SUMMARYSubtle random deviations from perfect symmetry in bilateral traits are suggested to signal reduced phenotypic and genetic quality of a sender, but little is known about the related receiver mechanisms for discriminating symmetrical from asymmetrical traits. Here, we investigated these mechanisms in behavioural and neurophysiological experiments in the Mediterranean field cricket, Gryllus bimaculatus. A downward frequency modulation at the end of each syllable in the calling song has been suggested to indicate morphological asymmetry in sound radiating structures between left and right forewings. Even under ideal laboratory conditions on a trackball system, female crickets only discriminated between songs of symmetrical and asymmetrical males in two-choice experiments at carrier frequencies of 4.4 kHz and a large modulation depth of 600 and 800 Hz. Under these conditions they preferred the pure-tone calling songs over the modulated (asymmetrical) alternative, whereas no preference was observed at carrier frequencies of 4.9 and 5.2 kHz. These preferences correlate well with the responses of a pair of identified auditory interneurons (AN1), known for their importance in female phonotaxis. The AN1 interneuron is tuned to an average frequency of 4.9 kHz, and the roll-off towards lower and higher frequencies determines the magnitude of responses to pure-tone and frequency-modulated calling songs. The difference in response magnitude between the two neurons appears to drive the decision of females towards the song alternatives. We discuss the relevance of song differences based on asymmetry in the morphology of song-producing structures under natural conditions.