Human Vestibuloocular Reflex and Its Interactions With Vision and Fixation Distance During Linear and Angular Head Movement

Abstract

Human vestibuloocular reflex and its interactions with vision and fixation distance during linear and angular head movement. J. Neurophysiol. 80: 2391-2404, 1998. The vestibuloocular reflex (VOR) maintains visual image stability by generating eye movements that compensate for both angular (AVOR) and linear (LVOR) head movements, typically in concert with visual following mechanisms. The VORs are generally modulated by the "context" in which head movements are made. Three contextual influences on VOR performance were studied during passive head translations and rotations over a range of frequencies (0.5-4 Hz) that emphasized shifting dynamics in the VORs and visual following, primarily smooth pursuit. First, the dynamic characteristics of head movements themselves ("stimulus context") influence the VORs. Both the AVOR and LVOR operate with high-pass characteristics relative to a head velocity input, although the cutoff frequency of the AVOR (<0.1 Hz) is far below that of the LVOR ( approximately 1 Hz), and both perform well at high frequencies that exceed, but complement, the capabilities of smooth pursuit. Second, the LVOR and AVOR are modulated by fixation distance, implemented with a signal related to binocular vergence angle ("fixation context"). The effect was quantified by analyzing the response during each trial as a linear relationship between LVOR sensitivity (in deg/cm), or AVOR gain, and vergence (in m-1) to yield a slope (vergence influence) and an intercept (response at 0 vergence). Fixation distance (vergence) was modulated by presenting targets at different distances. The response slope rises with increasing frequency, but much more so for the LVOR than the AVOR, and reflects a positive relationship for all but the lowest stimulus frequencies in the AVOR. A third influence is the context of real and imagined targets on the VORs ("visual context"). This was studied in two ways-when targets were either earth-fixed to allow visual enhancement of the VOR or head-fixed to permit visual suppression. The VORs were assessed by extinguishing targets for brief periods while subjects continued to "fixate" them in darkness. The influences of real and imagined targets were most robust at lower frequencies, declining as stimulus frequency increased. The effects were nearly gone at 4 Hz. These properties were equivalent for the LVOR and AVOR and imply that the influences of real and imagined targets on the VORs generally follow low-pass and pursuit-like dynamics. The influence of imagined targets accounts for roughly one-third of the influence of real targets on the VORs at 0.5 Hz.

Effect of unilateral vestibular deafferentation on the initial human vestibulo-ocular reflex to surge translation

“…Dynamics and kinematics of the LVOR have been studied in detail in monkeys (Paige 1989;Schwarz et al 1989;Paige and Tomko 1991;Schwarz and Miles 1991;Telford et al 1996;Angelaki et al 2000a;McHenry and Angelaki 2000). The human heave LVOR is strongly dependent on context, particularly the target viewed or imagined (Baloh et al 1988;Skipper and Barnes 1989;Bronstein et al 1991;Oas et al 1992;Gianna et al 1997;Telford et al 1997;Paige et al 1998), and exhibits high pass dynamics with a cutoff frequency of ~1 Hz (Paige et al 1998). The surge LVOR has been studied in monkeys for steady-state motion, and exhibited geometrically appropriate dependencies on target location (McHenry and Angelaki 2000;Paige and Tomko 1991;Seidman et al 1999).…”

Dynamic Cyclovergence during Vertical Translation in Humans

“…This is in contrast with the characteristics of the linear VOR response in foveate species, in which the amplitude of the eye movement is modulated by the object's distance (Schwarz et al, 1989;Paige et al, 1998).…”

Body position differentially influences responses to exogenous and endogenous cues

“…While one is statically positioned in the HDNF orientation, the orientation of gravity relative to the head differs drastically from that of a typical head-upright position. Because a change in body orientation relative to potential target locations (Grubb et al, 2008;Karnath et al, 1991), changes in hand position relative to potential targets (Reed, Grubb, & Steele, 2006), and dynamic body maneuvers have all been shown to modify visual attention (e.g., Paige, Telford, Seidman, & Barnes, 1998;Seidman et al, 1998), it is entirely possible that the static HDNF position could influence visual attention. The combination of visual and vestibular inputs affects the current state of the system because the atypical positioning of the vestibular apparatus causes an increased demand on the multisensory processing that occurs within the central nervous system (Grubb et al, 2008).…”