In insects, head movements are mediated by neck muscles supplied by nerves originating in the brain and prothoracic ganglion. Extracellular recordings of the nerves demonstrate units that respond to visual stimulation of the compound eyes and to mechanosensory stimulation of the halteres. The number of neck muscles required for optokinetic eye movements in flies is not known, although in other taxa, eye movements can involve as few as three pairs of muscles. This study investigates which neck motor neurons are likely to be involved in head movements by examining the relationships between neck muscle motor neurons and the terminals visiting them from approximately 50 pairs of descending neurons. Many of these descending neurons have dendrites in neuropils that are associated with modalities other than vision, and recording show that visual stimuli activate only a few neck motor neurons, such as the sclerite depressor neurons, which respond to local or wide-field, directionally specific motion, as do a subset of descending neurons coupled to them. The results suggest that, like in the vertebrate eye or the retinas of jumping spiders, optokinetic head movements of flies require only a few muscles. In addition to the importance of visual inputs, a major supply to neck muscle centers by nonvisual descending neurons suggests a role for tactile, gustatory, and olfactory signals in controlling head position.