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

Abstract

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.

Experimentally induced active and quiet sleep engage non-overlapping transcriptional programs inDrosophila

“…While it is not evident how to study emotions in insects (but see [87]), it could be argued that arousal systems more generally are employed to detect prediction errors and thereby promote learning [88]. Thus, we and others have suggested that active sleep might be crucial for optimizing prediction, and attention, and learning [2,67,89], and this may involve different kinds of homeostatic mechanisms centered on brain circuits rather than cells. Our finding that dFB-induced active sleep in Drosophila upregulates different nAchRa subunits is consistent with new findings that these subunits regulate appetitive memories in flies [90] and that cholinergic systems more generally underpin learning and memory in this animal [91].…”

“…Henceforth, we call this 'quiet' sleep, in contrast to the 'active' sleep that seems to be engaged by dFB activation [2,10]. Notably, calcium imaging of spontaneous sleep bouts in Drosophila also revealed active and quiet sleep stages [10], suggesting that both of our experimental approaches are physiologically relevant.…”

“…This suggests that different sleep stages, such as rapid eye movement (REM) and slow-wave sleep (SWS) in humans and other mammals [3] are accomplishing distinct functions that are nevertheless collectively important for adaptive behavior and survival [4]. While REM and SWS appear to be restricted to a subset of vertebrates (e.g., mammals, birds, and possibly some reptiles [5][6][7] a broader range of animals, including invertebrates, demonstrate evidence of 'active' versus 'quiet' sleep, which could represent evolutionary antecedents of REM and SWS, respectively [1,2,8]. During active sleep, although animals are less responsive, brain recordings reveal a level of neural activity that is similar to wakefulness, in contrast to quiet sleep, which is characterized by significantly decreased neural activity in invertebrates [9,10] as well as certain fish [11], mollusks [12], and reptiles [6].…”

“…This suggests that different sleep stages, such as rapid eye movement (REM) and slow-wave sleep (SWS) in humans and other mammals [3] are accomplishing distinct functions that are nevertheless collectively important for adaptive behavior and survival [4]. While REM and SWS appear to be restricted to a subset of vertebrates (e.g., mammals, birds, and possibly some reptiles [5][6][7] a broader range of animals, including invertebrates, demonstrate evidence of 'active' versus 'quiet' sleep [1,2,8]. Whether active and quiet sleep represent evolutionary antecedents of REM and SWS, respectively, remains speculative [1,2].…”

Диагностические Возможности Анализа Сновидений: Теоретические Предпосылки И Методические Подходы

“…Несмотря на некоторое сходство переживаемых в сновидении событий с реальностью у спящего снижается волевая активность и произвольный контроль над собой и происходящими событиями (Nir & Tononi, 2010). Отсутствие самоконтроля во время сна может быть связано со снижением активности таких областей мозга, как нижняя теменная, орбитофронтальная, дорсолатеральная и префронтальная кора (Van De Poll & van Swinderen, 2021;Vertes & Linley, 2021). Действительно, было показано, что снижение активности в префронтальной области коры во время сенсорного восприятия в бодрствовании сопровождалось снижением самосознания (Yang & Lewis, 2021;Kim et al, 2022).…”