Visual perception of axes of head rotation

Abstract

Registration of ego-motion is important to accurately navigate through space. Movements of the head and eye relative to space are registered through the vestibular system and optical flow, respectively. Here, we address three questions concerning the visual registration of self-rotation. (1) Eye-in-head movements provide a link between the motion signals received by sensors in the moving eye and sensors in the moving head. How are these signals combined into an ego-rotation percept? We combined optic flow of simulated forward and rotational motion of the eye with different levels of eye-in-head rotation for a stationary head. We dissociated simulated gaze rotation and head rotation by different levels of eye-in-head pursuit. We found that perceived rotation matches simulated head- not gaze-rotation. This rejects a model for perceived self-rotation that relies on the rotation of the gaze line. Rather, eye-in-head signals serve to transform the optic flow's rotation information, that specifies rotation of the scene relative to the eye, into a rotation relative to the head. This suggests that transformed visual self-rotation signals may combine with vestibular signals. (2) Do transformed visual self-rotation signals reflect the arrangement of the semi-circular canals (SCC)? Previously, we found sub-regions within MST and V6+ that respond to the speed of the simulated head rotation. Here, we re-analyzed those Blood oxygenated level-dependent (BOLD) signals for the presence of a spatial dissociation related to the axes of visually simulated head rotation, such as have been found in sub-cortical regions of various animals. Contrary, we found a rather uniform BOLD response to simulated rotation along the three SCC axes. (3) We investigated if subject's sensitivity to the direction of the head rotation axis shows SCC axes specifcity. We found that sensitivity to head rotation is rather uniformly distributed, suggesting that in human cortex, visuo-vestibular integration is not arranged into the SCC frame.

Dissociation of retinal and headcentric disparity signals in dorsal human cortex

“…Our observation bolsters an earlier observation (Arnoldussen et al, 2013b ) that perceived self-rotation depends on the rotational flow relative to the head and not relative to the gaze line. That study and the present indicate that the visual flow relative to the head is paramount to the self-motion percept.…”

“…Thus, the strong modulation of optic flow responses by H suggests an important contribution of V3A/V6 to process the speed of the head's movement in depth. This lines up nicely with a previous study concluding that V6 combines retinal rotational motion and eye pursuit signals to indicate the speed of rotation of the head in space rather than rotation speed of the gaze line (Arnoldussen et al, 2011 , 2013b ).…”

“…The visual system, extended with eye movement signals, appears to gather information about the rotation and translation of the head relative to the scene. This shift from visual retinal flow to headcentric flow was proposed before (Beintema and Van den Berg, 1998 ; Arnoldussen et al, 2013b ) as a step to align visual information on self-motion with the information from the vestibular system, which reports the head's motion relative to the world.…”

Learning to integrate contradictory multisensory self-motion cue pairings

“…To our knowledge, there exists no anatomical or functional evidence for a facilitated integration of pitch with yaw versus roll with yaw stimuli. Neither at the level of the vestibular nuclei (Büttner-Ennever, 1992;Highstein & Holstein, 2006;Naito, Newman, Lee, Beykirch, & Honrubia, 1995) nor in the cortex (Arnoldussen, Goossens, & van den Berg, 2013) can the pattern of projections from the semicircular canals account for our findings. Although recordings of neural responses to vertical rotations reveal that roll neurons outnumber pitch neurons in the brain stem (Baker, Goldberg, Hermann, & Peterson, 1984;Bolton et al, 1992;Endo, Thomson, Wilson, Yamaguchi, & Yates, 1995;Kasper, Schor, & Wilson, 1988;Wilson, Yamagata, Yates, Schor, & Nonaka, 1990), optimal activations of cortical vestibular neurons are uniformly distributed over all possible rotation planes (Akbarian et al, 1988;Grüsser, Pause, & Schreiter, 1990).…”

Investigating Head Movements Induced by ‘Riloid’ Patterns in Migraine and Control Groups Using a Virtual Reality Display

“…Alternatively, there are potential neurological mechanisms for differences in motion processing in migraine -there is increased cortical thickness in areas MT+ and V3A in those with migraine compared to controls (Granziera et al, 2006). These areas are both strongly associated with motion processing, and also with the processing of head movements (Goosens et al, 2006;Arnoldussen et al, 2011;Fisher et al, 2012;Arnoldussen et al, 2013). Imaizumi et al, (2015) used a stabilometer to show that that postural sway is greater in migraine sufferers with eyes closed, compared to eyes open: this is increased on viewing the "rotating snakes illusion", which elicits strong illusory motion in the observer.…”