The recognition of the male calling song is essential for phonotaxis in female crickets. We investigated the responses toward different models of song patterns by ascending, local, and descending neurons in the brain of standing and walking crickets. We describe results for two ascending, three local, and two descending interneurons. Characteristic dendritic and axonal arborizations of the local and descending neurons indicate a flow of auditory information from the ascending interneurons toward the lateral accessory lobes and point toward the relevance of this brain region for cricket phonotaxis. Two aspects of auditory processing were studied: the tuning of interneuron activity to pulse repetition rate and the precision of pattern copying. Whereas ascending neurons exhibited weak, low-pass properties, local neurons showed both low- and band-pass properties, and descending neurons represented clear band-pass filters. Accurate copying of single pulses was found at all three levels of the auditory pathway. Animals were walking on a trackball, which allowed an assessment of the effect that walking has on auditory processing. During walking, all neurons were additionally activated, and in most neurons, the spike rate was correlated to walking velocity. The number of spikes elicited by a chirp increased with walking only in ascending neurons, whereas the peak instantaneous spike rate of the auditory responses increased on all levels of the processing pathway. Extra spiking activity resulted in a somewhat degraded copying of the pulse pattern in most neurons.