Abstract
The monoamines dopamine (DA), serotonin (5HT), and octopamine (Oct) can each sculpt a unique motor pattern from the pyloric network in the stomatogastric ganglion (STG) of the spiny lobster Panulirus interruptus. In this paper we investigate the contribution of individual network components in determining the specific amine-induced cycle frequency. We used photoinactivation of identified neurons and pharmacological blockade of synapses to isolate the anterior burster (AB) and pyloric dilator (PD) neurons. Bath application of DA, 5HT, or Oct enhanced cycle frequency in an isolated AB neuron, with DA generating the most rapid oscillations and Oct the slowest. When an AB-PD or AB-2xPD subnetworks were tested, DA often reduced the ongoing cycle frequency, whereas 5HT and Oct both evoked similar accelerations in cycle frequency. However, in the intact pyloric network, both DA and Oct either reduced or did not alter the cycle frequency, whereas 5HT continued to enhance the cycle frequency as before. Our results show that the major target of 5HT in altering the pyloric cycle frequency is the AB neuron, whereas DA's effects on the AB-2xPD subnetwork are critical in understanding its modulation of the cycle frequency. Octopamine's effects on cycle frequency require an understanding of its modulation of the feedback inhibition to the AB-PD group from the lateral pyloric neuron, which constrains the pacemaker group to oscillate more slowly than it would alone. We have thus demonstrated that the relative importance of the different network components in determining the final cycle frequency is not fixed but can vary under different modulatory conditions.
MeSH Terms
Animals
Biogenic Monoamines/physiology
Dopamine/pharmacology,physiology
Efferent Pathways/physiology
Female
Ganglia, Invertebrate/physiology
Male
Nephropidae/physiology
Nerve Net/physiology
Neurons/drug effects,physiology
Octopamine/physiology
Pylorus/innervation
Serotonin/physiology
Chemicals
Biogenic Monoamines
Octopamine
Serotonin
Dopamine
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Ayali A
Section of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853, USA.
Harris-Warrick R M
References (30)
30 references, click to expand
-
Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. III. Synaptic connections of electrically coupled pyloric neurons.
J Neurophysiol. 1982 Dec;48(6):1392-1415
PMID: 6296329
-
Aminergic modulation of graded synaptic transmission in the lobster stomatogastric ganglion.
J Neurosci. 1990 Jul;10(7):2066-76
PMID: 2165519
-
Interaction of dopamine and cardiac sac modulatory inputs on the pyloric network in the lobster stomatogastric ganglion.
Brain Res. 1998 May 25;794(1):155-61
PMID: 9630592
-
Rapid killing of single neurons by irradiation of intracellularly injected dye.
Science. 1979 Nov 9;206(4419):702-4
PMID: 386514
-
Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. I. Pyloric system.
J Neurophysiol. 1980 Dec;44(6):1102-21
PMID: 6256508
-
Aminergic modulation in lobster stomatogastric ganglion. II. Target neurons of dopamine, octopamine, and serotonin within the pyloric circuit.
J Neurophysiol. 1986 May;55(5):866-81
PMID: 3086514
-
Modulation of neural networks for behavior.
Annu Rev Neurosci. 1991;14:39-57
PMID: 2031576
-
Emerging principles governing the operation of neural networks.
Annu Rev Neurosci. 1989;12:185-204
PMID: 2648949
-
Neuropeptide fusion of two motor-pattern generator circuits.
Nature. 1990 Mar 8;344(6262):155-8
PMID: 2308633
-
The stomatogastric nervous system: structure and function of a small neural network.
Prog Neurobiol. 1976;7(3):215-90
PMID: 11525
-
Oscillating Networks: Control of Burst Duration by Electrically Coupled Neurons.
Neural Comput. 1991 Winter;3(4):487-497
PMID: 31167330
-
CNS control of pattern generators in the lobster stomatogastric ganglion.
Brain Res. 1979 Nov 30;177(3):598-602
PMID: 227545
-
Distributed amine modulation of graded chemical transmission in the pyloric network of the lobster stomatogastric ganglion.
J Neurophysiol. 1995 Jul;74(1):437-52
PMID: 7472345
-
Amine modulation of electrical coupling in the pyloric network of the lobster stomatogastric ganglion.
J Comp Physiol A. 1993;172(6):715-32
PMID: 8350285
-
Modulation of the lobster pyloric rhythm by the peptide proctolin.
J Neurosci. 1987 Jul;7(7):2097-112
PMID: 3612231
-
Dopamine modulates graded and spike-evoked synaptic inhibition independently at single synapses in pyloric network of lobster.
J Neurophysiol. 1998 Apr;79(4):2063-9
PMID: 9535968
-
Dopamine modulates two potassium currents and inhibits the intrinsic firing properties of an identified motor neuron in a central pattern generator network.
J Neurophysiol. 1999 Jan;81(1):29-38
PMID: 9914264
-
Quantitative single-cell-reverse transcription-PCR demonstrates that A-current magnitude varies as a linear function of shal gene expression in identified stomatogastric neurons.
J Neurosci. 1997 Sep 1;17(17):6597-610
PMID: 9254672
-
Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. IV. Network properties of pyloric system.
J Neurophysiol. 1982 Dec;48(6):1416-32
PMID: 7153799
-
Dopamine modulation of two subthreshold currents produces phase shifts in activity of an identified motoneuron.
J Neurophysiol. 1995 Oct;74(4):1404-20
PMID: 8989381
-
The effect of electrical coupling on the frequency of model neuronal oscillators.
Science. 1990 Apr 6;248(4951):83-5
PMID: 2321028
-
Aminergic modulation in lobster stomatogastric ganglion. I. Effects on motor pattern and activity of neurons within the pyloric circuit.
J Neurophysiol. 1986 May;55(5):847-65
PMID: 3086513
-
Dopamine modulation of transient potassium current evokes phase shifts in a central pattern generator network.
J Neurosci. 1995 Jan;15(1 Pt 1):342-58
PMID: 7823140
-
Amine modulation of glutamate responses from pyloric motor neurons in lobster stomatogastric ganglion.
J Neurophysiol. 1997 Dec;78(6):3210-21
PMID: 9405540
-
A mechanism for production of phase shifts in a pattern generator.
J Neurophysiol. 1984 Jun;51(6):1375-93
PMID: 6145759
-
Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. II. Oscillatory properties of pyloric neurons.
J Neurophysiol. 1982 Dec;48(6):1378-91
PMID: 7153798
-
Multiple mechanisms of bursting in a conditional bursting neuron.
J Neurosci. 1987 Jul;7(7):2113-28
PMID: 3112322
-
Pharmacological dissection of pyloric network of the lobster stomatogastric ganglion using picrotoxin.
J Neurophysiol. 1980 Dec;44(6):1089-1101
PMID: 6256507
-
Roles for electrical coupling in neural circuits as revealed by selective neuronal deletions.
J Exp Biol. 1984 Sep;112:147-67
PMID: 6392466
-
Artificial electrical synapses in oscillatory networks.
J Neurophysiol. 1992 Jun;67(6):1691-4
PMID: 1629771