Developmental Changes in Electrophysiological Properties and Synaptic Transmission in Rat Intracardiac Ganglion Neurons

Abstract

Rimmer, Katrina and Alexander A. Harper. Developmental changes in electrophysiological properties and synaptic transmission in rat intracardiac ganglion neurons. J Neurophysiol 95: 3543-3552, 2006. First published April 12, 2006 doi:10.1152/jn.01220.2005. We charted postnatal changes in the intrinsic electrophysiological properties and synaptic responses of rat intrinsic cardiac ganglion (ICG) neurons. We developed a whole-mount ganglion preparation of the excised right atrial ganglion plexus. Using intracellular recordings and nerve stimulation we tested the hypothesis that substantial transformations in the intrinsic electrical characteristics and synaptic transmission accompany postnatal development. Membrane potential (E m ) did not change but time constant () and cell capacitance increased with postnatal development. Accordingly, input resistance (R in ) decreased but specific membrane resistance (R m ) increased postnatally.Comparison of the somatic active membrane properties revealed significant changes in electrical phenotype. All neonatal neurons had somatic action potentials (APs) with small overshoots and small afterhyperpolarizations (AHPs). Adult neurons had somatic APs with large overshoots and large AHP amplitudes. The range of AHP duration was larger in adults than in neonates. The AP characteristics of juvenile neurons resembled those of adults, with the exception of AHP duration, which fell midway between neonate and adult values. Phasic, multiply adapting, and tonic evoked discharge activities were recorded from ICG neurons. Most neurons displayed phasic discharge at each developmental stage. All neurons received excitatory synaptic inputs from the vagus or interganglionic nerve trunk(s), the strength of which did not change significantly with postnatal age. The changes in the electrophysiological properties of the postganglionic neuron suggest that increased complexity of parasympathetic regulation of cardiac function accompanies postnatal development.

Phenotypic properties of adult mouse intrinsic cardiac neurons maintained in culture

“…For electrophysiology, neurons were readily distinguished by their large somas (ϳ20 m diameter) with distinct nuclei, and projections from the cell bodies often apposed nearby cells (Fig. The membrane potential of Ϫ43 mV was determined by the zero-current voltage (V-track), and it compared favorably with that reported for rat intracardiac ganglion neurons by sharp glass microelectrodes (25). Values for passive electrical properties taken from whole cell patch-clamp recordings of cells 1 day in culture are shown in Table 2.…”

“…This work has provided evidence that, in addition to cholinergic efferent neurons, the intrinsic cardiac ganglia contain noradrenergic efferent neurons, local circuit neurons, and sensory neurons (3,7). Intrinsic cardiac neurons have been classified as phasic, accommodating/adapting, or tonic depending, respectively, on whether they discharge only one or two action potentials during a constant depolarizing current injection, several action potentials at a decreasing rate, or repetitive action potentials at a constant rate (1,25). Intrinsic cardiac neurons have been classified as phasic, accommodating/adapting, or tonic depending, respectively, on whether they discharge only one or two action potentials during a constant depolarizing current injection, several action potentials at a decreasing rate, or repetitive action potentials at a constant rate (1,25).…”

Reactive oxygen species modulate neuronal excitability in rat intrinsic cardiac ganglia

“…The right atrial ganglion plexus and underlying myocardium were isolated from the dorsal surface of the atria. The preparation was pinned to the Sylgard (Dow-Corning, Midland, MI) covered base of a 35 mm tissue culture dish and superfused with a bicarbonate-buffered Krebs solution comprising (in mM): NaCl 118.4, NaHCO 3 25.0, NaH 2 PO 4 1.13, CaCl 2 1.8, KCl 4.7, MgCl 2 1.3 and glucose 11.1, gassed with Carbogen (95% O 2 :5% CO 2 ) to pH 7.4 (Rimmer and Harper, 2006). The recording chamber was continuously superfused (∼ 2 ml/min) with Krebs solution at 35 °C.…”

SHP-2 deletion in postmigratory neural crest cells results in impaired cardiac sympathetic innervation

“…These studies revealed that cKOs exhibit sinus bradycardia (two-way ANOVA, P = 0.0012; Fig. 3 A and B) beginning at P12, corresponding to the developmental timing of sympathetic control of heart rate (28,29). At P6, before the sympathetic nervous system is thought to be functionally relevant for establishing basal heart rate, there is no difference between mutants and littermate controls ( Fig.…”

“…Sympathetic (i.e., TH-positive) innervation is first observed at the base of the fetal heart; this innervation then extends onto the surface of the atria and eventually to the ventricles before following blood vessels into the ventricular wall to innervate the myocardium and project to the sinoatrial and atrioventricular nodes postnatally (27). The sympathetic innervation of the heart is not functionally relevant (i.e., does not control heart rate) until the second postnatal week of life in rodents (23,28,29), and the adult pattern of innervation is not fully achieved until 3 wk after birth (23,30). This developmental process requires nerve growth factor (NGF), which is produced by the target organ (the myocardium in the case of the heart) and is the main neurotrophic factor in establishing and maintaining sympathetic innervation (31).…”