The control of consumatory behavior resides in a dialogue integrating hypothalamic and neocortical function. In starved and thirsted animals and human, cortical direct current (DC)-potential fluctuation of negative polarity has been reported during ingestion of food and liquid. In vitro/ex vivo brain slice technique was used to investigate the effect of repetitive DC fluctuations occurring during and after drinking in thirsted rats on neuronal network excitability in neocortex and hippocampus. In thirsted rats cortical DC-potential shifts of negative polarity were recorded during lapping water. Rat hippocampal and neocortical slices were incubated with the voltage-sensitive dye RH795 and neuronal activity was monitored using a fast-imaging photodiode array combined with standard field potential recordings. The mean amplitude of optical signals significantly increased in neocortex and decreased in CA1 area of hippocampus. Induction of long-term potentiation was also affected by repetitive negative DC-potential shifts. Induction of LTP significantly increased in the third layer of neocortex and decreased in CA1 area of hippocampus. Both neocortical and hippocampal slices were tested for their hypoxia tolerance. Repetitive DC-potential negativity increased the latency of anoxic terminal negativity after onset of hypoxia in hippocampus. The sequence of negative potential shifts associated with drinking indicates a coordinate regulation of cortical and subcortical excitability that may modulate consumatory behavior and its context-dependent memorization.