Abstract
Extracellular osmolality plays a crucial role in controlling the activation of neurons. Hypertonic stimulation modulates glutamatergic inputs to the supraoptic nucleus (SON) magnocellular neurosecretory cells (MNCs) putative vasopressin (VP) neurons through capsaicin-insensitive transient receptor potential vanilloid (TRPV) 1 channels on the presynaptic terminals. However, it remains unclear whether osmotic stimulation modulates GABAergic inputs to VP-secreting neurons within punched-out slices containing only the SON and the perinuclear zone.To answer this question, we studied the effects of various osmotic conditions on the miniature GABAergic postsynaptic currents (mGPSCs) using the whole-cell patch-clamp technique on rat SON putative VP-secreting neurons in small slice preparations.We revealed that incubation in hypertonic solution for 2 h reduced both the frequency and amplitude of the mGPSCs to the SON putative VP neurons, whereas the mGPSCs were unaffected when the external osmolality was changed from isotonic to hypotonic. Of interest, we found that changing from a hypertonic to hypotonic environment increased the frequency of the mGPSCs. This effect was independent of TRPV4.We hypothesize that two coordinated mechanisms may play an important role in the regulation of a wide range of physiological functions of VP.: 1) the modulation of GABAA receptor properties by brain-derived neurotrophic factor (BDNF)-induced tyrosine kinase B receptor-mediated signaling under hypertonic conditions, and 2) cell swelling-induced activation of whole-cell anion currents under hypotonic conditions.
Highlights
Magnocellular neurosecretory cells (MNCs) in the supraoptic nucleus (SON) synthesize and secrete arginine vasopressin (VP) and oxytocin (OT)
We have revealed that short-term (5 min) hypertonic stimulation affected neither the frequency nor the amplitude of the miniature GABAergic postsynaptic currents (mGPSCs) in rat SON slice preparation which is the same-size sample we used in the present study (Yokoyama et al, 2010)
Hypotonic stimulation rapidly increased the frequency of the mGPSCs in an osmolality-dependent manner, where lower osmolality was associated with a larger increase in mGPSC frequency relative to baseline (Fig. 2)
Summary
Magnocellular neurosecretory cells (MNCs) in the supraoptic nucleus (SON) synthesize and secrete arginine vasopressin (VP) and oxytocin (OT). Fast synaptic inputs (from glutamate and GABAA receptors, respectively) are two of the most important regulators of MNC electrical activity (Leng et al, 1999; Shibuya et al, 2000). Remains unclear whether osmotic stimulation affects miniature GABAergic postsynaptic currents (mGPSCs) to the SON VP neurons through osmosensors such as TRPV on the presynaptic terminal and/or on the postsynaptic cell membrane, which lead increase of intracellular Ca2+ (Balena et al, 2010). The specific biologic mechanisms of this effect remain unclear, prior evidence has suggested that hypertonic-induced brain-derived neurotrophic factor (BDNF) release and hypo-osmotic cell swelling-induced activation of whole-cell anion currents may be involved in this process
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