Neuroscientists speak of regions of interest with regard to brain imaging and mirroring that, in our tour of the new edition of Principles of Neural Science, we have been referring to chapters of interest. The next stop on our tour, in the Section on Movement, is chapter 35 titled The Control of Gaze, replete with its networks of excitations and inhibitions (shades of Beach Boys’ Good Vibrations).
This is one of those chapters in which much of the information will be old hat to you, but the way in which its co- authors Goldberg and Walker put it together, provides renewed appreciation of the information. They note that, to a good approximation, the eye is a sphere that sits in a socket, the orbit. Eye movements are simply rotations of the eye in the orbit. At all times, the eye’s orientation can be defined by three axes of rotation – horizontal, vertical, and torsional. We have previously pointed out, but it bears repeating, that the eyes are specialized joints adapted for sight. Bear in mind the kinematics of the eyeballs with regard to pulley systems, ligaments, tendons, collagen, and fatty tissue impacting movement in any ball and socket joint space.
Each eye muscle has a dual insertion. The part of the muscle farthest from the eye inserts on a soft tissue pulley through which the rest of the muscle passes on its way to the eyeball. When the extraocular muscles contract, they not only rotate the eyes but also change their pulling directions as a results of these pulleys.
For eye movements to be made, location signals are transformed into signals for the eye muscles to execute the desired velocity and change in eye position. The motor signals for eye movements must include both a position component to counter elastic forces and a velocity component to overcome orbital viscosity.
Consider a simplistic graphic of the motor circuit in moving the eyes rightward:
Regarding the eye velocity component, long-lead burst neurons relay signals from higher centers to excitatory burst neurons in the paramedian pontine reticular formation that synapse on motor neurons and interneurons in the abducens nucleus. Motor neurons project to the ipsilateral lateral rectus while interneurons projects to the contralateral media rectus by axons that cross the midline and ascend in the medial longitudinal fasciculus. The integrity of this neurology plays an important role in how the patient handles crossing the midline.
The eye position component arises from a neural integrator comprising neurons distributed throughout the medial vestibular nuclei and nucleus prepositus hypoglossi on both sides of the brain stem. These neurons receive velocity signals from excitatory burst neurons and integrate this velocity into a position signal.
Movement and coordination of the eyes in the orbits involves coordinating the motor commands and signals between the two eyes to deal with multiple forces in parallel. The brain has to continually update the equations it writes for eye muscles and blink rate to solve factoring in these viscoelastic elastic forces, which include increased coefficients of drag, when the eyes are inadequately lubricated. This is one reason why dry eyes should be of concern to functional optometry, and why keeping both eyes adequately lubricated through systemic control, rather than just dumping in eye drops or plugging the punctae, is important.
While there is danger in looking at vision reductionistically as a pair of eyeballs, there is also danger in disregarding the fact that we rely on a pair of eyeballs for binocular vision. This perpetual dance between reductionism and holism in binocular vision has been around since the days of Helmholtz, and was lauded by Albert Darwin Ruedemann when he spearheaded the Department of Ophthalmology at The Cleveland Clinic one hundred years ago.
Thus far we’ve been focusing on resultant (bottom-up) eye movements, but Goldberg and Walker do a very nice job of integrating this with top-down neuronal signal communication. Superior colliculus and parietal cortex get their fair share of coverage, but with regard to saccades they give nice coverage to three neuron arcs in the frontal eye field (FEF): visual neurons, movement-related neurons, and visuomovement neurons. Movement-related neurons in FEF control superior colliculus through two pathways, one excitatory and one inhibitory release.
In addition to FEF, the supplementary eye field (SEF) brings up the rear of the supplementary motor area that is crucial in the cognitive control of eye movements. SEF contains neurons that encode spatial information essential for the direction of desired eye movement. While much of the research on gaze control presented in this chapter stems from monkeys, our brains and visually guided behavior are eerily similar to that of our first cousins.