In the flicker of an eye
Year: 2008
Type: article
Abstract: Dreams were tentatively associated with twitching of the eyelids and somatic muscles during sleep in 1868 by Griesinger (Finger, 1994). However, it was not until 1953 that Aserinsky & Kleitman (1953) identified a discrete sleep stage they termed rapid eye movement (REM) sleep characterized by recurrent episodes of non-respiratory muscle atonia and desynchronized EEG, coinciding with enriched dream content. Superimposed upon these tonic REM features, they observed phasic phenomena including increased heart rate, irregular and shallower respiration, brief muscle twitches, and REM's hallmark, bursts of rapid eye movements. Although there is some evidence for the correlation of dream content and eye movements, REMs are maintained or increased after destruction or removal of the cerebral cortex, and continue in animals after midbrain transection (Jouvet, 1962), arguing against them being caused by cortical activity. Remarkably, given the role of REMs in defining this interesting behavioural state, the study of the REMs themselves has been largely phenomenological. In standard polysomnography, the electro-oculogram (EOG) is used for the measurement of eye movement, helping to easily identify REM sleep. This method measures the alteration in charge between two electrodes due to the movement of the large polarized retina with the globe of the eye. The EOG is not, however, suitable to determine slow eye movements or absolute eye position accurately. As a result, earlier studies focused mainly on the very rapid and predominantly conjugate horizontal eye movements that characterize REMs. An early study employing the monocular magnetic search coil technique maintained a similar focus (Vanni-Mercier et al. 1994). Magnetic search coil techniques, with scleral annuli were introduced in 1963 by Robinson and gained popularity in the 1980s. They are currently the technique of choice for experimental studies in which accurate absolute measurement of eye position in all three axes is required. In the present issue of The Journal of Physiology, Márquez-Ruiz & Escudero (2008a,b) use binocular search coils to describe accurately REMs in cats, including, for the first time, measurement of tonic and vergence movements, associated changes in abducens activity, and the relationship of these phenomena to ponto-geniculooccipital waves. Although REMs are stereotypical and occur reliably as a marker of REM sleep, the oculomotor control during REM sleep remains poorly understood. The abducens nucleus is responsible for abduction of the globe and conjugate adduction via a projection to the contra-lateral oculomotor nucleus. It receives input from a variety of structures (Maciewicz et al. 1977), including the vestibular nuclei and dorsal paragigantocellular region of the rostral medulla, both of which are REM active. Vestibular inputs to the oculomotor nuclei play an important role in disynaptic vestibuloocular reflexes. However, the inputs from the region immediately caudal to the abducens nucleus are less well understood. In non-human primates, this dorsal paragigantocellular region is currently characterized as containing inhibitory burst neurons (Strassman et al. 1986), and in rats, as containing REM-on neurons (Goutagny et al. 2008). Saccadic eye movements consist of two components. The first, a rapid and large extra-ocular muscle contraction, begins a rapid rotation of the globe. Subsequently, a step function then maintains eye position. Present models describe excitatory burst neurons of the paramedian pontine reticular formation and vestibular nuclei, and neurons of the nucleus prepositus hypoglossi, respectively, as responsible for these two components of horizontal saccades (Leigh & Zee, 2006). During REM sleep, however, eye movements consist of only the first burst component, without a subsequent step function. In a series of papers in the mid-1960s, Pompieano and Morrison (see Pompeiano & Morrison, 1965) describe the loss of REMs and other phasic phenomena in cats following electrolytic lesions of the inferior and medial vestibular nuclei. The lesions were somewhat variable as the technique was difficult to control and destroyed fibres of passage. The premotor region mediating the burst thus remains poorly characterized, but represents an opportunity to identify phasic REM mechanisms, and may assist in differentiating their functional anatomy from the tonic REM circuitry. The identification of the source of phasic activity in REM sleep is of clinical importance, as phasic autonomic activation during REM sleep increases the risk for myocardial ischaemia or arrhythmia. Márquez-Ruiz and Escudero here comprehensively characterize two important components of REMs: a slow change in tonic eye position between wakefulness, non-REM and REM sleep, upon which is superimposed phasic REMs during REM sleep. The tonic change in eye position is from an outward and divergent position, to a downward and convergent position during REM. This novel finding leads us to ask what differential tonic changes occur in oculomotor nuclei during the transitions into non-REM and REM sleep. It may be, for example, that abducens motorneurons are inhibited to a relatively greater extent than those of the oculomotor and trochlear nuclei during REM, as would be consistent with Márquez-Ruiz and Escudero's description of abducens nucleus inhibition during REM. These papers by Márquez-Ruiz and Escudero provide important details about the precise nature of REMs and abducens unit activity that may constitute an important alternative approach to studying oculomotor control, and further our understanding of the mechanisms of both phasic and tonic REM sleep phenomena. Phasic REM features are loosely coordinated, and it is likely that they originate in a brain structure one or two synapses from the abducens nucleus. These articles and the utilized techniques will allow future studies that narrow candidate regions.
Source: The Journal of Physiology
Authors: N. P. Pedersen, P. M. Fuller, J. Lu, C. B. Saper
Institution: Beth Israel Deaconess Medical Center
Language: English
Subfield: Cognitive Neuroscience
Field: Neuroscience
Domain: Life Sciences
Open Access status: green
OpenAlex ID: W2124607395