Phasic spike patterning in rat supraoptic neurones in vivo and in vitro

Abstract

In vivo, most vasopressin cells of the hypothalamic supraoptic nucleus fire action potentials in a 'phasic' pattern when the systemic osmotic pressure is elevated, while most oxytocin cells fire continuously. The phasic firing pattern is believed to arise as a consequence of intrinsic activity-dependent changes in membrane potential, and these have been extensively studied in vitro. Here we analysed the discharge patterning of supraoptic nucleus neurones in vivo, to infer the characteristics of the post-spike sequence of hyperpolarization and depolarization from the observed spike patterning. We then compared patterning in phasic cells in vivo and in vitro, and we found systematic differences in the interspike interval distributions, and in other statistical parameters that characterized activity patterns within bursts. Analysis of hazard functions (probability of spike initiation as a function of time since the preceding spike) revealed that phasic firing in vitro appears consistent with a regenerative process arising from a relatively slow, late depolarizing afterpotential that approaches or exceeds spike threshold. By contrast, in vivo activity appears to be dominated by stochastic rather than deterministic mechanisms, and appears consistent with a relatively early and fast depolarizing afterpotential that modulates the probability that random synaptic input exceeds spike threshold. Despite superficial similarities in the phasic firing patterns observed in vivo and in vitro, there are thus fundamental differences in the underlying mechanisms.

Glutamatergic Inputs Contribute to Phasic Activity in Vasopressin Neurons

“…In contrast, VP neurons in acute slices displayed longer bursts (75 s) and silent periods (49 s). This has also been noted in previous studies of VP activity in acute slices [BD, 41 s; SD, 35 s in the study by Sabatier et al (2004)] and in explants [BD, 47 s; SD, 44 s in the study by Ghamari-Langroudi and Bourque (2000)]. Thus, the phasic activity of VP neurons in organotypic slice cultures appears more similar to that observed in vivo than in acute slices.…”

“…As has been suggested by several groups (Andrew and Dudek, 1984;Sabatier et al, 2004), synaptic activity may be an alternative process to generate phasic activity. Detailed analysis of the recordings obtained from cells in the organotypic slice cultures revealed that bursts were often preceded by an increased EPSP activity, which summated to form a plateau-like potential (Fig.…”

“…In acute slices of adult tissue, what remains is essentially miniature postsynaptic activity. Sabatier et al (2004) proposed that the amplitude of DAPs, and thus their impact on phasic activity, is likely to be larger in acute slices than in vivo. It should be noted that in explants (Armstrong et al, 1994) and in acute slices (J.-M. Israel, unpublished results), not only do VP and OT neurons share basic intrinsic properties, but they both can display DAPs as well as phasic firing.…”

Expression of the long form of the prolactin receptor in magnocellular oxytocin neurons is associated with specific prolactin regulation of oxytocin neurons

“…Collision of antidromic action potentials triggered by spontaneous orthodromic action potentials was subsequently used to confirm identification. Oxytocin neurons were distinguished from vasopressin neurons by their continuous firing pattern and by a transient excitation in response to CCK (20 g/kg iv) (57) After a period of stable basal recording, prolactin (L6520, Sigma) dissolved in artificial cerebrospinal fluid (pH 7.2, 138 mM NaCl, 3.36 mM KCl, 9.52 mM NaHCO 3, 0.49 mM Na2HPO4, 1.26 mM CaCl2, 1.18 mM MgCl2 and 2.16 mM urea) was administered via the intracerebroventricular cannula (1-10 g in a volume of 2.5 l). For quantitative analysis, all comparisons were made at the lowest doses of prolactin used (1 g per injection).…”

Population Dynamics in Vasopressin Cells

“…Under the same baseline osmotic conditions, vasopressin cells display one of several activity patterns: silence, irregular spike discharge, phasic spike discharge and continuous spike discharge [19, 20]. Silent neurons presumably secrete little or no hormone, and the peripheral secretion from neurons that discharge spikes slowly and irregularly will be relatively low.…”