Eyes on Target: What Neurons Must do for the Vestibuloocular Reflex During Linear Motion

Abstract

Angelaki, Dora E. Eyes on target: what neurons must do for the vestibuloocular reflex during linear motion. J Neurophysiol 92: 20 -35, 2004; 10.1152/jn.00047.2004. A gaze-stabilization reflex that has been conserved throughout evolution is the rotational vestibuloocular reflex (RVOR), which keeps images stable on the entire retina during head rotation. An ethological newer reflex, the translational or linear VOR (TVOR), provides fast foveal image stabilization during linear motion. Whereas the sensorimotor processing has been extensively studied in the RVOR, much less is currently known about the neural organization of the TVOR. Here we summarize the computational problems faced by the system and the potential solutions that might be used by brain stem and cerebellar neurons participating in the VORs. First and foremost, recent experimental and theoretical evidence has shown that, contrary to popular beliefs, the sensory signals driving the TVOR arise from both the otolith organs and the semicircular canals. Additional unresolved issues include a scaling by both eye position and vergence angle as well as the temporal transformation of linear acceleration signals into eye-position commands. Behavioral differences between the RVOR and TVOR, as well as distinct differences in neuroanatomical and neurophysiological properties, raise multiple functional questions and computational issues, only some of which are readily understood. In this review, we provide a summary of what is known about the functional properties and neural substrates for this oculomotor system and outline some specific hypotheses about how sensory information is centrally processed to create motor commands for the VORs. I N T R O D U C T I O NThe world is viewed from a constantly shifting platform, where visual mechanisms function optimally only if images on the retina remain stable. This is achieved primarily by the vestibuloocular reflexes (VORs), which provide fast compensation during both translational and rotational motions. Although the rotational VOR (RVOR) is phylogenetically older and highly conserved throughout evolution, the translational VOR (TVOR) represents a relatively recent evolutionary acquisition that appears to have evolved in parallel with foveal vision, vergence eye movements, and stereopsis (Miles 1993(Miles , 1998. Its amplitude and functional properties are only well described for humans and non-human primates (Angelaki and McHenry 1999; McHenry and Angelaki 2000;Paige 1989; Paige and Tomko 1991a,b;Ramat and Zee 2003;Schwarz and Miles 1991;Schwarz et al. 1989;Telford et al. 1997;Zhou et al. 2003). In contrast, an image-stabilization system appropriate to compensate for the visual consequences of translational motion remains rudimentary or absent in lateral-eyed species (Baarsma and Collewijn 1975; Dickman and Angelaki 1999;Hess and Dieringer 1990, 1991; Hess et al. 1984; Maruta et al. 2001). The functional goal of the TVOR is to decrease conjugate retinal slip and minimize binocular disparities during either self-motion...

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