Rapid Eye Movements in Sleep Furnish a Unique Probe into the Ontogenetic and Phylogenetic Development of the Visual Brain: Implications for Autism Research.

With positron emission tomography followed by functional magnetic resonance imaging (fMRI), we demonstrated that rapid eye movements (REMs) in sleep are saccades that scan dream imagery. The brain "sees" essentially the same way while awake and while dreaming in REM sleep. As expected, an event-related fMRI study (events = REMs) showed activation time-locked to REMs in sleep ("REM-locked" activation) in the oculomotor circuit that controls saccadic eye movements and visual attention. More crucially, the fMRI study provided a series of unexpected findings, including REM-locked multisensory integration. REMs in sleep index the processing of endogenous visual information and the hierarchical generation of dream imagery through multisensory integration. The neural processes concurrent with REMs overlap extensively with those reported to be atypical in autism spectrum disorder (ASD). Studies on ASD have shown atypical visual processing and multisensory integration, emerging early in infancy and subsequently developing into autistic symptoms. MRI studies of infants at high risk for ASD are typically conducted during natural sleep. Simply timing REMs may improve the accuracy of early detection and identify markers for stratification in heterogeneous ASD patients. REMs serve as a task-free probe useful for studying both infants and animals, who cannot comply with conventional visual activation tasks. Note that REM-probe studies would be easier to implement in early infancy because REM sleep, which is markedly preponderant in the last trimester of pregnancy, is still pronounced in early infancy. The brain may practice seeing the world during REM sleep in utero before birth. The REM-probe controls the level of attention across both the lifespan and typical-atypical neurodevelopment. Longitudinal REM-probe studies may elucidate how the brain develops the ability to "see" and how this goes awry in autism. REMs in sleep may allow a straightforward comparison of animal and human data. REM-probe studies of animal models of autism have great potential. This narrative review puts forth every reason to believe that employing REMs as a probe into the development of the visual brain will have far-reaching implications.