Spatial orientation of the vestibular system: dependence of optokinetic after-nystagmus on gravity

Abstract

1. Monkeys received optokinetic stimulation at 60 degrees/s about their yaw (animal vertical) and pitch (animal horizontal) axes, as well as about other head-centered axes in the coronal plane. The animals were upright or tilted in right-side-down positions with regard to gravity. The stimuli induced horizontal, vertical, and oblique optokinetic nystagmus (OKN). OKN was followed by optokinetic after-nystagmus (OKAN), which was recorded in darkness. 2. When monkeys were tilted, stimulation that generated horizontal or yaw axis eye velocity during OKN induced a vertical or pitch component of slow phase velocity during OKAN. This has been designated as "cross-coupling" of OKAN. Eigenvalues and eigenvectors associated with the system generating OKAN were found as a function of tilt. They were determined by use of the Levenberg-Marquardt algorithm to minimize the mean square error between the output of a model of OKAN and the data. 3. The eigenvector associated with yaw OKAN (yaw axis eigenvector) was maintained close to the spatial vertical regardless of the angle of tilt. The eigenvector associated with pitch OKAN (pitch axis eigenvector) was always aligned with the body axis. The data indicate that velocity storage can be modeled by a piecewise linear system, the structure of which is dependent on gravity and the yaw axis eigenvector, which tends to align with gravity. 4. Yaw axis eigenvectors were also determined by giving optokinetic stimulation about head-centered axes in the coronal plane with the animal in various angles of tilt. A technique using a spectral analysis of residuals was developed to estimate whether yaw and pitch OKAN slow phase velocities decayed concurrently at the same relative rate and over the same time course. The eigenvectors determined by this method were in agreement with those obtained by analyzing OKAN elicited by yaw OKN. 5. During yaw OKN with the animal in tilted positions, the mean vector of the ensuing nystagmus was closer to the body axis than to the spatial vertical. This suggests that there is suppression of the cross-coupled pitch component during OKN. The direction of the stimulus may be utilized to suppress components of velocity storage not coincident with the direction of stimulus motion. 6. There were similarities between the monkey eigenvectors and human perception of the spatial vertical, and the mean of eigenvectors for upward and downward eye velocities overlay human 1-g perceptual data.(ABSTRACT TRUNCATED AT 400 WORDS)

Neural Processing of Gravito-Inertial Cues in Humans. IV. Influence of Visual Rotational Cues During Roll Optokinetic Stimuli

“…The axis-shift component is very small in humans during both optokinetic and canal stimulation. In addition, this axis-shift seems to be "economical" in the sense that the eye movement rotation axis always shifts toward alignment with gravity "through the smallest angle," as was suggested in our recent model of reflexive eye responses to visual-vestibular interactions and by numerous experimental investigations (Angelaki and Hess 1994;Dai et al 1991;Fetter FIG. 9.…”

“…It has been observed that the eye rotation axis of reflexive eye movements tends to shift toward alignment with gravity in response to either 1) optokinetic stimulation in humans (Furman and Koizuka 1994;Gizzi et al 1994;Wei et al 1994) and monkeys Dai et al 1991;Raphan and Cohen 1988) or 2) canal stimulation in humans (Fetter et al 1992;Furman and Koizuka 1994;Harris and Barnes 1987;Zupan et al 2000) and monkeys (Angelaki and Hess 1994;Jaggi-Schwarz et al 2000;Young 1992, 1995;Merfeld et al 1993a;Wearne et al 1999). The axis-shift component is very small in humans during both optokinetic and canal stimulation.…”

Neuronal Substrates of Motor Learning in the Velocity Storage Generated During Optokinetic Stimulation in the Squirrel Monkey

“…Second, vestibularly driven vertical eye movements require the coordination of two semicircular canal planes and four extraocular muscle pairs, compared with the single canal plane and two extraocular muscle pairs required for pure horizontal eye movements. Third, horizontal and vertical OKAN are maximal at different head orientations with respect to the gravitoinertial axis (Dai et al 1991;Raphan and Cohen 1985;Raphan and Sturm 1991). In an upright posture, horizontal OKAN is maximal and vertical OKAN is minimal (Cohen et al 2002;Raphan and Cohen 1988).…”

Differential processing of semicircular canal signals in the vestibulo- ocular reflex

“…During optokinetic stimulation, visual pathways are activated whose dependence on gravity signals has not been determined. If the gyroscopic properties of the vestibular system were limited to the "yaw axis eigenvector of the velocity storage integrator" as proposed by Raphan and colleagues, its manifestation in the oculomotor output would indeed only reflect a central representation of the spatial vertical (Dai et al, 1991). If, however, all semicircular canal signals were spatially transformed into a signal representing head motion in space, the functional ramifications of such processing would be much more intriguing.…”

“…For example, head tilts at slow velocity taking 4-6 set to complete did no longer elicit transformation of vertical or torsional postrotatory responses towards alignment with gravity (Angelaki and Hess, 1994). Such difficulties, as well as previous reports that vertical optokinetic afternystagmus does not reorient relative to gravity have been taken as arguments against the existence of inertial vestibular signals (Dai et al, 1991;Raphan et al, 1994).…”