Persistent sodium currents in mesencephalic V neurons participate in burst generation and control of membrane excitability

被引:117
作者
Wu, NP
Enomoto, A
Tanaka, S
Hsiao, CF
Nykamp, DQ
Izhikevich, E
Chandler, SH
机构
[1] Univ Calif Los Angeles, Dept Physiol Sci, Los Angeles, CA 90095 USA
[2] Osaka Univ, Grad Sch Dent, Dept Oral & Maxillofacial Surg 1, Suita, Osaka 565, Japan
[3] Matsumoto Dent Univ, Dept Oral & Maxillofacial Surg, Nagano, Japan
[4] Univ Minnesota, Sch Math, Minneapolis, MN 55455 USA
[5] Inst Neurosci, San Diego, CA USA
关键词
D O I
10.1152/jn.00636.2004
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
The functional and biophysical properties of a persistent sodium current (I-NaP) previously proposed to participate in the generation of subthreshold oscillations and burst discharge in mesencephalic trigeminal sensory neurons (Mes V) were investigated in brain stem slices ( rats, p7 - p12) using whole cell patch-clamp methods. I-NaP activated around - 76 mV and peaked at - 48 mV, with V-1/2 of -58.7 mV. Ramp voltage-clamp protocols showed that I-NaP undergoes time- as well as voltage-dependent inactivation and recovery from inactivation in the range of several seconds (tau(onset) = 2.04 s, tau(recov) = 2.21 s). Riluzole (<= 5 mu M) substantially reduced I-NaP, membrane resonance, postinhibitory rebound (PIR), and subthreshold oscillations, and completely blocked bursting, but produced modest effects on the fast transient Na+ current (I-NaT). Before complete cessation, burst cycle duration was increased substantially, while modest and inconsistent changes in burst duration were observed. The properties of the I-NaT were obtained and revealed that the amplitude and voltage dependence of the resulting "window current" were not consistent with those of the observed I-NaP recorded in the same neurons. This suggests an additional mechanism for the origin of I-NaP. A neuronal model was constructed using Hodgkin-Huxley parameters obtained experimentally for Na+ and K+ currents that simulated the experimentally observed membrane resonance, subthreshold oscillations, bursting, and PIR. Alterations in the model g(NaP) parameters indicate that I-NaP is critical for control of subthreshold and suprathreshold Mes V neuron membrane excitability and burst generation.
引用
收藏
页码:2710 / 2722
页数:13
相关论文
共 60 条
[1]   Persistent sodium channel activity mediates subthreshold membrane potential oscillations and low-threshold spikes in rat entorhinal cortex layer V neurons [J].
Agrawal, N ;
Hamam, BN ;
Magistretti, J ;
Alonso, A ;
Ragsdale, DS .
NEUROSCIENCE, 2001, 102 (01) :53-64
[2]   A NOVEL VOLTAGE-DEPENDENT CATION CURRENT IN RAT NEOCORTICAL NEURONS [J].
ALZHEIMER, C .
JOURNAL OF PHYSIOLOGY-LONDON, 1994, 479 (02) :199-205
[3]  
ALZHEIMER C, 1993, J NEUROSCI, V13, P660
[4]  
Amir R, 1999, J NEUROSCI, V19, P8589
[5]   Burst discharge in primary sensory neurons: Triggered by subthreshold oscillations, maintained by depolarizing afterpotentials [J].
Amir, R ;
Michaelis, M ;
Devor, M .
JOURNAL OF NEUROSCIENCE, 2002, 22 (03) :1187-1198
[6]   Low-threshold, persistent sodium current in rat large dorsal root ganglion neurons in culture [J].
Baker, MD ;
Bostock, H .
JOURNAL OF NEUROPHYSIOLOGY, 1997, 77 (03) :1503-1513
[7]   ELECTROTONIC COUPLING BETWEEN NEURONES IN RAT MESENCEPHALIC NUCLEUS [J].
BAKER, R ;
LLINAS, R .
JOURNAL OF PHYSIOLOGY-LONDON, 1971, 212 (01) :45-+
[8]   Subthreshold oscillation of the membrane potential in magnocellular neurones of the rat supraoptic nucleus [J].
Boehmer, G ;
Greffrath, W ;
Martin, E ;
Hermann, S .
JOURNAL OF PHYSIOLOGY-LONDON, 2000, 526 (01) :115-128
[9]   Models of respiratory rhythm generation in the pre-Botzinger complex. I. Bursting pacemaker neurons [J].
Butera, RJ ;
Rinzel, J ;
Smith, JC .
JOURNAL OF NEUROPHYSIOLOGY, 1999, 82 (01) :382-397
[10]   PERSISTENT NA+ CONDUCTANCE IN MEDIUM-SIZED NEOSTRIATAL NEURONS - CHARACTERIZATION USING INFRARED VIDEOMICROSCOPY AND WHOLE-CELL PATCH-CLAMP RECORDINGS [J].
CEPEDA, C ;
CHANDLER, SH ;
SHUMATE, LW ;
LEVINE, MS .
JOURNAL OF NEUROPHYSIOLOGY, 1995, 74 (03) :1343-1348