No cognitive processing in the unconscious, anesthetic-like, state of sleep

Abstract

We review evidence challenging the hypothesis that memories are processed or consolidated in sleep. We argue that the brain is in an unconscious state in sleep, akin to general anesthesia (GA), and hence is incapable of meaningful cognitive processing-the sole purview of waking consciousness. At minimum, the encoding of memories in sleep would require that waking events are faithfully transferred to and reproduced in sleep. Remarkably, however, this has never been demonstrated, as waking experiences are never truly replicated in sleep but rather appear in very altered or distorted forms. General anesthetics (GAs) exert their effects through endogenous sleep-wake control systems and accordingly GA and sleep share several common features: sensory blockade, immobility, amnesia and lack of awareness (unconsciousness). The loss of consciousness in non-REM (NREM) sleep or to GAs is characterized by: (a) delta oscillations throughout the cortex; (b) marked reductions in neural activity (from waking) over widespread regions of the cortex, most pronounced in frontal and parietal cortices; and (c) a significant disruption of the functional connectivity of thalamocortical and corticocortical networks, particularly those involved in "higher order" cognitive functions. Several (experimental) reports in animals and humans have shown that disrupting the activity of the cortex, particularly the orbitofrontal cortex, severely impairs higher order cognitive and executive functions. The profound and widespread deactivation of the cortex in the unconscious states of NREM sleep or GA would be expected to produce an equivalent, or undoubtedly a much greater, disruptive effect on mnemonic and cognitive functions. In conclusion, we contend that the unconscious, severely altered state of the brain in NREM sleep would negate any possibility of cognitive processing in NREM sleep.

Keywords: cognition; consciousness; functional connectivity; general anesthetics; memory; non-REM sleep; prefrontal cortex.

Figure 1

Locations of waking/arousal-related cell groups of the brainstem and caudal diencephalon at which general anesthetics (GAs) exert anesthetic actions. They include the pontomesencephalic reticular formation (PRF), locus coeruleus (LC), parabrachial nucleus (PB), tuberomammillary nucleus (TMN) and orexin-containing cells of the lateral hypothalamus (LHy). Abbreviations: 3V, third ventricle; AQ, cerebral aqueduct; CMT, central medial thalamic nucleus; DR, dorsal raphe nucleus; fx, fornix; LD, laterodorsal nucleus of the thalamus; LDT, laterodorsal tegmental nucleus; LGN, lateral geniculate nucleus of the thalamus; LP, lateral posterior nucleus of thalamus; MD, mediodorsal nucleus of thalamus; ml, medial lemniscus; MR, median raphe nucleus; PAG, periaqueductal gray; PH, posterior hypothalamus; PSV, principal sensory nucleus of trigeminal nerve; PV, paraventricular nucleus of thalamus; RE, nucleus reuniens of thalamus; RF, reticular formation; RM, raphe magnus, RPC, reticularis pontis caudalis; RT, reticular nucleus of thalamus; V, motor nucleus of trigeminal nerve; VB, ventrobasal complex of thalamus; VM, ventromedial nucleus of thalamus; VTN, ventral tegmental nucleus; ZI, zona incerta.

Figure 2

Locations of NREM sleep “centers” of the basal forebrain at which general anesthetics (GAs) exert anesthetic actions. They include the ventral lateral preoptic area (VLPO), the median preoptic area (MnPO), the supraoptic nucleus (SON) and the para-SON area. Abbreviations: 3V, third ventricle; aco, anterior commissure; AHN, anterior hypothalamus; BST, bed nucleus of stria terminalis; fx, fornix; LHy, lateral hypothalamus; LPO, lateral preoptic area; MPN, medial preoptic nucleus; MPO; medial preoptic area; och, optic chiasm; opt, optic tract; PVh, paraventricular nucleus of hypothalamus; sm, stria medullaris.