Journal of Neurophysiology, Vol 71, Issue 2 479-492, Copyright © 1994 by APS

ARTICLES

Whole-cell analysis of ionic currents underlying the firing pattern of neurons in the gustatory zone of the nucleus tractus solitarii

F. Tell and R. M. Bradley
Department of Biologic and Materials Sciences, School of Dentistry, University of Michigan, Ann Arbor 48109-1078.

1. Previous work from this laboratory has shown that rostral nucleus tractus solitarii (rNTS) neurons can be separated into four different classes on the basis of responses to a current injection paradigm consisting of membrane hyperpolarization immediately followed by a depolarizing pulse. These classes have been termed Group I, II, III, and IV neurons. The regular repetitive firing discharge pattern of Group I cells is changed into an irregular spike train by membrane hyperpolarization. Hyperpolarization of Group II neurons delays the firing discharge induced by depolarization. Hyperpolarization had the least effect on the discharge pattern of Group III neurons. The discharge pattern of Group IV neurons consisted of a short burst of spikes. We used whole-cell recordings and pharmacological channel blockers in an in vitro brain stem slice preparation to determine the ionic basis for the repetitive firing properties of rNTS neurons. 2. Application of 4-aminopyridine (4-AP, 1 mM) decreased input resistance and increased action potential duration in all groups of neurons. However, the discharge pattern of Group I, III, and IV neurons was either unaltered or slightly modified by 4-AP. In contrast the delay in firing of Group II cells induced by hyperpolarization was strongly reduced and in some cases completely suppressed by application of 4-AP. This suggests that a 4-AP-sensitive conductance primarily underlies the firing pattern of Group II cells. 3. Voltage-clamp recordings revealed that the delay in Group II neurons is due to a transient outward potassium current that is partially inactivated around the resting membrane potential. Hyperpolarization removed this inactivation, causing a delay in the firing of the cell. The potassium current was blocked by 4-AP. A similar current was occasionally seen in neurons of the other groups. On the basis of its voltage and pharmacological dependence this current was presumed to be an A-current (IKA). 4. Blockade of calcium currents by a low-calcium (0.5 mM) saline containing 2 mM Co2+ depressed the excitability of rNTS cells. For Group II neurons the delay in firing activity was increased. In the other groups the repetitive firing pattern was suppressed. In addition the amplitude of the afterhyperpolarization occurring after a short train of action potentials was substantially reduced. This indicates that calcium currents (ICa) and calcium-activated potassium currents (IKCa) contribute to the repetitive firing properties of rNTS neurons. 5. In about half of Group I, III, and IV neurons an additional property was found.(ABSTRACT TRUNCATED AT 400 WORDS)

This article has been cited by other articles:

				J. Nasse, D. Terman, S. Venugopal, G. Hermann, R. Rogers, and J. B. Travers Local circuit input to the medullary reticular formation from the rostral nucleus of the solitary tract Am J Physiol Regulatory Integrative Comp Physiol, November 1, 2008; 295(5): R1391 - R1408. [Abstract] [Full Text] [PDF]

				T. Suwabe and R. M. Bradley Effects of 5-Hydroxytryptamine and Substance P on Neurons of the Inferior Salivatory Nucleus J Neurophysiol, April 1, 2007; 97(4): 2605 - 2611. [Abstract] [Full Text] [PDF]

				T. Endoh Involvement of Src tyrosine kinase and mitogen-activated protein kinase in the facilitation of calcium channels in rat nucleus of the tractus solitarius by angiotensin II J. Physiol., November 1, 2005; 568(3): 851 - 856. [Abstract] [Full Text] [PDF]

				K. Nataraj and J. J. Wenstrup Roles of Inhibition in Creating Complex Auditory Responses in the Inferior Colliculus: Facilitated Combination-Sensitive Neurons J Neurophysiol, June 1, 2005; 93(6): 3294 - 3312. [Abstract] [Full Text] [PDF]

				P. Lachamp, B. Balland, F. Tell, A. Baude, C. Strube, M. Crest, and J.-P. Kessler Early expression of AMPA receptors and lack of NMDA receptors in developing rat climbing fibre synapses J. Physiol., May 1, 2005; 564(3): 751 - 763. [Abstract] [Full Text] [PDF]

				H. Fukami and R. M. Bradley Biophysical and Morphological Properties of Parasympathetic Neurons Controling the Parotid and von Ebner Salivary Glands in Rats J Neurophysiol, February 1, 2005; 93(2): 678 - 686. [Abstract] [Full Text] [PDF]

				K. L. Barnes, D. M. DeWeese, and M. C. Andresen Angiotensin potentiates excitatory sensory synaptic transmission to medial solitary tract nucleus neurons Am J Physiol Regulatory Integrative Comp Physiol, May 1, 2003; 284(5): R1340 - R1353. [Abstract] [Full Text] [PDF]

				T. W. Bailey, Y.-H. Jin, M. W. Doyle, and M. C. Andresen Vanilloid-Sensitive Afferents Activate Neurons with Prominent A-Type Potassium Currents in Nucleus Tractus Solitarius J. Neurosci., September 15, 2002; 22(18): 8230 - 8237. [Abstract] [Full Text] [PDF]

				A. Jean Brain Stem Control of Swallowing: Neuronal Network and Cellular Mechanisms Physiol Rev, April 1, 2001; 81(2): 929 - 969. [Abstract] [Full Text] [PDF]

				S. Bertrand and J.-R. Cazalets Postinhibitory Rebound During Locomotor-Like Activity in Neonatal Rat Motoneurons In Vitro J Neurophysiol, January 1, 1998; 79(1): 342 - 351. [Abstract] [Full Text] [PDF]

				K. Fujino, K. Koyano, and H. Ohmori Lateral and Medial Olivocochlear Neurons Have Distinct Electrophysiological Properties in the Rat Brain Slice J Neurophysiol, May 1, 1997; 77(5): 2788 - 2804. [Abstract] [Full Text] [PDF]