Differences in spike train variability in rat vasopressin and oxytocin neurons and their relationship to synaptic activity

Abstract

The firing pattern of magnocellular neurosecretory neurons is intimately related to hormone release, but the relative contribution of synaptic versus intrinsic factors to the temporal dispersion of spikes is unknown. In the present study, we examined the firing patterns of vasopressin (VP) and oxytocin (OT) supraoptic neurons in coronal slices from virgin female rats, with and without blockade of inhibitory and excitatory synaptic currents. Inhibitory postsynaptic currents (IPSCs) were twice as prevalent as their excitatory counterparts (EPSCs), and both were more prevalent in OT compared with VP neurons. Oxytocin neurons fired more slowly and irregularly than VP neurons near threshold. Blockade of Cl − currents (including tonic and synaptic currents) with picrotoxin reduced interspike interval (ISI) variability of continuously firing OT and VP neurons without altering input resistance or firing rate. Blockade of EPSCs did not affect firing pattern. Phasic bursting neurons (putative VP neurons) were inconsistently affected by broad synaptic blockade, suggesting that intrinsic factors may dominate the ISI distribution during this mode in the slice. Specific blockade of synaptic IPSCs with gabazine also reduced ISI variability, but only in OT neurons. In all cases, the effect of inhibitory blockade on firing pattern was independent of any consistent change in input resistance or firing rate. Since the great majority of IPSCs are randomly distributed, miniature events (mIPSCs) in the coronal slice, these findings imply that even mIPSCs can impart irregularity to the firing pattern of OT neurons in particular, and could be important in regulating spike patterning in vivo. For example, the increased firing variability that precedes bursting in OT neurons during lactation could be related to significant changes in synaptic activity.

Dynamics of firing patterns, synchronization and resonances in neuronal electrical activities: experiments and analysis

“…For example, Magnocellular neurosecretory cells (MNCs) in the supraoptic nucleus (SON) and paraventricular nucleus (PVN) were specialized to synthesize the neurohormones vasopressin (VP) and oxytocin (OT) [63]. SON neurons exhibited various firing patterns such as continuous firing, irregular firing and bursting firing.…”

Glia-Dependent Switch of Kainate Receptor Presynaptic Action

“…The mean amplitude and frequency of mIPSCs varied a lot from one cell to another (from 0.25 to 6.51 Hz and from 115 to 338 pA, respectively). Part of this variability was due to differences between OT and VP neurons as previously reported (Li et al, 2007) as well as differences associated with the physiological state of the animals (Brussaard et al, 1999).…”

New determinants of firing rates and patterns of vasopressinergic magnocellular neurons: predictions using a mathematical model of osmodetection

“…Reported amplitudes of synaptic events show a strong heterogeneity among studies (2 to 20 mV) (Inenaga et al 1997;Li et al 2007;Shibuya et al 1998;Wuarin and Dudek 1993;Boehmer et al 2000;Richard and Bourque 1995). These variations in EPSP amplitude could result from an asynchronous barrage of many small excitatory quanta triggered by electrical stimulation of excitatory fibers (Iremonger and Bains 2007).…”

“…The frequency of IPSPs implemented in the present MCN model is 4 Hz (Richard and Bourque 1995;Li et al 2007) under normal CSF osmolality (295 mosmol/L). In the present model, the IPSP frequency is fixed and does not depend on changes in osmolality (Richard and Bourque 1995).…”