I’m not only a member of the New York Academy of Sciences; I’m one of its biggest fans. Access to the Annals of NYAS alone is worth the price of membership. The most recent annals is volume 1233, presenting the proceedings of the conference Basic and Clinic Ocular Motor and Vestibular Research, held as a tribute to the career of Dr. Richard Leigh, a world-renowned expert in the neurological control of eye movements.
There are many fine papers in the volume, but one in particular by Carpenter caught my eye, and it bears the title of this blog post. As Skeffington was to behavioral optometry, Sherrington was to eye movements. It turns out that in addition to winning the Nobel Prize for Medicine in 1932, Sherrington was also a bit of a poet and philosopher, publishing a remarkable work in 1940 – Man on his Nature. Consider this passage: “An act which may seem simple even to banality is the directing of gaze. Yet its factors engage the roof-brain far and wide.” Anticipating the social complexity of gaze-following which has emerged as a huge topic in developmental science, Sherrington was even more prescient in 1906 when he published a volume on Integrative Action of the Nervous System.
Yet, Carpenter notes, perhaps because Sherrington was educated as a classicist, there was an important aspect of neural integration that he appeared to have missed completely, and that is that neural phenomena are integrated in time as they are in space. That subsequently became the heart of oculomotor integration theory, and we in Optometry have numerous models of this, as reviewed by Ebenholtz and Hung & Ciuffreda, for example.
As depicted below, Carpenter sugggests that the concept of an oculomotor integrator is essential in the vestibulo-ocular reflex (VOR) in order to convert the signals from the semicircular canals – which under natural conditions signal the rotational velocity of the head – to eye position in the orbit.
As illustrated above, stimuli in motor systems in general demonstrate adaptation or rate sensitivity (d/dt) in order to generate responses, and are mediated by a differential. The afferent signals arriving at the brain are invariably high-pass filtered, whether through neural processing or through mechanisms built into the sensory receptors themselves. Adaptation or rate sensitivity is useful in aiding prediction, eliminating redundancy in neural codes, and increasing dynamic ranges. Most significantly, rate sensitivity has the consequence that the brain works in terms of change: if we are to make sustained responses to maintained stimuli, afferent differentiation must be exactly counterbalanced by efferent integration. Elsewhere Carpenter does a nice job of using the saccade system as a microcosm of this type of neural integration.
Here is a beautiful quote from Carpenter: “Our eyes alternately shift and hold, reflecting the alternation of reaching and grasping that is the systole and diastole of the motor system as a whole.” He continues: “There is a cliche – often wrongly – attributed to Sherrington, that ‘movement begins with posture.’ What Sherrington did say in 1915 was that ‘The role of muscle as an executant of movements is so striking that its office in preventing movement and displacement is somewhat overlooked’. This type of balance/counterbalance is particularly true of the oculomotor system and part of what we look for when, for example, we watch happens to pursuit eye movements as a patient crosses the midline, or when we observe head and body movement during standardized oculomotor testing such as the NSUCO.
Lastly, in biomedical engineering terms we might say that conditions involving an undesirable shift in the visual guidance of posture and movement is due to a leaky neural integrator. When we do something as basic as probing the effect of yoked prisms in cases of visual midline shift, for example, we are at some level fixing a hole in the leaky integrator that keeps us from wandering.
All this supports the notion that vision is not a separate isolated function. It is profoundly integrated with the development of the total action system of the patient, including posture, coordination, and personality. I wish I had thought of that myself, but it’s actually a quote from the incomparable Al Sutton.
– Leonard J. Press, O.D., FCOVD, FAAO