Balancing Prediction and Surprise: A Role for Active Sleep at the Dawn of Consciousness?

The brain is a prediction machine. Yet the world is never entirely predictable, for any animal. Unexpected events are surprising, and this typically evokes prediction error signatures in mammalian brains. In humans such mismatched expectations are often associated with an emotional response as well,...

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Autores principales:	Matthew N. Van De Poll, Bruno van Swinderen
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	REM sleep consciousness predictive coding emotions invertebrate Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571
Acceso en línea:	https://doaj.org/article/0a0952984c504c09b01300c36f6d1c85
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spelling	oai:doaj.org-article:0a0952984c504c09b01300c36f6d1c852021-11-05T14:16:59ZBalancing Prediction and Surprise: A Role for Active Sleep at the Dawn of Consciousness?1662-513710.3389/fnsys.2021.768762https://doaj.org/article/0a0952984c504c09b01300c36f6d1c852021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fnsys.2021.768762/fullhttps://doaj.org/toc/1662-5137The brain is a prediction machine. Yet the world is never entirely predictable, for any animal. Unexpected events are surprising, and this typically evokes prediction error signatures in mammalian brains. In humans such mismatched expectations are often associated with an emotional response as well, and emotional dysregulation can lead to cognitive disorders such as depression or schizophrenia. Emotional responses are understood to be important for memory consolidation, suggesting that positive or negative ‘valence’ cues more generally constitute an ancient mechanism designed to potently refine and generalize internal models of the world and thereby minimize prediction errors. On the other hand, abolishing error detection and surprise entirely (as could happen by generalization or habituation) is probably maladaptive, as this might undermine the very mechanism that brains use to become better prediction machines. This paradoxical view of brain function as an ongoing balance between prediction and surprise suggests a compelling approach to study and understand the evolution of consciousness in animals. In particular, this view may provide insight into the function and evolution of ‘active’ sleep. Here, we propose that active sleep – when animals are behaviorally asleep but their brain seems awake – is widespread beyond mammals and birds, and may have evolved as a mechanism for optimizing predictive processing in motile creatures confronted with constantly changing environments. To explore our hypothesis, we progress from humans to invertebrates, investigating how a potential role for rapid eye movement (REM) sleep in emotional regulation in humans could be re-examined as a conserved sleep function that co-evolved alongside selective attention to maintain an adaptive balance between prediction and surprise. This view of active sleep has some interesting implications for the evolution of subjective awareness and consciousness in animals.Matthew N. Van De PollBruno van SwinderenFrontiers Media S.A.articleREM sleepconsciousnesspredictive codingemotionsinvertebrateNeurosciences. Biological psychiatry. NeuropsychiatryRC321-571ENFrontiers in Systems Neuroscience, Vol 15 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	REM sleep consciousness predictive coding emotions invertebrate Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571
spellingShingle	REM sleep consciousness predictive coding emotions invertebrate Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571 Matthew N. Van De Poll Bruno van Swinderen Balancing Prediction and Surprise: A Role for Active Sleep at the Dawn of Consciousness?
description	The brain is a prediction machine. Yet the world is never entirely predictable, for any animal. Unexpected events are surprising, and this typically evokes prediction error signatures in mammalian brains. In humans such mismatched expectations are often associated with an emotional response as well, and emotional dysregulation can lead to cognitive disorders such as depression or schizophrenia. Emotional responses are understood to be important for memory consolidation, suggesting that positive or negative ‘valence’ cues more generally constitute an ancient mechanism designed to potently refine and generalize internal models of the world and thereby minimize prediction errors. On the other hand, abolishing error detection and surprise entirely (as could happen by generalization or habituation) is probably maladaptive, as this might undermine the very mechanism that brains use to become better prediction machines. This paradoxical view of brain function as an ongoing balance between prediction and surprise suggests a compelling approach to study and understand the evolution of consciousness in animals. In particular, this view may provide insight into the function and evolution of ‘active’ sleep. Here, we propose that active sleep – when animals are behaviorally asleep but their brain seems awake – is widespread beyond mammals and birds, and may have evolved as a mechanism for optimizing predictive processing in motile creatures confronted with constantly changing environments. To explore our hypothesis, we progress from humans to invertebrates, investigating how a potential role for rapid eye movement (REM) sleep in emotional regulation in humans could be re-examined as a conserved sleep function that co-evolved alongside selective attention to maintain an adaptive balance between prediction and surprise. This view of active sleep has some interesting implications for the evolution of subjective awareness and consciousness in animals.
format	article
author	Matthew N. Van De Poll Bruno van Swinderen
author_facet	Matthew N. Van De Poll Bruno van Swinderen
author_sort	Matthew N. Van De Poll
title	Balancing Prediction and Surprise: A Role for Active Sleep at the Dawn of Consciousness?
title_short	Balancing Prediction and Surprise: A Role for Active Sleep at the Dawn of Consciousness?
title_full	Balancing Prediction and Surprise: A Role for Active Sleep at the Dawn of Consciousness?
title_fullStr	Balancing Prediction and Surprise: A Role for Active Sleep at the Dawn of Consciousness?
title_full_unstemmed	Balancing Prediction and Surprise: A Role for Active Sleep at the Dawn of Consciousness?
title_sort	balancing prediction and surprise: a role for active sleep at the dawn of consciousness?
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/0a0952984c504c09b01300c36f6d1c85
work_keys_str_mv	AT matthewnvandepoll balancingpredictionandsurprisearoleforactivesleepatthedawnofconsciousness AT brunovanswinderen balancingpredictionandsurprisearoleforactivesleepatthedawnofconsciousness
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Balancing Prediction and Surprise: A Role for Active Sleep at the Dawn of Consciousness?

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