Short‐term plasticity impacts information transfer at glutamate synapses onto parvocellular neuroendocrine cells in the paraventricular nucleus of the hypothalamus

Abstract

Glutamatergic synaptic inputs onto parvocellular neurosecretory cells (PNCs) in the paraventricular nucleus of the hypothalamus (PVN) regulate the hypothalamic-pituitary-adrenal (HPA) axis responses to stress and undergo stress-dependent changes in their capacity to transmit information. In spite of their pivotal role in regulating PNCs, relatively little is known about the fundamental rules that govern transmission at these synapses. Furthermore, since salient information in the nervous system is often transmitted in bursts, it is also important to understand the short-term dynamics of glutamate transmission under basal conditions. To characterize these properties, we obtained whole-cell patch clamp recordings from PNCs in brain slices from postnatal day 21-35 male Sprague-Dawley rats and examined EPSCs. EPSCs were elicited by electrically stimulating glutamatergic afferents along the periventricular aspect. In response to a paired-pulse stimulation protocol, EPSCs generally displayed a robust short-term depression that recovered within 5 s. Similarly, trains of synaptic stimuli (5-50 Hz) resulted in a frequency-dependent depression until a near steady state was achieved. Application of inhibitors of AMPA receptor (AMPAR) desensitization or the low-affinity, competitive AMPAR antagonist failed to affect the depression due to paired-pulse and trains of synaptic stimulation indicating that this use-dependent short-term synaptic depression has a presynaptic locus of expression. We used cumulative amplitude profiles during trains of stimulation and variance-mean analysis to estimate synaptic parameters. Finally, we report that these properties contribute to hamper the efficiency with which high frequency synaptic inputs generate spikes in PNCs, indicating that these synapses operate as effective low-pass filters in basal conditions.