I was out on a small boat going to the Marietta Islands to fulfill a long-time dream of seeing blue-footed boobies (fun to say, don’t you think?) and was trying to take some pictures. Check out how that turned out:

The pictures are not steady because my hands moved as the boat rolled, pitched, and rotated on the choppy ocean. I could not keep my hands steady on the moving boat. But think about it – did my view (what I saw) move about? Absolutely not. Why not? Because every movement of my head was opposed by a movement of my eyes. I used my vestibular reflexes to stabilize my gaze.

Gaze means where you are looking, where your eyes are pointed. [It may be a great temptation to say “where our eyes are focused” to mean where we’re looking. However, light is focused by our eyes which are fixated on some point in space. Light is focused. Eyes are not focused. Eyes fixate. I have to say that it took me an embarrassingly long time to register the correct meaning of focus and fixate.]

Gaze is determined by eye and head position. Under many, perhaps most, circumstances, we control gaze nearly exclusively using movements of our eyes. For example, as you read this, your eyes are moving left to right in short bursts, returning to the left and repeat. It is entertaining to watch this. Just ask someone to read from a book or computer screen and watch their eyes dart along the text. Here is a video of me reading from The Uncommon Reader by Alan Bennett (Picador, New York, 2008):

You see my eyes moving in bursts called saccades. You may also notice that my head appears to move a bit. In fact that movement comes from the fact that the camera is hand-held and therefore moving (think The Blair Witch Project). Head movement while standing on steady ground is minuscule in healthy individuals. But head movements happen all the time, either because we produce them (e.g. as we walk or jog or dance or jump) or because of outside forces (e.g. riding on a merry-go-round or in a bus or sitting on a tree branch that is swaying in the wind or stumbling and falling). Gravity also acts on our head. Head movements (actually head accelerations) are detected by cells in the vestibular labyrinth located in the inner ear. Head movements are the cue that the brain uses to stabilize gaze. The vestibuloocular reflex, affectionately termed the VOR by neurobiologists, serves to produce eye movements that oppose head movements. The vestibulocollic reflex uses neck movements to oppose head movements.

We use vestibular input rather than vision to drive the VOR and keep our gaze steady. There is a really easy way for you to demonstrate this to yourself.  Hold your finger out in front of you. Shake your head back and forth as though indicating “no”. Does your image of your finger remain clear? Now keep your head steady and move your finger back and forth. Is the image of your finger steady? By doing this exercise, you will see that gaze is steady when your head moves but not when an object moves. The vestibular reflexes that keep gaze steady are automatic. They depend on circuits in the brainstem and are not a function to which we devote conscious control or forebrain time and energy. In fact, we are blissfully unaware of our vestibular senses under normal circumstances. We typically become aware of our vestibular sense only when it does not work. For example, when suffering from food poisoning or extremely drunk, the room may start to spin. In such cases, conscious vestibular sensations are experienced as extremely unpleasant. Normally, we are entirely unaware of our vestibular state. We adapt to our vestibular status so rapidly that it never even enters our consciousness. Adaptation happens in all sensory systems but it is really, really rapid in the vestibular system. A runner up might be touch: shortly after putting our clothes on, the sensation of the clothes fades from consciousness.

The reason that we use the VOR to steady gaze is because it is so fast. In all ways imaginable, the vestibular system is far faster than the visual system. The difference in speed begins with the very first step in sensation, transduction. Transduction means transforming stimulus energy into an electrical code that neurons can understand. Transduction in the vestibular system depends on an ion channel whereas transduction in the retina depends on a G-protein named transducin that induces a chemical cascade that in turn closes an ion channel.

Correction added on April 27, 2014: Thanks to a colleague who pointed out an error in this post.  Originally, I wrote that “transduction in the retina depends on a G-protein coupled receptor named transducin”. Transducin is actually the G-protein. It is coupled to a photon-responsive “receptor” molecule called rhodopsin (made up of retinal and an opsin). You can think of rhodopsin as a receptor whose ligand is a photon.

A second source of vestibular speed stems from the small number of synapses involved in the VOR. To get from the inner ear to an extraocular muscle (one of the 6 muscles that moves the eyeball) takes 4 synapses (hair cell to vestibular afferent to vestibular nuclear neuron to motoneuron to muscle for those counting at home). In contrast, there is no short path from retina to extraocular muscles. After four synapses, the visual message has just made it out of the retina.

Finally, let’s consider what the term reflex does and does not mean. The VOR is one of the best examples, maybe the best, of a reflex. The VOR cannot be performed deliberately, meaning you cannot fake it. The VOR uses well-connected neurons in a set sequence. However, the VOR is not always the same and can even be suppressed altogether. You can do a few exercises to convince yourself of this. First, shake your head while looking at your finger. Now go outside and fixate at a point on the horizon. Shake your head. You will see that your eyes barely move when you are fixating on the horizon. Thus, the gain of the VOR (output/input or in this case, eye movement / head movement) is much greater when looking at near objects than at far objects. Now rotate your head and your finger together in one direction. Keep fixated on your finger. In this situation, you have suppressed your VOR. You have actually turned it off. Your head is rotating but your eyes are staying stationary within your head. The plasticity (or changeability) of the VOR is true for all reflexes.

Oh, and yes, in case you were wondering, the mission to see blue-footed boobies was not only accomplished but photographically documented:

Check out those baby blues!!!