Control of eye orientation: where does the brain's role end and the muscle's begin?

Dora E. Angelaki, Bernhard J. M. Hess
2004 European Journal of Neuroscience  
Our understanding of how the brain controls eye movements has bene®ted enormously from the comparison of neuronal activity with eye movements and the quanti®cation of these relationships with mathematical models. Although these early studies focused on horizontal and vertical eye movements, recent behavioural and modelling studies have illustrated the importance, but also the complexity, of extending previous conclusions to the problems of controlling eye and head orientation in three
more » ... (3-D). An important facet in understanding 3-D eye orientation and movement has been the discovery of mobile, soft-tissue sheaths or 'pulleys' in the orbit which might in¯uence the pulling direction of extraocular muscles. Appropriately placed pulleys could generate the eye-position-dependent tilt of the ocular rotation axes which are characteristic for eye movements which follow Listing's law. Based on such pulley models of the oculomotor plant it has recently been proposed that a simple two-dimensional (2-D) neural controller would be suf®cient to generate correct 3-D eye orientation and movement. In contrast to this apparent simpli®cation in oculomotor control, multiple behavioural observations suggest that the visuo-motor transformations, as well as the premotor circuitry for saccades, pursuit eye movements and the vestibulo-ocular re¯exes, must include a neural controller which operates in 3-D, even when considering an eye plant with pulleys. This review summarizes the most recent work and ideas on this controversy. In addition, by proposing directly testable hypotheses, we point out that, in analogy to the previously successful steps towards elucidating the neural control of horizontal eye movements, we need a quantitative characterization ®rst of motoneuron and next of premotor neuron properties in 3-D before we can succeed in gaining further insight into the neural control of 3-D motor behaviours. For ocular movements with the goal to stabilize images on the whole retina, the brain has to unambiguously specify all three degrees of freedom of the eye, which determine 3-D ocular orientation. One such example is the rotational vestibulo-ocular re¯ex (RVOR), which causes a compensatory eye rotation that is matched in angular velocity and direction to head rotation. Accordingly, not just gaze direction, which is de®ned by the horizontal and vertical components of the eye
doi:10.1111/j.1460-9568.2004.03068.x pmid:14750958 fatcat:h6byzqyvxzfrzjrnmlj2pcekee