Aperiodic sleep networks promote memory consolidation

Abstract:

Hierarchical synchronization of sleep oscillations establishes communication pathways to support memory reactivation, transfer, and consolidation. From an information-theoretical perspective, oscillations constitute highly structured network states that provide limited information-coding capacity. Recent findings indicate that sleep oscillations occur in transient bursts that are interleaved with aperiodic network states, which were previously considered to be random noise. We argue that aperiodic activity exhibits unique and variable spatiotemporal patterns, providing an ideal information-rich neurophysiological substrate for imprinting new mnemonic patterns onto existing circuits. We discuss novel avenues in conceptualizing and quantifying aperiodic network states during sleep to further understand their relevance and interplay with sleep oscillations in support of memory consolidation.

Authors:

• Randolph F Helfrich

• Janna D Lendner

• Robert T Knight

Date: 2021

DOI: https://doi.org/10.1016/j.tics.2021.04.009

View PDF

Top–Down Attentional Modulation in Human Frontal Cortex: Differential Engagement during External and Internal Attention

Abstract:

Decades of electrophysiological research on top–down control converge on the role of the lateral frontal cortex in facilitating attention to behaviorally relevant external inputs. However, the involvement of frontal cortex in the top–down control of attention directed to the external versus internal environment remains poorly understood. To address this, we recorded intracranial electrocorticography while subjects directed their attention externally to tones and responded to infrequent target tones, or internally to their own thoughts while ignoring the tones. Our analyses focused on frontal and temporal cortices. We first computed the target effect, as indexed by the difference in high frequency activity (70–150 Hz) between target and standard tones. Importantly, we then compared the target effect between external and internal attention, reflecting a top–down attentional effect elicited by task demands, in each region of interest. Both frontal and temporal cortices showed target effects during external and internal attention, suggesting this effect is present irrespective of attention states. However, only the frontal cortex showed an enhanced target effect during external relative to internal attention. These findings provide electrophysiological evidence for top–down attentional modulation in the lateral frontal cortex, revealing preferential engagement with external attention.

Authors:

• Julia WY Kam

• Randolph F Helfrich

• Anne-Kristin Solbakk

• Tor Endestad

• Pål G Larsson

• Jack J Lin

• Robert T Knight

Date: 2020

DOI: https://doi.org/10.1093/cercor/bhaa262

View PDF

An electrophysiological marker of arousal level in humans

Abstract:

Deep non-rapid eye movement sleep (NREM) and general anesthesia with propofol are prominent states of reduced arousal linked to the occurrence of synchronized oscillations in the electroencephalogram (EEG). Although rapid eye movement (REM) sleep is also associated with diminished arousal levels, it is characterized by a desynchronized, ‘wake-like’ EEG. This observation implies that reduced arousal states are not necessarily only defined by synchronous oscillatory activity. Using intracranial and surface EEG recordings in four independent data sets, we demonstrate that the 1/f spectral slope of the electrophysiological power spectrum, which reflects the non-oscillatory, scale-free component of neural activity, delineates wakefulness from propofol anesthesia, NREM and REM sleep. Critically, the spectral slope discriminates wakefulness from REM sleep solely based on the neurophysiological brain state. Taken together, our findings describe a common electrophysiological marker that tracks states of reduced arousal, including different sleep stages as well as anesthesia in humans.

Authors:

• Janna D Lendner

• Randolph F Helfrich

• Bryce A Mander

• Luis Romundstad

• Jack J Lin

• Matthew P Walker

• Pal G Larsson

• Robert T Knight

Date: 2020

DOI: https://doi.org/10.7554/eLife.55092

View PDF

Slow wave-spindle coupling during sleep predicts language learning and associated oscillatory activity

Abstract:

Language is one of the most defining human capabilities, involving the coordination of brain networks that generalise the meaning of linguistic units of varying complexity. On a neural level, neocortical slow waves and thalamic spindles during sleep facilitate the reactivation of newly encoded memory traces, manifesting in distinct oscillatory activity during retrieval. However, it is currently unknown if the effect of sleep on memory extends to the generalisation of the mechanisms that subserve sentence comprehension. We address this question by analysing electroencephalogram data recorded from 36 participants during an artificial language learning task and an 8hr nocturnal sleep period. We found that a period of sleep was associated with increased alpha/beta synchronisation and improved behavioural performance. Cross-frequency coupling analyses also revealed that spindle-slow wave coupling predicted the consolidation of varying word order permutations, which was associated with distinct patterns of task-related oscillatory activity during sentence processing. Taken together, this study presents converging behavioural and neurophysiological evidence for a role of sleep in the consolidation of higher order language learning and associated oscillatory neuronal activity.

Authors:

• Zachariah R Cross

• Randolph F Helfrich

• Mark J Kohler

• Andrew W Corcoran

• Scott Coussens

• Lena Zou-Williams

• Matthias Schlesewsky

• M Gareth Gaskell

• Robert T Knight

• Ina Bornkessel-Schlesewsky

Date: 2020

DOI: https://doi.org/10.1101/2020.02.13.948539

View PDF

Neural entrainment and network resonance in support of top-down guided attention

Abstract:

Which neural mechanisms provide the functional basis of top-down guided cognitive control? Here we review recent evidence that suggest that the neural basis of attention is inherently rhythmic. In particular, we discuss two physical properties of self-sustained networks, namely entrainment and resonance, and how these shape the timescale of attentional control. Several recent findings revealed theta-band (3-8 Hz) dynamics in top-down guided behavior. These reports were paralleled by intracranial recordings, which implicated theta oscillations in the organization of functional attention networks. We discuss how the intrinsic network architecture shapes covert attentional sampling as well as overt behavior. Taken together, we posit that theta rhythmicity is an inherent feature of the attention network in support of top-down guided goal-directed behavior.

Authors:

• Randolph F Helfrich

• Assaf Breska

• Robert T Knight

Date: 2019

DOI: 10.1016/j.copsyc.2018.12.016

View PDF

Bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans

Abstract:

How are memories transferred from short-term to long-term storage? Systems-level memory consolidation is thought to be dependent on the coordinated interplay of cortical slow waves, thalamo-cortical sleep spindles and hippocampal ripple oscillations. However, it is currently unclear how the selective interaction of these cardinal sleep oscillations is organized to support information reactivation and transfer. Here, using human intracranial recordings, we demonstrate that the prefrontal cortex plays a key role in organizing the ripple-mediated information transfer during non-rapid eye movement (NREM) sleep. We reveal a temporally precise form of coupling between prefrontal slow-wave and spindle oscillations, which actively dictates the hippocampal-neocortical dialogue and information transfer. Our results suggest a model of the human sleeping brain in which rapid bidirectional interactions, triggered by the prefrontal cortex, mediate hippocampal activation to optimally time subsequent information transfer to the neocortex during NREM sleep.

Authors:

• Randolph F Helfrich

• Janna D Lendner

• Bryce A Mander

• Heriberto Guillen

• Michelle Paff

• Lilit Mnatsakanyan

• Sumeet Vadera

• Matthew P Walker

• Jack J Lin

• Robert T Knight

Date: 2019

DOI: https://doi.org/10.1038/s41467-019-11444-x

View PDF

Sleep as a potential biomarker of tau and β-amyloid burden in the human brain

Abstract:

Recent proposals suggest that sleep may be a factor associated with accumulation of two core pathological features of Alzheimer's disease (AD): tau and β-amyloid (Aβ). Here we combined PET measures of Aβ and tau, electroencephalogram sleep recordings, and retrospective sleep evaluations to investigate the potential utility of sleep measures in predicting in vivo AD pathology in male and female older adults. Regression analyses revealed that the severity of impaired slow oscillation-sleep spindle coupling predicted greater medial temporal lobe tau burden. Aβ burden was not associated with coupling impairment but instead predicted the diminished amplitude of <1 Hz slow-wave-activity, results that were statistically dissociable from each other. Additionally, comparisons of AD pathology and retrospective, self-reported changes in sleep duration demonstrated that changes in sleep across the lifespan can predict late-life Aβ and tau burden. Thus, quantitative and qualitative features of human sleep represent potential noninvasive, cost-effective, and scalable biomarkers (current and future forecasting) of AD pathology, and carry both therapeutic and public health implications.

Authors:

• Joseph R Winer

• Bryce A Mander

• Randolph F Helfrich

• Anne Maass

• Theresa M Harrison

• Suzanne L Baker

• Robert T Knight

• William J Jagust

• Matthew P Walker

Date: 2019

DOI: https://doi.org/10.1523/JNEUROSCI.0503-19.2019

View PDF