Oxytocin neurones are recruited into co-ordinated fluctuations of firing before bursting in the rat

Hypothalamic oxytocin neurones have dual physiological functions with associated characteristic activity patterns: a homeostatic osmoregulatory role involving continuous low frequency firing at a relatively constant rate, and roles associated with reproduction involving periodic, brief, synchronised, high frequency bursts of spikes. Apparently the same neurones maintain both roles during reproduction, when both activity patterns occur simultaneously, although sometimes factors linked to the homeostatic response predominate and prevent bursting. With the object of understanding how oxytocin neuronal networks manage both roles during lactation, we analysed basal activity between bursts in simultaneously recorded neurones to reveal potentially adaptive changes in network behaviour. Negative autocorrelation on a time scale of 0.5–2 s occurs in basal activity between bursts but also in non-bursting oxytocin neurones, and can therefore be associated with the system's homeostatic role. Although the system responds to the pups suckling by the induction of bursting, there are also increasing fluctuations in firing that are positively correlated in some simultaneously recorded neurones during basal activity between bursts. A few seconds before bursts, cross-correlation strengthens, irregularity of firing increases, and serial correlation (autocorrelation) weakens, all substantially. After pharmacological treatments known to facilitate bursting, cross-correlation and irregularity of firing increase and autocorrelation weakens, and the reverse occurs in conditions that delay bursting (hyperosmotic stress and pharmacological interventions). Our analyses suggest heterogeneity in the population of oxytocin neurones during lactation; the range including ‘leader neurones’ that readily display co-ordinated fluctuations in firing in response to suckling and escape from negative autocorrelation just before bursts, and ‘follower neurones’ that fire at a relatively constant rate in no apparent relationship to others, except when recruited late to bursting, probably in response to massive stimulation from already bursting neurones. The steep increases in correlation a few seconds before bursts reflect an accelerating process of recruitment of follower neurones to co-ordinated fluctuations, leading to the phase transition that constitutes the critical stage of burst generation.