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REM sleep and dreaming: towards a theory of protoconsciousness

Key Points

  • We know how, but not why, the brain is activated in sleep. I suggest that brain activation in sleep allows the development and maintenance of circuits necessary for higher brain functions, including consciousness.

  • Brain activation and sleep occurs early in the development of mammals and birds. It may therefore be a state of protoconsciousness in those animals that evince rapid eye movement (REM) sleep.

  • Our dreams are reminders that we too were (and still are) protoconscious. We are always ourselves in our dreams; we sense, we act and we feel vividly in an entirely fictive world of the brain's devising.

  • The protoconscious state of REM sleep dreaming is as much a preparation for waking consciousness as a reaction to it. We are as much getting ready to behave as we are getting over the effects of our behaviour.

  • Dreams have more in common than not across individuals. As a species, we need REM sleep dreaming to accomplish shared goals, such as being capable of consciousness when awake.

  • REM sleep dreaming can be viewed as a virtual reality pattern generator used by the brain to instantiate and maintain its readiness for adaptive interaction with the world.

Abstract

Dreaming has fascinated and mystified humankind for ages: the bizarre and evanescent qualities of dreams have invited boundless speculation about their origin, meaning and purpose. For most of the twentieth century, scientific dream theories were mainly psychological. Since the discovery of rapid eye movement (REM) sleep, the neural underpinnings of dreaming have become increasingly well understood, and it is now possible to complement the details of these brain mechanisms with a theory of consciousness that is derived from the study of dreaming. The theory advanced here emphasizes data that suggest that REM sleep may constitute a protoconscious state, providing a virtual reality model of the world that is of functional use to the development and maintenance of waking consciousness.

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Figure 1: Dream Caused by the Flight of a Bee around a Pomegranate a Second Before Awakening (Salvador Dali).
Figure 2: Developmental and evolutionary considerations.
Figure 3: Proposed steps in brain development leading to the emergence of the NREM–REM sleep cycle and its alternation with waking.
Figure 4: AIM model of brain–mind state control.
Figure 5: Normal and lucid dreaming: differential regional activation patterns.

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Acknowledgements

The research reported here was supported by the US National Institute of Mental Health, the National Science Foundation and the MacArthur Foundation. The theoretical work was supported by the Sleep Research Society (keynote lecture of 6/26/08) and by Roehampton University (William James Lectures of 3/18/09). I am grateful to U. Voss, M. Czisch, S. Datta, M. Dresler and R. Wehrle for helpful suggestions. I thank N. Tranquillo for his administrative assistance in the production of the manuscript. Protoconsciousness theory is inspired, in part, by the genetic programming hypothesis of REM sleep, created by my mentor and colleague, M. Jouvet.

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Some formal properties of dream consciousness of relevance to neurobiology (PDF 212 kb)

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Methods and strategy of dream neuroscience (PDF 158 kb)

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Glossary

Perception

Detailed visuomotor and other sense modality information that constitutes the representational structure of awareness. Such awareness must involve the interaction and integration of emotion.

Secondary consciousness

Subjective awareness including perception and emotion that is enriched by abstract analysis (thinking) and metacognitive components of consciousness (awareness of awareness).

Rapid eye movement (REM) sleep

Sleep with electroencephalographic evidence of brain activation (similar to that of waking) but with inhibition of muscle tone (as measured by electromyography) and involuntary saccadic eye movements (the REMs).

Primary consciousness

Subjective awareness of perception and emotion.

Consciousness

Subjective awareness of the world, the body and the self, including awareness of awareness.

Waking

A brain state associated with electroencephalographic activation (similar to that of REM) but with the muscle tone enhancement (as measured by electromyography) that is necessary for posture and movement.

Non-rapid eye movement (NREM) sleep

Sleep with electroencephalographic evidence of brain deactivation; spindles and slow waves characterize this brain state.

Lucid dreaming

The subjective awareness that one is dreaming and not awake (as is usually incorrectly assumed).

Binding problem

A science of consciousness must explain how so many aspects of our experience are integrated. The binding of perception, emotion, thought and memory requires a physical explanation at the level of brain function.

Protoconsciousness

A primordial state of brain organization that is a building block for consciousness. In humans, protoconsciousness is proposed to develop as brain development proceeds in REM sleep in utero and in early life.

Activation

(A). In behavioural neurobiology and cognitive science, the term activation is used to express the level of energy of the brain and its constituent circuits. The analogy to a power supply with an on–off switch conveys the essence of this idea.

Input–output gating

(I). The process that facilitates or inhibits, as the brain changes state, access to the brain of sensory information (input) from the outside world and the transmittal of motor commands from the brain (output) to the musculature.

Modulation

(M). The chemical microclimate of the brain is determined largely by neurons in the brainstem, which send their axons widely to the forebrain, spinal cord and cerebellum. Among the chemicals released by these cells are dopamine, noradrenaline, serotonin, histamine and acetylcholine.

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Hobson, J. REM sleep and dreaming: towards a theory of protoconsciousness. Nat Rev Neurosci 10, 803–813 (2009). https://doi.org/10.1038/nrn2716

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