Theoretical reviewDoes abnormal non-rapid eye movement sleep impair declarative memory consolidation?: Disturbed thalamic functions in sleep and memory processing
Introduction
Sleep and memory researchers have extensively investigated sleep processes and their consolidating effects on memory. Many studies focused on the role of rapid-eye movement (REM) sleep in cognitive procedural memory.1 More recently, non-rapid eye movement (NREM) sleep has garnered support for its role in hippocampus-based declarative memory consolidation in humans. Although significant advances have been made in understanding the mechanism driving sleep-dependent memory consolidation, it remains unclear as to what occurs when that mechanism becomes dysfunctional. This paper attempts to take an in depth look at the pathological processes underlying abnormal NREM sleep activity and its possible link to declarative memory impairment. A theoretical model is generated to explain the potential relationship between abnormal electroencephalogram activity found during NREM sleep and co-occurring declarative memory impairment, mediated by thalamocortical network dysfunction. Empirical findings from studies on patients with schizophrenia, Alzheimer’s disease, and fibromyalgia syndrome are utilized to provide substantial support for the proposed model. In addition, we explore the phenomena of disturbed sleep, which is prevalent within the aforementioned patient populations, and how it may be concomitant with, or a risk factor for declarative memory impairment. Before introducing our model a brief review of the significance of NREM sleep on declarative memory consolidation is provided. By reviewing the literature on this relatively new and rapidly growing area of interest, our hope is to stimulate new research in further investigating the possible association between abnormal sleep processes and memory impairment.
Section snippets
NREM sleep and declarative memory
NREM sleep has been established to play a significant role in restoration of physiological functions.2, 3 However, relatively recent within the history of sleep research it has been discovered to serve an additional and equally important function, that of memory consolidation. First, it is necessary to define NREM sleep based on the latest definition. It consists of three stages referred to as stages N1, N2, and N3.4 Stage N1 is characterized by low amplitude mixed frequency (4–7 Hz) activity,
Decreases in SWS and sleep spindle activity associated with declarative memory impairment
There is a growing body of evidence suggesting that memory deficits in a wide range of neuropsychiatric disorders may be related to problems with SWS and spindle functioning. Schizophrenia serves as a prime example. Individuals with schizophrenia present with symptoms of hallucinations, delusions, thought disorder, emotional flattening, and social withdrawal. The characterized neuropathology include dysfunctional inhibitory neuronal circuits, reduced cortical neuropil, and disproportionately
Thalamic functioning in sleep spindle generation and declarative memory consolidation
Describing the neurophysiologic mechanisms underlying the complex network between NREM sleep regulation and declarative memory consolidation may shed further light as to what may be happening during such network dysfunction. The thalamus, a key brain structure within this network, constitutes the main portion of the diencephalon and serves multiple functions including the relay of sensory information through the thalamocortical network to various parts of the neocortex. It contributes to the
Thalamic abnormalities associated with declarative memory impairment and sleep disturbances
Thalamic lesions contribute to deficits in explicit memory wherein the size of the lesion directly relates to long-term explicit memory performance.65 Furthermore, lesioning the anterior thalamus has resulted in direct and negative effects on neuronal integrity and learning.66 Thus, thalamic pathology concomitant with hippocampal dysfunction may provide a possible neurophysiologic basis for declarative memory impairment seen in specific populations.67 Co-occurring sleep disturbances would
Future research and implications
Studies should investigate the risk for declarative memory impairment in individuals within the general population who evidence similar abnormal EEG activity during NREM sleep as previously described. An important inquiry to be made is whether a natural disposition for shortened SWS and reduced spindle activity in a non-patient population can accurately predict poor declarative memory functioning. The previous investigations mentioned regarding age-related declines in NREM sleep activity and
Conclusion
Indeed, the significant role of NREM sleep in memory consolidation has been firmly established. However, theories on the sequelae of NREM sleep dysfunction within the neuropsychiatrically disordered population have been only a budding endeavor. Drawing from research conducted on patients with schizophrenia, AD, and FMS it is suggested that abnormal EEG activity during NREM sleep is, in part, associated with co-occurring declarative memory impairment and sleep disruption. Furthermore, structural
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2022, Brain Research BulletinCitation Excerpt :At the thalamic level, this rhythmic firing at delta frequency is derived from the intrinsic voltage-gated ion channels of thalamocortical neurons which promote bursting at delta frequencies when these neurons are hyperpolarized due to the withdrawal of excitatory neuromodulatory inputs and/or increased hyperpolarization from GABAergic neurons, especially from the thalamic reticular nucleus (Jahnsen and Llinas, 1984a, 1984b; Leresche et al., 1990; Lewis et al., 2015; Maquet et al., 1997; Soltesz et al., 1991; Steriade et al., 1993b; Uygun et al., 2022). One of the well-studied functions of SWA is its role in sleep-dependent memory consolidation (Lu and Goder, 2012; Marshall et al., 2006; Steriade and Timofeev, 2003; Walker, 2009). Studies showed that cortical SOs trigger the reactivation of temporarily-stored hippocampal memories in coordination with hippocampal sharp-wave ripples and sleep spindles, which will be reviewed in more detail in the later sections (Diekelmann and Born, 2010; Klinzing et al., 2019; Rasch and Born, 2013).
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Quantitative electroencephalogram measures in adult obstructive sleep apnea – Potential biomarkers of neurobehavioural functioning
2017, Sleep Medicine ReviewsCitation Excerpt :This compromised integrity and vulnerability of the PFC in OSA patients may manifest as altered sleep/wake EEG activity and consequential neurobehavioural dysfunction. It is possible that structural or functional changes in thalamocortical networks may also underlie altered EEG profiles in OSA by compromising the ability to generate specific EEG activity (such as slow oscillations or sleep spindles), resulting in impaired memory consolidation and poor sleep quality but data are lacking (for theoretical review, see Lu and Goder 2012 [101]). OSA and its associated sleep fragmentation and intermittent hypoxemia/hypercapnia may further exacerbate alterations in brain function and structure that naturally occur with ageing [102].
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