During sexual pursuit, male flies Sarcophaga bullata, stabilize the image of a pursued target on the dorso-frontal acute zone of their compound eyes. By retinotopic projection, this region is represented in the upper frontal part of the lobula where it is sampled by ensembles of male-specific motion- and flicker-sensitive interneurons. Intracellular recordings of descending neurons, followed by biocytin injection, demonstrate that male-specific neurons are dye-coupled to specific descending neurons and that the response characteristics of these descending neurons closely resemble those of male-specific lobula neurons. Such descending neurons are biocytin-coupled in the thoracic ganglia, revealing their connections with ipsilateral frontal nerve motor neurons supplying muscles that move the head and with contralateral basalar muscle motor neurons that control wing beat amplitude. Recordings from neck muscle motor neurons demonstrate that although they respond to movement of panoramic motion, they also selectively respond to movement of small targets presented to the male-specific acute zone. The present results are discussed with respect to anatomical and physiological studies of sex-specific interneurons and with respect to sex-specific visual behavior. The present study, and those of the two preceding papers, provide a revision of Land and Collett's hypothetical circuit underlying target localization and motor control in males pursuing females.