Journal of Neurophysiology, Vol 68, Issue 4 1307-1320, Copyright © 1992 by APS

ARTICLES

Electrophysiology of the mammillary complex in vitro. I. Tuberomammillary and lateral mammillary neurons

R. R. Llinas and A. Alonso
Department of Physiology and Biophysics, New York University Medical Center, New York 10016.

1. The electrophysiological properties of the tuberomammillary and lateral mammillary neurons in the guinea pig mammillary body were studied using an in vitro brain slice preparation. 2. Tuberomammillary (n = 79) neurons were recorded mainly ventral to the lateral mammillary body as well as ventromedially to the fornix within the rostral part of the medial mammillary nucleus. Intracellular staining with horseradish peroxidase (n = 9) and Lucifer yellow (n = 3) revealed that these cells have several thick, long, spiny dendrites emerging from large (20-35 microns) fusiform somata. 3. Most tuberomammillary neurons (66%) fired spontaneously at a relatively low frequency (0.5-10 Hz) at the resting membrane potential. The action potentials were broad (2.3 ms) with a prominent Ca(2+)-dependent shoulder on the falling phase. Deep (17.8 mV), long-lasting spike afterhyperpolarizations were largely Ca(2+)-independent. 4. All tuberomammillary neurons recorded displayed pronounced delayed firing when the cells were activated from a potential negative to the resting level. The cells also displayed a delayed return to the baseline at the break of hyperpolarizing pulses applied from a membrane potential level close to firing threshold. Analysis of the voltage- and time dependence of this delayed rectification suggested the presence of a transient outward current similar to the A current (IA). These were not completely blocked by high concentrations of 4-aminopyridine, whereas the delayed onset of firing was always abolished when voltage-dependent Ca2+ conductances were blocked by superfusion with Cd2+. 5. Tuberomammillary neurons also displayed inward rectification in the hyperpolarizing and, primarily, depolarizing range. Block of voltage-gated Na(+)-dependent conductances with tetrodotoxin (TTX) selectively abolished inward rectification in the depolarizing range, indicating the presence of a persistent low-threshold sodium-dependent conductance (gNap). In fact, persistent TTX-sensitive, plateau potentials were always elicited following Ca2+ block with Cd2+ when K+ currents were reduced by superfusion with tetraethylammonium. 6. The gNap in tuberomammillary neurons may subserve the pacemaker current underlying the spontaneous firing of these cells. The large-amplitude spike afterhyperpolarization of these neurons sets the availability of the transient outward rectifier, which, in conjunction with the pacemaker current, establishes the rate at which membrane potential approaches spike threshold. 7. Repetitive firing elicited by direct depolarization enhanced the spike shoulder of tuberomammillary neurons. Spike trains were followed by a Ca(2+)-dependent, apamine-sensitive, slow afterhyperpolarization. 8. Lateral mammillary neurons were morphologically and electrophysiologically different from tuberomammillary neurons. All lateral mammillary neurons neurons recorded (n = 44) were silent at rest (-60 mV).(ABSTRACT TRUNCATED AT 400 WORDS)

This article has been cited by other articles:

				H. L. Haas, O. A. Sergeeva, and O. Selbach Histamine in the Nervous System Physiol Rev, July 1, 2008; 88(3): 1183 - 1241. [Abstract] [Full Text] [PDF]

				A. C. Jackson and B. P. Bean State-Dependent Enhancement of Subthreshold A-Type Potassium Current by 4-Aminopyridine in Tuberomammillary Nucleus Neurons J. Neurosci., October 3, 2007; 27(40): 10785 - 10796. [Abstract] [Full Text] [PDF]

				M. Puopolo, E. Raviola, and B. P. Bean Roles of Subthreshold Calcium Current and Sodium Current in Spontaneous Firing of Mouse Midbrain Dopamine Neurons J. Neurosci., January 17, 2007; 27(3): 645 - 656. [Abstract] [Full Text] [PDF]

				K. Takahashi, J.-S. Lin, and K. Sakai Neuronal Activity of Histaminergic Tuberomammillary Neurons During Wake-Sleep States in the Mouse J. Neurosci., October 4, 2006; 26(40): 10292 - 10298. [Abstract] [Full Text] [PDF]

				M. Puopolo, B. P. Bean, and E. Raviola Spontaneous Activity of Isolated Dopaminergic Periglomerular Cells of the Main Olfactory Bulb J Neurophysiol, November 1, 2005; 94(5): 3618 - 3627. [Abstract] [Full Text] [PDF]

				P. Song and X.-J. Wang Angular Path Integration by Moving "Hill of Activity": A Spiking Neuron Model without Recurrent Excitation of the Head-Direction System J. Neurosci., January 26, 2005; 25(4): 1002 - 1014. [Abstract] [Full Text] [PDF]

				I. A. Rybak, K. Ptak, N. A. Shevtsova, and D. R. McCrimmon Sodium Currents in Neurons From the Rostroventrolateral Medulla of the Rat J Neurophysiol, September 1, 2003; 90(3): 1635 - 1642. [Abstract] [Full Text] [PDF]

				V. V. Uteshev, E. M. Meyer, and R. L. Papke Regulation of Neuronal Function by Choline and 4OH-GTS-21 Through alpha 7 Nicotinic Receptors J Neurophysiol, April 1, 2003; 89(4): 1797 - 1806. [Abstract] [Full Text] [PDF]

				G. I. Hatton and Q. Z. Yang Ionotropic Histamine Receptors and H2 Receptors Modulate Supraoptic Oxytocin Neuronal Excitability and Dye Coupling J. Neurosci., May 1, 2001; 21(9): 2974 - 2982. [Abstract] [Full Text] [PDF]

				R. W. Stackman and J. S. Taube Firing Properties of Rat Lateral Mammillary Single Units: Head Direction, Head Pitch, and Angular Head Velocity J. Neurosci., November 1, 1998; 18(21): 9020 - 9037. [Abstract] [Full Text] [PDF]

				I. J. Kirk, S. D. Oddie, J. Konopacki, and B. H. Bland Evidence for Differential Control of Posterior Hypothalamic, Supramammillary, and Medial Mammillary Theta-Related Cellular Discharge by Ascending and Descending Pathways J. Neurosci., September 1, 1996; 16(17): 5547 - 5554. [Abstract] [Full Text] [PDF]