In young virgin Acheta domesticus females, the spiking response of the prothoracic L3 auditory interneuron discriminates between calling songs (CSs) with phonotactically attractive and unattractive syllable periods (SPs), which parallels phonotactic discrimination. Presentation of a CS with an originally attractive SP, but with the intensity modulated so as to minimize L3's selective response, results in a CS with little phonotactic attractiveness. Conversely, a CS with an originally unattractive SP becomes much more attractive when the CS is intensity modulated in ways that duplicate L3's selective response. L3's discriminatory response to CS SP deteriorates with age, in parallel with decreased phonotactic selectiveness (females, older than 14 days, typically are unselective for CS SPs). SP-selective processing, which was not apparent in these old L3s, is immediately restored by removing the contralateral ear. SP-specific information is resident in a network of neurons within the prothoracic ganglion that results in the SP selective responses of the L3 neuron in young females. Changes in the SP-selective responses of the L3 neuron are highly correlated with corresponding changes in the female's phonotactically selective behavior.