Developmental changes in cortical sensory processing during wakefulness and sleep

Abstract

Infants are exposed to auditory and visual information during sleep as well as wakefulness. Little is known, however, about the differences in cortical processing of sensory input between these different behavioral states. In the present study, cortical hemodynamic responses to auditory and visual stimuli during wakefulness and sleep were measured in infants aged 2–10 months using functional near-infrared spectroscopy (fNIRS). While asynchronously presented auditory and visual stimuli during wakefulness induced focal responses in the corresponding sensory regions of the occipital and temporal cortices, the responses to the same stimuli during sleep were dramatically different. Auditory stimuli during sleep induced global responses over the frontal, temporal, and occipital regions, and the response pattern did not change between 2 and 10 months of age. In contrast, visual stimuli during sleep induced responses in the occipital cortex, and the response pattern exhibited developmental changes from a pattern of activation to one of deactivation around a half year of age. The functional connectivity among the cortical regions was generally higher during sleep than during wakefulness. The hemoglobin phase of oxygenation and deoxygenation (hPod) and the phase locking index of hPod (hPodL) showed general developmental changes and behavioral state dependent differences but no significant differences were seen between the stimulus types. The results suggest that the behavioral states have a fundamental impact on cortical sensory processing; (1) sensory processing during wakefulness is performed in more localized regions, (2) auditory processing is active during both wakefulness and sleep, (3) visual processing undergoes development of inhibitory mechanisms during sleep, and (4) these phenomena primarily reflect neural development rather than vascular and metabolic development.