V. Brezina
Temperature Compensation of Neuromuscular Modulation in Aplysia
J Neurophysiol, November 1, 2005; 94(5): 3259 - 3277.
[Abstract] [Full Text] [PDF]
H.-Y. Koh and K. R. Weiss
Peptidergic Contribution to Posttetanic Potentiation at a Central Synapse of Aplysia
J Neurophysiol, August 1, 2005; 94(2): 1281 - 1286.
[Abstract] [Full Text] [PDF]
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]
V. Brezina, C. C. Horn, and K. R. Weiss
Modeling Neuromuscular Modulation in Aplysia. III. Interaction of Central Motor Commands and Peripheral Modulatory State for Optimal Behavior
J Neurophysiol, March 1, 2005; 93(3): 1523 - 1556.
[Abstract] [Full Text] [PDF]
V. Brezina, I. V. Orekhova, and K. R. Weiss
Neuromuscular Modulation in Aplysia. I. Dynamic Model
J Neurophysiol, October 1, 2003; 90(4): 2592 - 2612.
[Abstract] [Full Text] [PDF]
V. Brezina, I. V. Orekhova, and K. R. Weiss
Neuromuscular Modulation in Aplysia. II. Modulation of the Neuromuscular Transform in Behavior
J Neurophysiol, October 1, 2003; 90(4): 2613 - 2628.
[Abstract] [Full Text] [PDF]
H.-Y. Koh, F. S. Vilim, J. Jing, and K. R. Weiss
Two Neuropeptides Colocalized in a Command-Like Neuron Use Distinct Mechanisms to Enhance Its Fast Synaptic Connection
J Neurophysiol, September 1, 2003; 90(3): 2074 - 2079.
[Abstract] [Full Text] [PDF]
I. V. Orekhova, V. Alexeeva, P. J. Church, K. R. Weiss, and V. Brezina
Multiple Presynaptic and Postsynaptic Sites of Inhibitory Modulation by Myomodulin at ARC Neuromuscular Junctions of Aplysia
J Neurophysiol, March 1, 2003; 89(3): 1488 - 1502.
[Abstract] [Full Text] [PDF]
B. D. Burrell, C. L. Sahley, and K. J. Muller
Differential Effects of Serotonin Enhance Activity of an Electrically Coupled Neural Network
J Neurophysiol, June 1, 2002; 87(6): 2889 - 2895.
[Abstract] [Full Text] [PDF]
C. J. H. Elliott and A. J. Susswein
Comparative neuroethology of feeding control in molluscs
J. Exp. Biol., April 1, 2002; 205(7): 877 - 896.
[Abstract] [Full Text] [PDF]
V. Thirumalai and E. Marder
Colocalized Neuropeptides Activate a Central Pattern Generator by Acting on Different Circuit Targets
J. Neurosci., March 1, 2002; 22(5): 1874 - 1882.
[Abstract] [Full Text] [PDF]
L. E. Fox and P. E. Lloyd
Evidence That Post-Tetanic Potentiation Is Mediated by Neuropeptide Release in Aplysia
J Neurophysiol, December 1, 2001; 86(6): 2845 - 2855.
[Abstract] [Full Text] [PDF]
K. Ohnuma, M. D Whim, R. D Fetter, L. K Kaczmarek, and R. S Zucker
Presynaptic target of Ca2+ action on neuropeptide and acetylcholine release in Aplysia californica
J. Physiol., September 15, 2001; 535(3): 647 - 662.
[Abstract] [Full Text] [PDF]
S. Gutovitz, J. T. Birmingham, J. A. Luther, D. J. Simon, and E. Marder
GABA Enhances Transmission at an Excitatory Glutamatergic Synapse
J. Neurosci., August 15, 2001; 21(16): 5935 - 5943.
[Abstract] [Full Text] [PDF]
I. V. Orekhova, J. Jing, V. Brezina, R. A. DiCaprio, K. R. Weiss, and E. C. Cropper
Sonometric Measurements of Motor-Neuron-Evoked Movements of an Internal Feeding Structure (the Radula) in Aplysia
J Neurophysiol, August 1, 2001; 86(2): 1057 - 1061.
[Abstract] [Full Text] [PDF]
B. D. Burrell, C. L. Sahley, and K. J. Muller
Non-Associative Learning and Serotonin Induce Similar Bi-Directional Changes in Excitability of a Neuron Critical for Learning in the Medicinal Leech
J. Neurosci., February 15, 2001; 21(4): 1401 - 1412.
[Abstract] [Full Text] [PDF]
I. Hurwitz, E. C. Cropper, F. S. Vilim, V. Alexeeva, A. J. Susswein, I. Kupfermann, and K. R. Weiss
Serotonergic and Peptidergic Modulation of the Buccal Mass Protractor Muscle (I2) in Aplysia
J Neurophysiol, December 1, 2000; 84(6): 2810 - 2820.
[Abstract] [Full Text] [PDF]
A. Balkowiec and D. M. Katz
Activity-Dependent Release of Endogenous Brain-Derived Neurotrophic Factor from Primary Sensory Neurons Detected by ELISA In Situ
J. Neurosci., October 1, 2000; 20(19): 7417 - 7423.
[Abstract] [Full Text] [PDF]
V. Brezina, P. J. Church, and K. R. Weiss
Temporal Pattern Dependence of Neuronal Peptide Transmitter Release: Models and Experiments
J. Neurosci., September 15, 2000; 20(18): 6760 - 6772.
[Abstract] [Full Text] [PDF]
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]
D. Deodhar and I. Kupfermann
Studies of Neuromodulation of Oscillatory Systems in Aplysia, by Means of Genetic Algorithms
Adaptive Behavior, June 1, 2000; 8(3-4): 267 - 296.
[Abstract] [PDF]
S. C. Rosen, M. W. Miller, C. G. Evans, E. C. Cropper, and I. Kupfermann
Diverse Synaptic Connections Between Peptidergic Radula Mechanoafferent Neurons and Neurons in the Feeding System of Aplysia
J Neurophysiol, March 1, 2000; 83(3): 1605 - 1620.
[Abstract] [Full Text] [PDF]
F. S. Vilim, E. C. Cropper, D. A. Price, I. Kupfermann, and K. R. Weiss
Peptide Cotransmitter Release from Motorneuron B16 in Aplysia californica: Costorage, Corelease, and Functional Implications
J. Neurosci., March 1, 2000; 20(5): 2036 - 2042.
[Abstract] [Full Text] [PDF]
V. Brezina, I. V. Orekhova, and K. R. Weiss
The Neuromuscular Transform: The Dynamic, Nonlinear Link Between Motor Neuron Firing Patterns and Muscle Contraction in Rhythmic Behaviors
J Neurophysiol, January 1, 2000; 83(1): 207 - 231.
[Abstract] [Full Text] [PDF]
V. Brezina, I. V. Orekhova, and K. R. Weiss
Optimization of Rhythmic Behaviors by Modulation of the Neuromuscular Transform
J Neurophysiol, January 1, 2000; 83(1): 260 - 279.
[Abstract] [Full Text] [PDF]
J. T. Birmingham, Z. B. Szuts, L. F. Abbott, and E. Marder
Encoding of Muscle Movement on Two Time Scales by a Sensory Neuron That Switches Between Spiking and Bursting Modes
J Neurophysiol, November 1, 1999; 82(5): 2786 - 2797.
[Abstract] [Full Text] [PDF]
Y. Fujisawa, Y. Furukawa, S. Ohta, T. A. Ellis, N. C. Dembrow, L. Li, P. D. Floyd, J. V. Sweedler, H. Minakata, K. Nakamaru, et al.
The Aplysia Mytilus Inhibitory Peptide-Related Peptides: Identification, Cloning, Processing, Distribution, and Action
J. Neurosci., November 1, 1999; 19(21): 9618 - 9634.
[Abstract] [Full Text] [PDF]
C. Keating and P. E. Lloyd
Differential Modulation of Motor Neurons That Innervate the Same Muscle but Use Different Excitatory Transmitters in Aplysia
J Neurophysiol, October 1, 1999; 82(4): 1759 - 1767.
[Abstract] [Full Text] [PDF]
C. G. Evans, F. S. Vilim, O. Harish, I. Kupfermann, K. R. Weiss, and E. C. Cropper
Modulation of Radula Opener Muscles in Aplysia
J Neurophysiol, September 1, 1999; 82(3): 1339 - 1351.
[Abstract] [Full Text] [PDF]
A. Meir, S. Ginsburg, A. Butkevich, S. G. Kachalsky, I. Kaiserman, R. Ahdut, S. Demirgoren, and R. Rahamimoff
Ion Channels in Presynaptic Nerve Terminals and Control of Transmitter Release
Physiol Rev, July 1, 1999; 79(3): 1019 - 1088.
[Abstract] [Full Text] [PDF]
Y. Xin, I. Hurwitz, R. Perrins, C. G. Evans, V. Alexeeva, K. R. Weiss, and I. Kupfermann
Actions of a Pair of Identified Cerebral-Buccal Interneurons (CBI-8/9) in Aplysia That Contain the Peptide Myomodulin
J Neurophysiol, February 1, 1999; 81(2): 507 - 520.
[Abstract] [Full Text] [PDF]
X.-Y. Jiang and T. W. Abrams
Use-Dependent Decline of Paired-Pulse Facilitation at Aplysia Sensory Neuron Synapses Suggests a Distinct Vesicle Pool or Release Mechanism
J. Neurosci., December 15, 1998; 18(24): 10310 - 10319.
[Abstract] [Full Text] [PDF]
L. E. Fox and P. E. Lloyd
Serotonergic Neurons Differentially Modulate the Efficacy of Two Motor Neurons Innervating the Same Muscle Fibers in Aplysia
J Neurophysiol, August 1, 1998; 80(2): 647 - 655.
[Abstract] [Full Text] [PDF]
S. C. Baraban, G. Hollopeter, J. C. Erickson, P. A. Schwartzkroin, and R. D. Palmiter
Knock-Out Mice Reveal a Critical Antiepileptic Role for Neuropeptide Y
J. Neurosci., December 1, 1997; 17(23): 8927 - 8936.
[Abstract] [Full Text] [PDF]
M. L. Scott, V. Brezina, and K. R. Weiss
Ion Currents and Mechanisms of Modulation in the Radula Opener Muscles of Aplysia
J Neurophysiol, November 1, 1997; 78(5): 2372 - 2387.
[Abstract] [Full Text] [PDF]
B. K. Modney, C. L. Sahley, and K. J. Muller
Regeneration of a Central Synapse Restores Nonassociative Learning
J. Neurosci., August 15, 1997; 17(16): 6478 - 6482.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|