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. 2011 Jan;105(1):224-34.
doi: 10.1152/jn.00636.2010. Epub 2010 Nov 10.

Characteristics of calcium currents in rat geniculate ganglion neurons

Shiro Nakamura  1 , Robert M Bradley
Affiliations

Characteristics of calcium currents in rat geniculate ganglion neurons

Shiro Nakamura et al. J Neurophysiol. 2011 Jan.

Abstract

Geniculate ganglion (GG) cell bodies of chorda tympani (CT), greater superficial petrosal (GSP), and posterior auricular (PA) nerves transmit orofacial sensory information to the rostral nucleus of the solitary tract (rNST). We used whole cell recording to study the characteristics of the Ca(2+) channels in isolated Fluorogold-labeled GG neurons that innervate different peripheral receptive fields. PA neurons were significantly larger than CT and GSP neurons, and CT neurons could be further subdivided based on soma diameter. Although all GG neurons possess both low voltage-activated (LVA) "T-type" and high voltage-activated (HVA) Ca(2+) currents, CT, GSP, and PA neurons have distinctly different Ca(2+) current expression patterns. Of GG neurons that express T-type currents, the CT and GSP neurons had moderate and PA neurons had larger amplitude T-type currents. HVA Ca(2+) currents in the GG neurons were separated into several groups using specific Ca(2+) channel blockers. Sequential applications of L, N, and P/Q-type channel antagonists inhibited portions of Ca(2+) current in all CT, GSP, and PA neurons to a different extent in each neuron group. No difference was observed in the percentage of L- and N-type Ca(2+) currents reduced by the antagonists in CT, GSP, and PA neurons. Action potentials in GG neurons are followed by a Ca(2+) current initiated after depolarization (ADP) that may influence intrinsic firing patterns. These results show that based on Ca(2+) channel expression the GG contains a heterogeneous population of sensory neurons possibly related to the type of sensory information they relay to the rNST.

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Figures

Fig. 1.
Fig. 1.
Whole cell Ca2+ currents in a geniculate ganglion (GG) neuron. A: example of current traces in a greater superficial petrosal (GSP) neuron activated by depolarizing step pulses (150 ms) from a holding potential of –90 mV to test potentials (Vt) from −80 to 60 mV as shown at the top right in each trace. A fast decaying component of current was observed first at a Vt of −50 mV (arrowhead). B: current traces elicited from a holding potential of −40 mV as shown at the top right in each trace. Note the disappearance of transient inactivating components shown in A. Current traces in A and B were obtained from the same neuron. C: I–V relationship obtained from the current traces shown in A and B.
Fig. 2.
Fig. 2.
Whole cell Ca2+ currents in different subpopulations of GG neurons. A–C: families of Ca2+ currents evoked in representative chorda tympani (CT) (A), GSP (B), and posterior auricular (PA) (C) neurons by depolarizing steps from a holding potential of −90 mV to test potentials from −80 to 60 mV in 10 mV increments (top) and the representative current traces evoked from a holding potential of −90 mV to test potentials of −40 and 0 mV (bottom). Current traces in the bottom were obtained from the same neurons as in the top. Voltage protocols used to activate Ca2+ currents in A–C are shown below the current traces in column A. Note that CT and GSP neurons had small T-type Ca2+ currents and large high voltage–activated (HVA) Ca2+ currents, whereas PA neurons had large T-type Ca2+ currents and equally prominent HVA Ca2+ currents. D: average I-V curve obtained from CT, GSP, and PA neurons. The I-V curve for PA neurons displays a prominent shoulder at hyperpolarized test potentials. All points are the mean values from 45 CT, 32 GSP, and 28 PA neurons, respectively. E: histogram of the average ratio of currents at a test potential of −40 mV (I−40 mV) to currents at a test potential of 0 mV (I0 mV) for CT, GSP, and PA neurons (n = 45, 32, and 28 neurons, respectively). The ratio of T-type Ca2+ current to total Ca2+ current was significantly higher in PA neurons than in CT and GSP neurons (P < 0.01). In this and subsequent figures, error bars indicate mean ± SE and significant differences are marked by *P < 0.05 or **P < 0.01.
Fig. 3.
Fig. 3.
Comparison of T-type Ca2+ current characteristics in different subpopulations of GG neurons. A: histogram of the percentage of CT, GSP, and PA neurons with T-type Ca2+ currents. More PA neurons (27 of 28) had T-type Ca2+ currents than CT (28 of 45) and GSP neurons (26 of 32). B: frequency distributions of soma diameters of CT neurons with and without T-type Ca2+ currents. The data points are fitted by normal distribution curves (continuous curves). Average soma diameter of CT neurons with T-type Ca2+ currents was significantly different from CT neurons without T-type Ca2+ currents (P < 0.01). C: representative T-type Ca2+ current traces evoked by a step pulse from a holding potential of −90 mV to a test potential of −40 mV in a CT, GSP, and PA neuron. The amplitude of T-type Ca2+ current was larger in the PA neuron than the CT and the GSP neuron. D: histogram of the average T-type Ca2+ current density for CT, GSP, and PA neurons. There was a significant difference in the T-type Ca2+ current density between CT, GSP, and PA neurons (P < 0.05 or higher).
Fig. 4.
Fig. 4.
Voltage dependence of activation and steady-state inactivation for T-type Ca2+ currents in different subpopulations of GG neurons. A: representative current traces evoked by 150 ms step pulses to test potentials from −80 to −40 mV in 10 mV increments from a holding potential of −90 mV to investigate the voltage dependence of activation. B: representative current traces by varying the holding potentials from −100 to −40 mV for 2 s in 10 mV increments before changing the voltage to the test potential of −40 mV for 250 ms for the voltage dependence of steady-state inactivation. The bottom panels indicate voltage protocols. C: activation curve obtained from CT (□), GSP (○), and PA neurons (▵). Relative conductance (G/Gmax) of T-type Ca2+ current was plotted against membrane potential. D: steady-state inactivation curve from CT (□), GSP (○), and PA neurons (▵). Normalized current (I/Imax) was plotted against membrane potential. Data were fitted with a Boltzmann curve. There were no significant differences in the voltage dependence of activation and inactivation of the T-type Ca2+ currents between 3 subpopulations of GG neurons (P > 0.05).
Fig. 5.
Fig. 5.
Blocking effects of calcium channel antagonists on HVA Ca2+ currents in different subpopulations of GG neurons. HVA Ca2+ currents were evoked by repetitive constant step pulses to a test potential of −10 mV from a holding potential of −60 mV in CT (A), GSP (B), and PA neurons (C). Peak amplitude of current was plotted against time (A–C, left). Superimposed current traces in the right in A–C were selected from continuous recordings in the left at the locations indicated by corresponding numbers (labeled 1–5). Sequential application of nimodipine (5 μM), ω-conotoxin GVIA (ω-CgTX, 1 μM), and ω-agatoxin IVA (ω-Aga IVA, 200 nM) reduced the part of HVA Ca2+ currents but did not completely suppress HVA currents. Cd2+ (100 μM) completely blocked all the remaining currents.
Fig. 6.
Fig. 6.
Comparison of the different subtypes of Ca2+ currents in different subpopulations of GG neurons. Histogram shows the average percentage of total Ca2+ current blocked by nimodipine, ω-CgTX, and ω-Aga IVA in CT (n = 10), GSP (n = 10), and PA neurons (n = 10), obtained in experiments similar to those shown in Fig. 5. The residual component was estimated as the fraction of Ca2+ currents resistant to nimodipine, ω-CgTX, and ω-Aga IVA. There were significant differences in the percentage of P/Q-type Ca2+ current blocked by ω-Aga IVA and residual fraction of Ca2+ current between 3 subpopulations of GG neurons (P < 0.01 or higher).
Fig. 7.
Fig. 7.
Action potential and afterdepolarization (ADP) in different subpopulations of GG neurons. A: action potential evoked from successively more hyperpolarized membrane potentials. Note that the ADP was elicited from a membrane potential of −77 mV (arrowhead in the middle). B: effect of change in extracellular Ca2+ concentration. An action potential and ADP were evoked in 2 mM Ca2+ (control, left), 6 mM Ca2+ (high Ca2+, middle), and after returning to 2 mM Ca2+ (wash, right) in external solution in the same neuron. Increasing extracellular Ca2+ concentration caused a strong and reversible enhancement of the ADP. C: effect of Ni2+ application on ADP. Application of Ni2+ (200 μM) abolished the ADP and the additional spike (middle). The ADP returned partially after washout (right). D: effect of Ni2+ on rebound spike evoked after hyperpolarizing current pulses from resting membrane potential: 200 μM Ni2+ decreased the number of the rebound spikes (middle). The effect of Ni2+ was reversed after washout (right).
Fig. 8.
Fig. 8.
Comparison of the frequency of neurons with ADPs in different subpopulations of GG neurons. Histogram of the percentages in CT, GSP, and PA neurons with ADPs at resting membrane potential (RMP) and at a membrane potential of −70 mV. The frequency of PA neurons with ADP (11 of 11 neurons) was significantly higher than GSP neurons (7 of 13 neurons) at a membrane potential of −70 mV (Fisher's exact test: P < 0.05).
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