Dreaming and the brain: from phenomenology to neurophysiology

Abstract

Dreams are a remarkable experiment in psychology and neuroscience, conducted every night in every sleeping person. They show that the human brain, disconnected from the environment, can generate an entire world of conscious experiences by itself. Content analysis and developmental studies have promoted understanding of dream phenomenology. In parallel, brain lesion studies, functional imaging and neurophysiology have advanced current knowledge of the neural basis of dreaming. It is now possible to start integrating these two strands of research to address fundamental questions that dreams pose for cognitive neuroscience: how conscious experiences in sleep relate to underlying brain activity; why the dreamer is largely disconnected from the environment; and whether dreaming is more closely related to mental imagery or to perception.

Figure 1. Functional neuroanatomy of human REM sleep: a meta-analysis of PET results

Meta-analysis of relative increases and decreases in neuronal activity during REM sleep as seen with PET imaging using H2¹⁵O measurements of regional cerebral blood flow (rCBF) [15, 16, 19] or [¹⁸F]-flurodeoxyglucose measurements of glucose metabolism[17]. Top row: cortical surface, lateral view. Middle row: cortical surface, medial view. Bottom row: subcortical foci (left) and ventral view of cortical surface (right). Analysis is based on published Talairach coordinates of foci whose activity was significant at p<0.001 corrected (Z-score > 3.09). Circles, squares, triangles, and stars denote activity foci as reported by [15] (Maquet 96), [16] (Braun 97), [17] (Nofzinger 97), and [19] (Maquet 2000), respectively. Each symbol marks a region’s center-of-mass regardless of its spatial extent. Yellow symbols denote increased regional activity in the (1) mesopontine tegmentum and midbrain nuclei, (2) thalamus, (3) basal forebrain and diencephalic structures, (4) limbic MTL structures including amygdala and hippocampus, (5) medial prefrontal cortex, (6) occipito-temporal visual cortex, and (7) anterior cingulate cortex. Cyan symbols denote decreased activity in the (8) orbitofrontal cortex, (9) posterior cingulate and precuneus, (10) dorsolateral prefrontal cortex, and (11) inferior parietal cortex.

Figure 2. Neurophysiology of wake and sleep states

A comparison of cortical activity (upper panel) and neuromodulator activity (bottom panel) in wake, early NREM (when sleep pressure is high and dream reports are rare), late NREM (when sleep pressure dissipates, and dream reports are more frequent), and REM sleep (when dreams are most common). (a) Intracellular studies. The membrane potential of cortical neurons in both wake and REM sleep is depolarized and fluctuates around −63mV and −61mV, respectively [77]. In REM sleep, whenever phasic events such as rapid eye movements and PGO waves occur (gray arrows, events not shown), neurons increase their firing rates to levels that surpass those found in wake [77, 146]. In early NREM sleep, neurons alternate between two distinct states, each lasting tens/hundreds of milliseconds: UP states (red arrow) are associated with depolarization and increased firing, while in DOWN states (blue arrow) the membrane potential is hyperpolarized around −75mV, and neuronal firing fades[78, 147]. Intracellular studies focusing specifically on late NREM sleep are not available (N.A.). (b) Extracellular studies. Spiking of individual neurons in REM sleep reaches similar levels as in active wake. In both wake and REM sleep, neurons exhibit tonic irregular asynchronous activity [, –151]. Sustained activity in wake and REM sleep can be viewed as a continuous UP state [78] (red bars). In early NREM sleep, UP states are short and synchronous across neuronal populations, and are frequently interrupted by long DOWN states (blue bars). In late NREM sleep, UP states are longer and less synchronized [79]. (3) Polysomnography. Waking is characterized by low-amplitude, high-frequency EEG activity (above 7Hz), occasional saccadic eye movements, and elevated muscle tone. In early NREM sleep, high-amplitude slow waves (below 4Hz) dominate the EEG. Neuronal UP (red) and DOWN (blue) states correspond to positive and negative peaks in the surface EEG, respectively [79]. Eye movements are largely absent and muscle tone is decreased. In late NREM sleep, slow waves are less frequent, while spindles (related to UP states and surface EEG positivity) become more common. Eye movements and muscle tone are largely similar to early NREM sleep [152]. In REM sleep, theta activity (4–7 Hz) prevails, rapid eye movements occur, and muscle tone is dramatically reduced. (d) Neuromodulator activity. Subcortical cholinergic modulation is highly active in wake and REM sleep (green arrows) and leads to sustained depolarization in cortical neurons and EEG activation [77]. Wake is further maintained by activity of monoamines, histamine, and hypocretin/orexin (green arrows). In sleep, monoaminergic systems including norepinephrine and serotonin reduce their activity (pink arrows), and are silent in REM sleep (red arrows). While dopamine levels do not change dramatically across the sleep-wake cycle (asterisks), phasic events and regional profiles may differ[153]. Data are pooled across different species for illustration purposes. Intracellular cat data adapted with permission from Ref [77]; extracellular and EEG rat data obtained from V. Vyazovskiy (personal communication).