Experiments were carried out on the in vitro preparation of the lamprey brainstem isolated together with the labyrinths. The brain orientation in space could be changed in steps of 45 degrees by rotation (360 degrees) around the longitudinal axis (roll) or the transverse axis (pitch). Vestibular afferents in the VIII nerve, or reticulospinal (RS) neurons, were recorded extracellularly during roll and pitch. Two main types of afferents could be distinguished. Presumed otolith afferents responded both to a change of position and to a maintained new position. These afferents were classified in several groups according to the position of their zone of sensitivity. For roll, the largest group had their maximal sensitivity around 90 degrees tilt to the ipsilateral side, the next group in size responded at 180 degrees, and only a few afferents were activated by contralateral roll. For pitch, there are groups responding with maximal sensitivity at 90 degrees nose-up, 90 degrees nose-down and at 180 degrees. A minority of afferents were active when the brainstem was in a normal position, i.e. horizontal, with the dorsal side up. Another type of afferent responded only by a high-frequency burst to a change of brain orientation. They were classified as canal afferents in analogy with other species. All tested canal afferents responded to rotation towards ipsi-side down. Pitch tilt revealed two groups that responded to rotation towards either nose-up or nose-down. RS neurons from the anterior and middle rhombencephalic nuclei (ARRN and MRRN) were recorded before and after unilateral transection of the VIII nerve.(ABSTRACT TRUNCATED AT 250 WORDS)