BLOG: In dreams begin – ocular – responsibilities

I recently read a hypothesis from Fitt and colleagues that claimed, “contrary to previous opinion, the purpose of REM during sleep is to ensure corneal respiration in the absence of the buoyant mixing that routinely takes place ... during waking conditions.”

This didn’t seem right to me, but admittedly sounded intriguing. Then I realized that as an eye doctor, I knew very little about the rapid eye movements (REMs) that occur during sleep.

Why do they happen? Are they random? I came into REM literature with a lot of questions. I left humbled and with a lot more questions. The literature involving sleep and its stages is fascinating, but very complex and dense. It’s also – as you might imagine – hard to test many of these hypotheses, what with the patient being unconscious and all. But we have responsibilities as eye doctors, so let’s try to learn about REM.

There are four stages of sleep: the first three stages are non-REM (NREM) and cleverly named stages 1, 2 and 3, with the fourth stage being REM sleep. Stage 1 is the lightest sleep; we are easily awakened, but muscle tone relaxes, and EEG-measured brain activity slows. Stage 2 is a deeper sleep, and awakenings are fewer. Brain waves continue to slow, the heart rate drops, and body temperature falls. In stage 3, brain waves are traveling very slowly, and it can be difficult to arouse someone from this stage. This is the most restorative sleep we have, but adults spend only about 5% to 15% of our sleep in this stage (Ermis et al.) as opposed to 40% to 60% of our sleep time in stage 2 (children and adolescents spend longer in stage 3 than do adults). After stage 3, we go into REM stage, which is where we do most of our dreaming.

REM sleep is also known as paradoxical sleep, deriving that name because our brain activity rises to near wakened levels of activity, but our muscles undergo atonia, rendering us close to paralyzed. Our bodies accomplish this by hyperpolarizing motor neurons, thus requiring a very large neuronal stimulus to overcome this threshold to depolarize the nerve. It’s thought that muscle atonia occurs to prevent us from acting out our dreams and possibly injuring ourselves (Hobson et al.). But why do the extraocular movements not undergo atonia? Why do they fire so aggressively in this phase?

Rapid eye movements are immediately preceded by something known as Ponto-geniculo-occipital (PGO) waves, so it stands to reason that these waves of neuronal activity in the pons, geniculate bodies and occipital cortex are generating REMs (Peigneux et al.). However everything in sleep science seems to be controversial (even the definition of dreaming is argued), and it’s unclear exactly how PGOs and REMs are related.

I’ll present two leading theories vis-à-vis how they relate to REM sleep saccades: the activation synthesis model and the activation-only model. The activation synthesis model argues that PGOs are started in the brainstem (Antrobus), and during REM sleep, enough chaotic brainstem activity eventually triggers a depolarization, and a PGO wave occurs, and a saccade is generated essentially from randomness.

The activation-only model argues that PGOs are cortical in origin, a theory thought of as the scanning hypothesis. In this model, the REM saccades are the frontal eye fields’ attempt to fixate on a dream image, and the PGO wave starts in the visual cortex and transmits to the brainstem oculomotor nuclei to start the saccades (just like in waking saccades), according to Antrobus. The scanning hypothesis of REMs is intriguing, but you can imagine how difficult it would be to prove.

For just one example of the layers of complexity we’re dealing with, researcher Herman mentions that earlier studies “failed to take into account the dreamer’s fictive head movements which, in dreaming, may coincide with cortically directed saccades and modify such saccades via the vestibuloocular reflex.” So it gets tricky.

And this quote from a major paper from Hobson and colleagues summarizes the frustration in REM saccade research: “We want to emphasize that the field of dream research foundered because of its overinvestment in still unresolved arguments about scanning, and we ... appeal to keep the question of eye movement and dream imagery open until methods more adequate to its investigation are developed.”

So, we are forced into an agnosticism regarding the question of why we perform REMs during our sleep, but it’s fascinating to think about. Are these random movements? Or are they linked to the plot of the dream? Older theories postulated that REMs were a way to consolidate memories from the day (Crick et al.), a daily formatting of our internal hard drive, if you will. I found another hypothesis that pondered if REMs were our brain wandering through its plan of attack for the upcoming day – a dress-rehearsal type of daily walk-through. I think it’s nice to think that at least my brain knows what the plan is for tomorrow.

References:

Antrobus J. Psychological Review. 1991;doi.org/10.1037/0033-295X.98.1.96.

Ermis U, et al. J Sleep Res. 2010;doi:10.1111/j.1365-2869.2010.00831.x.

Crick F, et al. Nature. 1983;doi:10.1038/304111a0.

Fitt AD, et al. Bull Math Biol. 2006;doi:10.1007/s11538-005-9015-2.

Herman J. Behav Brain Sci. 2000;23:6.

Hobson JA, et al. Behav Brain Sci. 2000;23:793-1121.

Peigneux P, et al. Neuroimage. 2001;doi:10.1006/nimg.2001.0874.