The squirrel monkey vestibulo-ocular reflex (VOR) was studied in darkness during Earth-horizontal rotation over a frequency range, 0.01-4 Hz, with the head positioned both centrally and displaced radially relative to the axis of rotation. With the head centered, the canal-mediated angular VOR (AVOR) was recorded in isolation. However, with the head placed eccentrically, otolith-mediated linear VOR (LVOR) components interact with the AVOR to yield a combined AVOR-LVOR response. The plane of the ocular response could be manipulated by placing the head in different orientations relative to gravity (i.e. upright or nose-up). When the head was upright and centered, the horizontal AVOR was recorded. Comparisons between eye and head angular velocity showed that gain (pk eye/pk head velocity) was nearly flat, averaging 0.83, across the frequency range. Phase (difference in degrees between eye and head velocity, shifted 180 degrees by convention) was near 0 degrees, except at frequencies below 0.1 Hz where phase leads were seen. When the head was displaced eccentrically and in the nose-out position (facing away from the axis of rotation), gain rose above that of the AVOR alone. The enhancement was progressive with increasing frequency, but only for frequencies above 0.25 Hz. When the subject was turned nose-in, gain declined relative to the AVOR alone, and in a similar frequency-dependent fashion. These results are consistent with the notion that nose-out and nose-in responses to eccentric rotation represent a combined influence of the horizontal AVOR and LVOR, the latter driven by inter-aural tangential acceleration. To further evaluate this possibility, eccentric rotation was also used to assess the LVOR in isolation. With the head in the nose-up orientation, the AVOR was shifted into the head's roll plane and generated torsional ocular responses. With the head centered over the axis of rotation, no systematic horizontal responses were observed. However, when the head was displaced eccentrically and placed in the head-out and head-in positions, horizontal ocular responses were recorded which were proportional to head eccentricity and were of appropriate polarity to presume that they represented the inter-aural LVOR activated by inter-aural tangential acceleration. Response gain rose with increasing frequency, as did tangential acceleration. The LVOR in its resting state in darkness could be characterized by an average sensitivity of 40.3 degrees/s/g (g = 9.81 m/s2).(ABSTRACT TRUNCATED AT 400 WORDS)