Electrophysiological properties of identified oxytocin and vasopressin neurones

Abstract

To understand the contribution of intrinsic membrane properties to the different in vivo firing patterns of oxytocin (OT) and vasopressin (VP) neurones, in vitro studies are needed, where stable intracellular recordings can be made. Combining immunochemistry for OT and VP and intracellular dye injections allows characterisation of identified OT and VP neurones, and several differences between the two cell types have emerged. These include a greater transient K+ current that delays spiking to stimulus onset, and a higher Na+ current density leading to greater spike amplitude and a more stable spike threshold, in VP neurones. VP neurones also show a greater incidence of both fast and slow Ca2+‐dependent depolarising afterpotentials, the latter of which summate to plateau potentials and contribute to phasic bursting. By contrast, OT neurones exhibit a sustained outwardly rectifying potential (SOR), as well as a consequent depolarising rebound potential, not found in VP neurones. The SOR makes OT neurones more susceptible to spontaneous inhibitory synaptic inputs and correlates with a longer period of spike frequency adaptation in these neurones. Although both types exhibit prominent Ca2+‐dependent afterhyperpolarising potentials (AHPs) that limit firing rate and contribute to bursting patterns, Ca2+‐dependent AHPs in OT neurones selectively show significant increases during pregnancy and lactation. In OT neurones, but not VP neurones, AHPs are highly dependent on the constitutive presence of the second messenger, phosphatidylinositol 4,5‐bisphosphate, which permissively gates N‐type channels that contribute the Ca2+ during spike trains that activates the AHP. By contrast to the intrinsic properties supporting phasic bursting in VP neurones, the synchronous bursting of OT neurones has only been demonstrated in vitro in cultured hypothalamic explants and is completely dependent on synaptic transmission. Additional differences in Ca2+ channel expression between the two neurosecretory terminal types suggests these channels are also critical players in the differential release of OT and VP during repetitive spiking, in addition to their importance to the potentials controlling firing patterns.

The osmoresponsiveness of oxytocin and vasopressin neurones: Mechanisms, allostasis and evolution

“…These neurones have some features that distinguish them clearly from most other hypothalamic neurones, and some features that are more commonly observed in vasopressin cells than in oxytocin cells, and vice versa, although there is considerable variation within each of these populations. 81 A few cells appear to have an ambiguous phenotype; for example, a few cells not only generate both suckling-induced milk-ejection bursts, classically identifying them as oxytocin cells, but also show phasic firing patterns that are mainly associated with vasopressin cells. Most magnocellular neurones express mRNAs for both oxytocin and vasopressin; usually, these are present at very different levels, although a small proportion (approximately 3%) express both at equivalent levels.…”

Involvement of Hyperpolarization-Activated Cyclic Nucleotide-Gated Channel 3 in Oxytocin Neuronal Activity in Lactating Rats With Pup Deprivation

“…This is because PGE 2 can evoke more than 70% of oxytocin neurons to discharge burst firing in brain slices, while oxytocin can evoke the burst in less than 30% of oxytocin neurons ( Wang et al., 2016 ). The burst firing in oxytocin neurons has been linked to a rebound firing feature of oxytocin neurons ( Armstrong et al., 2019 ). Among several known ion channels on oxytocin neurons, hyperpolarization-activated cyclic nucleotide-gated channels (HCNs) have the feature of rebound excitation and burst-evoking ability ( Qiu et al., 2005 ; Ying et al., 2011 ).…”

Expression and functions of N-type Cav2.2 and T-type Cav3.1 channels in rat vasopressin neurons under normotonic conditions

“…Electrophysiological studies on VGCC currents showed that the soma of rat supraoptic MNCs functionally express T-, N-, L-, P/Q-and R-type Ca 2+ channels [25][26][27][28][29]. However, increasing evidence has shown that there are some differences in important properties including ion channel activities and firing patterns between AVP and OXT neurons [30]. Thus, further studies have been warranted to be performed on VGCC activities in AVP neurons by distinguishing from those in OXT neurons, and vice versa.…”