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The Journal of Neuroscience, September 1, 2001, 21(17):6967-6977

Responses of Magnocellular Neurons to Osmotic Stimulation Involves Coactivation of Excitatory and Inhibitory Input: An Experimental and Theoretical Analysis

Gareth Leng¹, Colin H. Brown¹, Philip M. Bull¹, David Brown², Sinead Scullion¹, James Currie¹, Ruth E. Blackburn-Munro³, Jianfeng Feng⁴, Tatsushi Onaka⁵, Joseph G. Verbalis³, John A. Russell¹, and Mike Ludwig¹

¹ Department of Biomedical Sciences, University Medical School, Edinburgh EH8 9XD, United Kingdom, ² The Babraham Institute, Cambridge CB2 4AT, United Kingdom, ³ Department of Medicine and Physiology, Georgetown University, Washington, DC 20007, ⁴ School of Cognitive and Computing Sciences, University of Sussex, Brighton BN1 9QH, United Kingdom, and ⁵ Department of Physiology, Jichi Medical School, Minamikawachi-machi, Tochigi-ken, 329-0498, Japan

How does a neuron, challenged by an increase in synaptic input, display a response that is independent of the initial level of activity? Here we show that both oxytocin and vasopressin cells in the supraoptic nucleus of normal rats respond to intravenous infusions of hypertonic saline with gradual, linear increases in discharge rate. In hyponatremic rats, oxytocin and vasopressin cells also responded linearly to intravenous infusions of hypertonic saline but with much lower slopes. The linearity of response was surprising, given both the expected nonlinearity of neuronal behavior and the nonlinearity of the oxytocin secretory response to such infusions. We show that a simple computational model can reproduce these responses well, but only if it is assumed that hypertonic infusions coactivate excitatory and inhibitory synaptic inputs. This hypothesis was tested first by applying the GABA_A antagonist bicuculline to the dendritic zone of the supraoptic nucleus by microdialysis. During local blockade of GABA inputs, the response of oxytocin cells to hypertonic infusion was greatly enhanced. We then went on to directly measure GABA release in the supraoptic nucleus during hypertonic infusion, confirming the predicted rise. Together, the results suggest that hypertonic infusions lead to coactivation of excitatory and inhibitory inputs and that this coactivation may confer appropriate characteristics on the output behavior of oxytocin cells. The nonlinearity of oxytocin secretion that accompanies the linear increase in oxytocin cell firing rate reflects frequency-facilitation of stimulus-secretion coupling at the neurohypophysis.

Key words: supraoptic nucleus; oxytocin; hyponatremia; microdialysis; hypothalamus; modeling

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Copyright © 2001 Society for Neuroscience  0270-6474/01/21176967-11$05.00/0

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