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Central clock excites vasopressin neurons by waking osmosensory afferents during late sleep

Abstract

Osmoregulated vasopressin release is facilitated during the late sleep period (LSP) to prevent dehydration and enuresis. Previous work has shown that clock neurons in the suprachiasmatic nucleus (SCN) have low firing rates during the LSP, but it is not known how this reduced activity enhances vasopressin release. We found that synaptic excitation of rat supraoptic nucleus neurons by osmosensory afferents is facilitated during the LSP. Stimulation of the SCN at this time inhibited excitatory synaptic currents induced in supraoptic neurons by activation of osmosensory afferents. This effect was associated with an increased rate of synaptic failures and occurred without changes in frequency facilitation, quantal size or in the ratio of postsynaptic responses mediated by AMPA and NMDA receptors. We conclude that clock neurons mediate an activity-dependent presynaptic silencing of osmosensory afferent synapses onto vasopressin neurons and that osmoregulatory gain is enhanced by removal of this effect during late sleep.

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Figure 1: Increased osmoregulatory gain during LSP.
Figure 2: Firing rate of SCN neurons during the MSP and LSP in angled horizontal slices of rat hypothalamus.
Figure 3: Electrical stimulation of SCN inhibits OVLT-MNC synapses.
Figure 4: Excitation of SCN neurons inhibits OVLT-MNC synapses.
Figure 5: Excitation of SCN neurons inhibits activation of MNCs by osmotic stimulation of OVLT.
Figure 6: SCN activation inhibits OVLT-MNC synapses at a presynaptic locus.
Figure 7: Effects of SCN stimulation on synaptic failures and frequency facilitation.
Figure 8: SCN neurons modulate sEPSC frequency in MNCs.

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Acknowledgements

The authors thank K.K. Murai and W.T. Farmer (McGill University) for help with the anterograde experiments (Supplementary Fig. 2) and M. Henry and D. Mouginot (Laval University) for help with the retrograde labeling experiments (Supplementary Fig. 3). This work was supported by operating grant MOP-9939 from the Canadian Institutes of Health Research and a James McGill Chair to C.W.B. E.T. was a recipient of a Doctoral Studentship from the Heart and Stroke Foundation of Canada. The Research Institute of the McGill University Health Centre is supported by the Fonds de la Recherche en Santé du Québec.

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All of the electrophysiological experiments, technical development and data analysis were performed by E.T. C.W.B. designed the experiments and wrote the paper in close consultation with E.T.

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Correspondence to Charles W Bourque.

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Trudel, E., Bourque, C. Central clock excites vasopressin neurons by waking osmosensory afferents during late sleep. Nat Neurosci 13, 467–474 (2010). https://doi.org/10.1038/nn.2503

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