Pre- and postnatal differences in membrane, action potential, and ion channel properties of rostral nucleus of the solitary tract neurons

Abstract

There is little known about the prenatal development of the rostral nucleus of the solitary tract (rNST) neurons in rodents or the factors that influence circuit formation. With morphological and electrophysiological techniques in vitro, we investigated differences in the biophysical properties of rNST neurons in pre- and postnatal rats from embryonic day 14 (E14) through postnatal day 20. Developmental changes in passive membrane and action potential (AP) properties and the emergence and maturation of ion channels important in neuron function were characterized. Morphological maturation of rNST neurons parallels changes in passive membrane properties. Mean soma size, dendritic branch points, neurite endings, and neurite length all increase prenatally. whereas neuron resting membrane potential, input resistance, and time constant decrease. Dendritic spines, on the other hand, develop after birth. AP discharge patterns alter in pre- and postnatal stages. At E14, neurons generated a single TTX-sensitive, voltage-gated Na(+) AP when depolarized; a higher discharge rate appeared at older stages. AP amplitude, half-width, and rise and fall times all change during development. Responses to current injection revealed a number of voltage-gated conductances in embryonic rNST, including a hyperpolarization-activated inward current and a low-threshold Ca(2+) current that initiated Ca(2+) spikes. A hyperpolarization-activated, transient outward potassium current was also present in the developing neurons. Although the properties of these channels change during development, they are present before synapses form and therefore, can contribute to initial establishment of neural circuits, as well as to the changing electrophysiological properties in developing rNST neurons.

Effects of high-fat diet and gastric bypass on neurons in the caudal solitary nucleus

“…As an index of neuron excitability, membrane voltage was measured for each level below threshold and the number of evoked action potentials counted at each level above threshold. Peak action potential amplitude, half-width and the amplitude of the after-hyperpolarization were calculated from the threshold for the action potential defined as the inflection point on the rising phase using standard templates in Clampfit (Suwabe, Mistretta et al 2011). In a second protocol under voltage clamp, we assessed the presence and magnitude of an “I A -like” transient outward current (TOC).…”

Gustatory solitary tract development: A role for neuropilins

“…Neuroanatomical characteristics in rNST of soma size, dendritic branch points, number of neurite endings and neurite length all increase from E14 through postnatal stages (Suwabe et al, 2011). The morphological maturation parallels changes in passive and action potential biophysical properties of the embryonic neurons.…”

“…The morphological maturation parallels changes in passive and action potential biophysical properties of the embryonic neurons. Voltage-gated, sodium channel properties alter dramatically with accompanying changes in discharge rate (Suwabe et al, 2011). In fact, ion channel function, albeit immature, is present before synaptic connections are detected and have proposed contributions to emerging central taste circuits (Suwabe et al, 2011).…”

“…Voltage-gated, sodium channel properties alter dramatically with accompanying changes in discharge rate (Suwabe et al, 2011). In fact, ion channel function, albeit immature, is present before synaptic connections are detected and have proposed contributions to emerging central taste circuits (Suwabe et al, 2011). It is likely that there is an interactive modulation among afferent input and developing collaterals, directed by regulatory molecules including the neuropilins, and developing neuron channel properties that affect the input to emerging rNST.…”

Excitatory and inhibitory synaptic function in the rostral nucleus of the solitary tract in embryonic rat

“…However, ion channel development has a widely ranging prenatal course and changing channel properties can contribute to emergence of synaptic properties and initial establishment of neural circuits in rNST neurons (Suwabe et al, 2011). NST synaptic thickenings appear at E15 and simple symmetrical membrane thickenings are seen at E17 followed by the appearance of vesicles at E19 (Zhang and Ashwell, 2001a).…”