The responses of single units in the brainstem of the decerebrate, paralysed, pigeon were studied. Natural vestibular stimulation was provided by horizontal, sinusoidal, oscillation of the bird and extraocular muscle afferents of the ipsilateral eye were activated by passive eye-movement. Unit responses to vestibular and/or orbital stimuli were examined in sets of peristimulus time histograms interleaved in time. Of 352 units in the brainstem, in the region of the vestibular nuclei, which were exposed to the effects of both vestibular stimuli and passive eye-movement, 40 (11%) responded only to the latter; the other 312 units (89%) responded to vestibular stimulation at 0.4 Hz (amplitude +/- 8 degrees). Of these 312 units, 129 (41%) were affected only by vestibular stimuli; in the other 183 units (59%) passive eye-movement produced clear modification of the vestibular responses by adding excitation or inhibition, or both. There were phasic modifications in most units; in 77 there were longer-lasting changes in the vestibular responses, often following a phasic response. In 124 units whose responses were subjected to statistical analysis, the vestibular responses of 42 (34%) were modified only by horizontal eye-movement and eight (6%) were affected only by vertical movement. A further 18% showed larger effects from horizontal than from vertical eye-movement; in 2% vertical eye-movement was preferred. Further examination of the specificity of the effects of eye-movement in planes between the vertical and horizontal was possible in 29 units which showed various degrees of "tuning" of the effect. In some units there was additional specificity for eye-movement in (a) particular directions (towards the beak rather than towards the tail, for example); (b) in particular arcs of the orbit (centre-to-temporal rather than nasal-to-centre, for example). Note that all these effects were upon the responses of the units to horizontal vestibular stimulation. Thus, the modifications of the vestibular responses depended upon specific characteristics of the passive eye-movement. The exact recording sites of 29 units were determined histologically; some were in the medial vestibular nucleus but many were in the adjacent reticular formation. The principal interest of the results is that they provide more detailed information than was available previously on the specificity of the effects of afferent signals from the extraocular muscles upon the vestibular responses of units in regions of the brainstem known to be involved in oculomotor control. The decerebrate pigeon proves to be a particularly good preparation in which to study these effects.(ABSTRACT TRUNCATED AT 400 WORDS)