Electrical stimulation of the lateral olfactory tract (LOT) has been shown to excite, monosynaptically, supraoptic nucleus (SON) neurons in slices of hypothalamus taken from male, virgin female or lactating rats. Only in the last of these, however, did 10 min of 10 Hz stimulation produce an increase in the incidence of Lucifer yellow dye-coupling, an indicator of electrotonic interactions. This coupling is virtually exclusively dendrodendritic. Since virgin females that have been induced to show full maternal behavior have altered dendritic morphology reminiscent of lactating animals (but different from males and untreated virgins) we investigated the effects of LOT stimulation in slices from maternally behaving virgins. Similar to the data for lactating rats, electrical stimulation of this tract, the terminals of which release excitatory amino acid transmitter, increased the incidence of dye-coupling by 112% (P less than 0.01). Also similar to lactating rats, the coupling was dendrodendritic and the increase was due entirely to increasing the number of neurons coupled to the injected neuron. No increase in coupling was seen in stimulated slices from pup-exposed control rats. We conclude that the maternal behaviors engaged in by both real mothers and induced virgins 'primes' the supraoptic neurons to increase coupling in response to olfactory system stimulation. This priming may occur via olfactory and vomeronasal stimulation during such behaviors as sniffing and anogenital licking of the pups. That coupling increased in tissue from maternally behaving virgins comparably to that from nursing mothers further suggests that SON neurons may play a role in maternal behavior independent of its well-documented role in the milk ejection reflex.