Vestibular, optokinetic, and cognitive contribution to the guidance of passive self-rotation toward instructed targets.
We ask how vestibular and optokinetic information is combined ("fused") when human subjects who are being passively rotated while viewing a stationary optokinetic pattern try to tell when they have reached a previously instructed angular displacement ("targeting task"). Inevitably such a task entices subjects to also draw on cognitive mechanisms such as past experience and contextual expectations. Specifically, because we used rotations of constant angular velocity, we suspected that they would resort, consciously or unconsciously, to extrapolation strategies even though they had no explicit knowledge of this fact. To study these issues, we presented the following six conditions to subjects standing on a rotatable platform inside an optokinetic drum: V, pure vestibular (passive rotation in darkness); O, pure optokinetic (observer motionless, drum rotating); VO, combined (passive rotation while viewing stationary drum); Oe, optokinetic extrapolation (similar to O, but drum visible only during first 90 degrees of rotation; thereafter subjects extrapolate the further course in their minds); VOe, combined extrapolation (similar to VO, but drum visible only during first 90 degrees ); AI, auditory imagination (rotation presented only metaphorically; observers imagine a drum rotation using the rising pitch of a tone as cue). In all conditions, angular velocities ( v(C)) of 15, 30, or 60 degrees /s were used (randomized presentation), and observers were to indicate when angular displacement (of the self in space or relative to the drum) had reached the instructed magnitude ("desired displacement", D(D); range 90-900 degrees ). Performance was analyzed in terms of the targeting gain ( G(T) = physical displacement at time of subjects' indication / D(D)) and variability (% E(R) = percentage absolute deviation from a subject's mean gain). In all six conditions, the global mean of G(T) (across v(C) and D(D)) was remarkably close to veracity, ranging from 0.95 (V) to 1.06 (O). A more detailed analysis of the gain revealed a trend of G(T) to be larger with fast than with slow rotations, reflecting an underestimation of fast and an overestimation of slow rotation. This effect varied significantly between conditions: it was smallest in VO, had intermediate values with the monomodal conditions V and O, and also with VOe, and was largest in Oe and AI. Variability was similar for all velocities, but depended significantly on the condition: it was smallest in VO, of intermediate magnitude in O, VOe, Oe, and largest in V and AI. Additional experiments with conditions V, O, and VO in which subjects repetitively indicated displacement increments of 90 degrees, up to a subjective displacement of 1080 degrees, yielded similar results and suggest, in addition, that the displacement perceptions measured at the beginning and during later phases of the rotation are correlated. With respect to the displacement perception during optokinetic stimulation, they also show that the gain and its variability are similar whether subjects feel stationary and see a rotating pattern, or feel rotated and see a stationary pattern (circular vection). We conclude that the vestibular and optokinetic information guiding the subjects' navigation toward an instructed target is not fused by straightforward averaging. Rather the subjects' internal velocity representation (which ultimately determines G(T)) appears to be a weighted average of (1) whatever sensory information is available and of (2) a cognitive default value reflecting the subjects' experiences and expectations. The less secure the sensory information (only one source as in V or O, additional degrading as in Oe or AI), the larger the weight of the default value. Vice versa, the better the information (e.g., two independent sources as in VO), the more the actual velocity and not the default value determines displacement perception. Moreover, we suggest that subjects intuitively proceeded from the notion of a constant velocity rotation, and therefore tended to carry on the perception built up during the beghe perception built up during the beginning of a rotation or, in the case of vestibular navigation, to compensate for the decaying vestibular cue by means of an internal recovery mechanism.
Jürgens
Reinhart
R
Sektion Neurophysiologie, Universität Ulm, Albert-Einstein-Allee 47, 89081, Ulm, Germany.
Nasios
Grigorios
G
Becker
Wolfgang
W
D000328:Adult; D000704:Analysis of Variance; D003071:Cognition / Q000502:physiology*; D005260:Female; D006801:Humans; D008297:Male; D017120:Nystagmus, Optokinetic / Q000502:physiology*; D011597:Psychomotor Performance / Q000502:physiology*; D012027:Reflex, Vestibulo-Ocular / Q000502:physiology*; D012399:Rotation