Journal of Neurophysiology, Vol 51, Issue 6 1362-1374, Copyright © 1984 by APS

ARTICLES

Electrically coupled pacemaker neurons respond differently to same physiological inputs and neurotransmitters

E. Marder and J. S. Eisen

The two pyloric dilator (PD) motor neurons and the single anterior burster (AB) interneuron are electrically coupled and together comprise the pacemaker for the pyloric central pattern generator of the stomatogastric ganglion of the lobster, Panulirus interruptus. Previous work (31) has shown that the AB neuron is an endogenously bursting neuron, while the PD neuron is a conditional burster. In this paper the effects of physiological inputs and neurotransmitters on isolated PD neurons and AB neurons were studied using the lucifer yellow photoinactivation technique (33). Stimulation of the inferior ventricular nerve (IVN) fibers at high frequencies elicits a triphasic response in AB and PD neurons: a rapid excitatory postsynaptic potential (EPSP) followed by a slow inhibitory postsynaptic potential (IPSP), followed by an enhancement of the pacemaker slow-wave depolarizations. Photoinactivation experiments indicate that the enhancement of the slow wave is due primarily to actions of the IVN fibers on the PD neurons but not on the AB neuron. Bath-applied dopamine dramatically alters the motor output of the pyloric system. Photoinactivation experiments show that 10(-4) M dopamine increases the amplitude and frequency of the slow-wave depolarizations recorded in the AB neurons but hyperpolarizes and inhibits the PD neurons. Bath-applied serotonin increases the frequency and amplitude of the slow-wave depolarizations in the AB neuron but has no effect on PD neurons. Pilocarpine, a muscarinic cholinergic agonist, stimulates slow-wave depolarization production in both PD neurons and the AB neuron, but the waveform and frequency of the slow waves elicited are quite different. These results show that although the electrically coupled PD and AB neurons always depolarize synchronously and act together as the pacemaker for the pyloric system, they respond differently to a neuronal input and to several putative neuromodulators. Thus, despite electrical coupling sufficient to ensure synchronous activity, the PD and AB neurons can be modulated independently.

This article has been cited by other articles:

				A. Bibbig, S. Middleton, C. Racca, M. J. Gillies, H. Garner, F. E. N. LeBeau, C. H. Davies, and M. A. Whittington Beta Rhythms (15-20 Hz) Generated by Nonreciprocal Communication in Hippocampus J Neurophysiol, April 1, 2007; 97(4): 2812 - 2823. [Abstract] [Full Text] [PDF]

				V. Zsiros, I. Aradi, and G. Maccaferri Propagation of postsynaptic currents and potentials via gap junctions in GABAergic networks of the rat hippocampus J. Physiol., January 15, 2007; 578(2): 527 - 544. [Abstract] [Full Text] [PDF]

				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]

				C. Soto-Trevino, P. Rabbah, E. Marder, and F. Nadim Computational Model of Electrically Coupled, Intrinsically Distinct Pacemaker Neurons J Neurophysiol, July 1, 2005; 94(1): 590 - 604. [Abstract] [Full Text] [PDF]

				M. C. Clark, T. E. Dever, J. J. Dever, P. Xu, V. Rehder, M. A. Sosa, and D. J. Baro Arthropod 5-HT2 Receptors: A Neurohormonal Receptor in Decapod Crustaceans That Displays Agonist Independent Activity Resulting from an Evolutionary Alteration to the DRY Motif J. Neurosci., March 31, 2004; 24(13): 3421 - 3435. [Abstract] [Full Text] [PDF]

				E. Garcia-Perez, M. Vargas-Caballero, N. Velazquez-Ulloa, A. Minzoni, and F. F. De-Miguel Synaptic Integration in Electrically Coupled Neurons Biophys. J., January 1, 2004; 86(1): 646 - 655. [Abstract] [Full Text] [PDF]

				B. R. Johnson, P. Kloppenburg, and R. M. Harris-Warrick Dopamine Modulation of Calcium Currents in Pyloric Neurons of the Lobster Stomatogastric Ganglion J Neurophysiol, August 1, 2003; 90(2): 631 - 643. [Abstract] [Full Text] [PDF]

				D. Bucher, V. Thirumalai, and E. Marder Axonal Dopamine Receptors Activate Peripheral Spike Initiation in a Stomatogastric Motor Neuron J. Neurosci., July 30, 2003; 23(17): 6866 - 6875. [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]

				M. Thoby-Brisson and J.-M. Ramirez Identification of Two Types of Inspiratory Pacemaker Neurons in the Isolated Respiratory Neural Network of Mice J Neurophysiol, July 1, 2001; 86(1): 104 - 112. [Abstract] [Full Text] [PDF]

				A. M. Swensen and E. Marder Modulators with Convergent Cellular Actions Elicit Distinct Circuit Outputs J. Neurosci., June 1, 2001; 21(11): 4050 - 4058. [Abstract] [Full Text] [PDF]

				F. F. De-Miguel, M. Vargas-Caballero, and E. Garcia-Perez Spread of synaptic potentials through electrical synapses in Retzius neurones of the leech J. Exp. Biol., January 10, 2001; 204(19): 3241 - 3250. [Abstract] [Full Text] [PDF]

				R. M. HARRIS-WARRICK, B. R. JOHNSON, J. H. PECK, P. KLOPPENBURG, A. AYALI, and J. SKARBINSKI Distributed Effects of Dopamine Modulation in the Crustacean Pyloric Network Ann. N.Y. Acad. Sci., November 16, 1998; 860(1): 155 - 167. [Abstract] [Full Text] [PDF]

				E. MARDER, Y. MANOR, F. NADIM, M. BARTOS, and M. P. NUSBAUM Frequency Control of a Slow Oscillatory Network by a Fast Rhythmic Input: Pyloric to Gastric Mill Interactions in the Crab Stomatogastric Nervous System Ann. N.Y. Acad. Sci., November 16, 1998; 860(1): 226 - 238. [Abstract] [Full Text] [PDF]

				B. R. Johnson and R. M. Harris-Warrick Amine Modulation of Glutamate Responses From Pyloric Motor Neurons in Lobster Stomatogastric Ganglion J Neurophysiol, December 1, 1997; 78(6): 3210 - 3221. [Abstract] [Full Text] [PDF]

				E. Marder, L. F. Abbott, G. G. Turrigiano, Z. Liu, and J. Golowasch Memory from the dynamics of intrinsic membrane currents PNAS, November 26, 1996; 93(24): 13481 - 13486. [Abstract] [Full Text] [PDF]

				T. Kepler, E Marder, and L. Abbott The effect of electrical coupling on the frequency of model neuronal oscillators Science, April 6, 1990; 248(4951): 83 - 85. [Abstract] [PDF]