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The Journal of Neuroscience, April 21, 2004, 24(16):3974-3984; doi:10.1523/JNEUROSCI.3720-03.2004

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Behavioral/Systems/Cognitive
Specific Na⁺ Sensors Are Functionally Expressed in a Neuronal Population of the Median Preoptic Nucleus of the Rat

Magali Grob, Guy Drolet, and Didier Mouginot

Centre de Recherche en Neurosciences, Centre Hospitalier de l'Université Laval, Québec G1V 4G2, Canada

Whole-cell patch-clamp recordings were performed on acute brain slices of male rats to investigate the ability of the neurons of the median preoptic nucleus (MnPO) to detect fluctuation in extracellular osmolarity and sodium concentration ([Na⁺]_out). Local application of hypotonic and hypertonic artificial CSF hyperpolarized and depolarized the neurons, respectively. Similar responses obtained under synaptic isolation (0.5 µM TTX) highlighted the intrinsic ability of the MnPO neurons to detect changes in extracellular osmolarity and [Na⁺]_out. Manipulating extracellular osmolarity, [Na⁺]_out, and [Cl^-]_out showed in an independent manner that the MnPO neurons responded to a change in [Na⁺]_out exclusively. The specific Na⁺ response was voltage insensitive and depended on the driving force for Na⁺ ions, indicating that a sustained background Na⁺ permeability controlled the membrane potential of the MnPO neurons. This specific response was not reduced by Gd³⁺, amiloride, or benzamil, ruling out the participation of mechanosensitive cationic channels, specific epithelial Na⁺ channels, and Phe-Met-Arg-Phe-gated Na⁺ channels, respectively. Combination of in situ hybridization, using a riboprobe directed against the atypical Na⁺ channel (Na_X), and immunohistochemistry, using an antibody against neuron-specific nuclei protein, revealed that a substantial population of MnPO neurons expressed the Na_X channel, which was characterized recently as a concentration-sensitive Na⁺ channel. This study shows that a neuronal population of the MnPO acts as functional Na⁺ sensors and that the Na_X channel might represent the molecular basis for the extracellular sodium level sensing in these neurons.

Key words: lamina terminalis; sodium homeostasis; salt appetite; sodium sensors; hydromineral homeostasis; Na_X; sodium channel

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Received Aug 8, 2003; revised February 17, 2004; accepted February 17, 2004.

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