Synaptic control of rat supraoptic neurones during osmotic stimulation of the organum vasculosum lamina terminalis in vitro.

Abstract

1. The effects of osmotic or electrical stimulation of the organum vasculosum lamina terminalis (OVLT) were examined during intracellular recordings (32°C) obtained from ninety-five supraoptic nucleus magnocellular neurosecretory cells (MNCs) in superfused explants of rat hypothalamus. 2. Brief (10-20 s) applications of hypertonic and hypotonic solutions to the area of the OVLT caused prolonged (> 1 min) increases and decreases, respectively, in electrical activity in seventy of seventy-four trials performed on neurones with membrane potentials near spike threshold (~-55 mV). Changes in firing frequency were related to changes in external osmolality in a dose-dependent manner between 275 and 355 mosmol kg-'.3. When 30 s periods recorded immediately before, and 30 s following, the application of an osmotic stimulus were examined, the frequency of spontaneous EPSPs (sEPSPs) was related in a dose-dependent manner to the osmolality of the solution superfusing the OVLT region. The increased EPSP frequency was maintained and did not adapt if the osmolality of the medium was raised for periods of > 10 min. In contrast, the frequency of spontaneous IPSPs (sIPSPs) was virtually unaffected by changes in external osmotic pressure. 4. Osmotically evoked changes in MNC firing were strongly correlated with accompanying changes in the frequency of sEPSPs (slope, 0 9; correlation coefficient (r) = 0 7), but not sIPSPs (r = 0 2), suggesting that changes in firing rate following osmotic stimulation of the OVLT are selectively mediated by changes in synaptic excitation.5. In the presence of bicuculline (5-10 /M), electrical stimulation of the OVLT evoked fast EPSPs in forty-seven of forty-eight MNCs tested. These responses were reversibly reduced by application of 20-40 /M kynurenic acid (n = 3) or 20-40 uM 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX; n = 11). Similarly, bath application of CNQX (n = 3) or kynurenic acid (n = 4) reversibly abolished the excitatory response of supraoptic neurones following hypertonic stimulation of the OVLT. 6. Brief (10-15 s) applications of y-aminobutyric acid (GABA) over the OVLT reversibly abolished increases in sEPSP frequency and action potential firing rate evoked by hyperosmotic stimulation of the OVLT. In the presence of GABA, the rates of sEPSP and sIPSP frequency were reduced to 37 + 10 and 44 + 13% (means + S.E.M.), respectively, of those observed under isotonic conditions (295 mosmol kg-1). 7. These results suggest that inhibitory and excitatory pathways originating from neurones located within the OVLT are tonically active under resting osmotic conditions in rat hypothalamic explants. Osmotically evoked changes in MNC firing, however, are selectively mediated through increases or decreases in the intensity of the excitatory component of OVLT-derived inputs.

Physiological contribution of the astrocytic environment of neurons to intersynaptic crosstalk

“…This will prevent the postsynaptic neuron from being contaminated by nonrelevant signals and will serve to increase the signal-to-noise ratio for pertinent information (8). In the SON, glutamate spillover is likely to occur during the brief (2-to 4-s) high-frequency (40-to 80-Hz) bursts of afferent glutamatergic potentials believed to mediate transmission of the suckling information (27) to oxytocin neurons as well as during the increase in glutamatergic synaptic activity induced by osmotic stimulation (28). If this were the case, the reduced astrocytic coverage of neurons characterizing the SON of lactating and dehydrated animals (13,14) would favor heterosynaptic inhibition of GABA release.…”

GABAergic Excitation of Vasopressin Neurons

“…[12][13][14][15][16][17][18] Recent work from our laboratory 19 indicated that GABA does not always function as an inhibitory neurotransmitter in this circuit. We demonstrated that, although GABA generally inhibits AVP neurons under resting conditions, it excites them under chronic hyperosmotic stress, a situation that demands increased AVP secretion.…”

Glutamatergic Inputs Contribute to Phasic Activity in Vasopressin Neurons

“…In vivo experiments unambiguously showed that glutamate receptor blockers reversibly interrupted phasic activity in VP neurons (Nissen et al, 1994(Nissen et al, , 1995Moos et al, 1997), whereas glutamatergic receptor agonists triggered (Nissen et al, 1995) or accelerated phasic activity. Glutamate was shown to be the sole source of EPSPs in coronal slices in vitro (van den Pol et al, 1990;Wuarin and Dudek, 1993;Yang et al, 1994;Richard and Bourque, 1995;Jourdain et al, 1998). In our cultures, blockade of EPSPs suppressed phasic activity even when firing was triggered and maintained with a depolarizing current indicating that glutamatergic EPSPs are required for generating rhythmic bursts.…”