ABSTRACT Head movement in the locust Schistocerca gregaria is mediated by 14 pairs of muscles. The normal motor output to many of these muscles has been investigated in the intact insect by recording with two intracellular microelectrodes from different fibres of a muscle during slow and fast phases of optokinetic nystagmus elicited by rotation of a striped drum in the visual field. In addition, details of the innervation pattern and muscle fibre spectrum of the muscles have been investigated by paired intracellular recording during graded stimulation of the motor nerves in the dissected preparation. Of more than 60 different axons shown histologically to innervate the neck muscles on each side, the activity of about 25 have been analysed and deductions are made about the way the muscles work together in concert to produce head movement. At least four physiologically distinct types of axon innervate several muscles. These types are tonic (slow), phaso-tonic (intermediate), phasic (fast) and inhibitory. Stationary head positions are maintained by low levels of motor output in the tonic axons alone, these axons also being mainly responsible, when active at higher frequency, for producing small slow head movements. Phaso-tonic axons become progressively more active during larger or faster head movements to augment the effect of tonic axon activity. The fastest head movements are correlated especially with activity of the phasic axons. Inhibitory neurones are active during and immediately before rapid head movements, the output to individual muscles being correlated with both contraction and relaxation. On the basis of their electrical responsiveness to the axons innervating them, muscle fibres have been classified into the following types: ‘phasic’, ‘intermediate’ and ‘tonic’, with the tonic class subdivided into ‘ordinary tonic’, ‘super-tonic’ and ‘super-sensitive’. Some muscles contain only a small range of fibre types, while others contain the complete range. Deductions are made about the way the different axon types interact on the different muscle fibre types to elicit various degrees of contraction or tension. The slow phase motor output patterns are the result of a centrally determined programme elicited by visual input (rotation of the striped drum), and are not dependent on, but may perhaps be modified by, proprioceptive feedback. On the other hand, the fast phase of nystagmus is initiated by the central nervous system only after reference to the proprioceptive input from various sense organs of the neck and prothorax.