Human brain activity time-locked to rapid eye movements during REM sleep

Abstract

To identify the neural substrate of rapid eye movements (REMs) during REM sleep in humans, we conducted simultaneous functional magnetic resonance imaging (fMRI) and polysomnographic recording during REM sleep. Event-related fMRI analysis time-locked to the occurrence of REMs revealed that the pontine tegmentum, ventroposterior thalamus, primary visual cortex, putamen and limbic areas (the anterior cingulate, parahippocampal gyrus and amygdala) were activated in association with REMs. A control experiment during which subjects made self-paced saccades in total darkness showed no activation in the visual cortex. The REM-related activation of the primary visual cortex without visual input from the retina provides neural evidence for the existence of human pontogeniculo-occipital waves (PGO waves) and a link between REMs and dreaming. Furthermore, the time-course analysis of blood oxygenation level-dependent responses indicated that the activation of the pontine tegmentum, ventroposterior thalamus and primary visual cortex started before the occurrence of REMs. On the other hand, the activation of the putamen and limbic areas accompanied REMs. The activation of the parahippocampal gyrus and amygdala simultaneously with REMs suggests that REMs and/or their generating mechanism are not merely an epiphenomenon of PGO waves, but may be linked to the triggering activation of these areas.

Activation of Retinotopic Visual Areas Is Central to REM Sleep Associated Dreams: Visual Dreams and Visual Imagery Possibly Co-Emerged In Evolution

“…However, REMS visual imagery uses very similar neural systems as those used in wakefulness (Borst, & Kosslyn, 2010Sprenger et al, 2010. Nevertheless, recent event-related fMRI showed activation of V1 during REMS (Hong et al, 2009Miyauchi et al, 2009) and the findings that REMS associated visual imagery uses very similar neural systems as those used in wakefulness (Nir & Tononi, 2010Sprenger et al, 2010 support our contention.…”

“…Recently, Miyauchi et al (2009) presented evidence for the existence of PGO waves in human REMS and demonstrated that activity in the pontine tegmentum, ventroposterior thalamus, and V1 took place in the few seconds prior to REM saccades. They proposed that REM saccades may be in response to PGO-initiated dreamed visual imagery, because V1 activation is arisen some seconds before REM saccades.…”

“…However, complex retinotopic visual can serve some special function not only during visual perception and imagery but also during REMS associated visual dreams. Since, it appears that numerous retinotopic visual areas are activated during REMS (Igawa et al, 2001Peigneux et al, 2001Hong et al, 2009Miyauchi et al, 2009, it suggests that one of the major aims of REMS is to activate visual imagery directed via subconscious processes. Based on present knowledge, the neuro-anatomo-chemical substrates in the brain for activation of REMS-associated expression of visual imagery may be supported by the diagram shown in Figure 1a and 1b.…”

Cognitive and emotional processes during dreaming: A neuroimaging view

“…These early PET results are also consistent with the observation that patients with cortical blindness (after primary visual cortex or perichiasmatic lesions) report that they still dream with visual images (Solms, 1997a). Yet, some recent fMRI studies suggest that rapid eye movements during REM sleep might be associated with increased fMRI activity in V1 (Miyauchi, Misaki, Kan, Fukunaga, & Koike, 2009). On the other hand, because several studies found that auditory stimuli may be processed to some extent during sleep (Atienza, Cantero, & Escera, 2001;Czisch et al, 2002;Perrin, Garcia-Larrea, Mauguiere, & Bastuji, 1999;Portas et al, 2000;Wehrle et al, 2007), we would predict that external auditory stimulation during sleep may effectively coordinate activation within primary and associative auditory cortices.…”

“…Several lines of evidence suggest the existence of PGO waves in humans: direct intracranial recordings in epileptic patients (Salzarule et al, 1975), surface EEG (Salzarule et al, 1975), magnetoencephalography (MEG) (Inoue, Saha, & Musha, 1999). Neuroimaging studies using PET and fMRI also found correlations during REM sleep, but not during wakefulness, between spontaneous eye movements and regional cerebral blood flow (rCBF) in the occipital cortex and the lateral geniculate of the thalamus (Peigneux et al, 2001;Wehrle et al, 2005;Miyauchi et al, 2009).…”