Synchronized Clusters of Action Potentials can Increase or Decrease the Excitability of the Axons of Magnocellular Hypothalamic Neurosecretory Cells

Abstract

Extracellular recordings were made from supraoptic nucleus (SON) cells in urethane anaesthetized male rats in vivo. Two stimulating electrodes were positioned to activate the cells antidromically, one in the mid axon region of the cells and the other at the axon terminals. Trains of 5-20 just-subthreshold stimuli at 5 s intervals decreased the threshold for antidromic activation from both sites. Whereas neither single stimuli, nor the stimuli at the beginning of a train of 20 stimuli evoked antidromic action potentials, later action potentials did so. Paradoxically, trains of 20 just-suprathreshold stimuli increased the threshold for activation of both axons and terminals. In recordings from the same cells, stimuli were applied singly at 5 s intervals at an intensity which almost invariably evoked an antidromic action potential. Identical stimuli were then applied in trains of 20 stimuli at 50 Hz. After the first train, the initial stimulus pulses of the trains frequently fell below threshold. Following a conditioning train of five stimuli applied to one electrode, the period of decreased threshold (increased excitability) at the other electrode lasted less than 100 ms and the period of increased threshold (decreased excitability) after 12 trains of 20 stimuli lasted between 5 and 10 s. Both decreased and increased excitability were seen at axons and terminals of both putative oxytocin and vasopressin cells. Since the excitability changes were shown in vivo at frequencies encountered during recordings, it is likely that they influence the probability of spike propagation and hormone secretion under physiological conditions.

Rhythmic changes in spike coding in the rat suprachiasmatic nucleus

“…It is not possible to measure transmitter release from the cells we recorded, but in the supraoptic nucleus the magnocellular neurones show greater efficiency in neuropeptide release for a given number of spikes with more patterned motifs of activity (Dutton & Dyball, 1979). It has also been known for some time that a brief series of short intervals can influence the excitability of some hypothalamic cells (Dyball & McKenzie, 2000) and we have recently shown that similar effects occur in cells of the suprachiasmatic nucleus (Dyball & Inyushkin, 2005).…”

A Predictive, Quantitative Model of Spiking Activity and Stimulus-Secretion Coupling in Oxytocin Neurons

“…The terminals do not contain clearly separate pools of readily releasable and reserve vesicles, but rather a heterogeneous population differing in releasability ( 50 ). Other mechanisms also affect stimulus-secretion coupling, including changes in axonal excitability that result from activity-dependent changes in extracellular potassium concentration ( 51 , 52 ). In this study, our purpose was not to construct a detailed model of all of the mechanisms that contribute to stimulus-secretion coupling, but rather to produce a minimalist model that by matching available data on stimulus-secretion coupling would enable us to predict secretion from spiking activity ( 31 , 52–54 ).…”

Daily Rhythms of Spike Coding in the Rat Supraoptic Nucleus

“…It is clear that the intervals between spikes and the variability and patterning of the inter‐spike interval sequence can profoundly affect the excitability of the axons of the neurosecretory cells (35, 36). The precise relationship between the information contained within a spike train and neurosecretory function, however, has not yet been established.…”