Ramping dynamics and theta oscillations reflect dissociable signatures during rule-guided human behavior

abstract:

Contextual cues and prior evidence guide human goal-directed behavior. The neurophysiological mechanisms that implement contextual priors to guide subsequent actions in the human brain remain unclear. Using intracranial electroencephalography (iEEG), we demonstrate that increasing uncertainty introduces a shift from a purely oscillatory to a mixed processing regime with an additional ramping component. Oscillatory and ramping dynamics reflect dissociable signatures, which likely differentially contribute to the encoding and transfer of different cognitive variables in a cue-guided motor task. The results support the idea that prefrontal activity encodes rules and ensuing actions in distinct coding subspaces, while theta oscillations synchronize the prefrontal-motor network, possibly to guide action execution. Collectively, our results reveal how two key features of large-scale neural population activity, namely continuous ramping dynamics and oscillatory synchrony, jointly support rule-guided human behavior.

Authors:

• Jan Weber

• Anne-Kristin Solbakk

• Alejandro O. Blenkmann

• Anais Llorens

• Ingrid Funderud

• Sabine Leske

• Pål Gunnar Larsson

• Lugoslav Ivanovic

• Robert T. Knight

• Tor Endestad

• Randolph F. Helfrich

Date: 2024

DOI: https://doi.org/10.1038/s41467-023-44571-7

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Periodic attention deficits after frontoparietal lesions provide causal evidence for rhythmic attentional sampling

Abstract:

Contemporary models conceptualize spatial attention as a blinking spotlight that sequentially samples visual space. Hence, behavior fluctuates over time, even in states of presumed ‘‘sustained’’ attention. Recent evidence has suggested that rhythmic neural activity in the frontoparietal network constitutes the functional basis of rhythmic attentional sampling. However, causal evidence to support this notion remains absent. Using a lateralized spatial attention task, we addressed this issue in patients with focal lesions in the frontoparietal attention network. Our results revealed that frontoparietal lesions introduce periodic attention deficits, i.e., temporally specific behavioral deficits that are aligned with the underlying neural oscillations. Attention guided perceptual sensitivity was on par with that of healthy controls during optimal phases but was attenuated during the less excitable sub-cycles. Theta-dependent sampling (3–8 Hz) was causally dependent on the prefrontal cortex, while high-alpha/low-beta sampling (8–14 Hz) emerged from parietal areas. Collectively, our findings reveal that lesion-induced high-amplitude, low-frequency brain activity is not epiphenomenal but has immediate behavioral consequences. More generally, these results provide causal evidence for the hypothesis that the functional architecture of attention is inherently rhythmic.

Authors:

• Isabel Raposo

• Sara M. Szczepanski

• Kathleen Haaland

• Tor Endestad

• Anne-Kristin Solbakk

• Robert T. Knight

• Randolph F. Helfrich

Date: 2023

DOI: https://doi.org/10.1016/j.cub.2023.09.065

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Human REM sleep recalibrates neural activity in support of memory formation

Abstract:

The proposed mechanisms of sleep-dependent memory consolidation involve the overnight regulation of neural activity at both synaptic and whole-network levels. Now, there is a lack of in vivo data in humans elucidating if, and how, sleep and its varied stages balance neural activity, and if such recalibration benefits memory. We combined electrophysiology with in vivo two-photon calcium imaging in rodents as well as intracranial and scalp electroencephalography (EEG) in humans to reveal a key role for non-oscillatory brain activity during rapid eye movement (REM) sleep to mediate sleep-dependent recalibration of neural population dynamics. The extent of this REM sleep recalibration predicted the success of overnight memory consolidation, expressly the modulation of hippocampal—neocortical activity, favoring remembering rather than forgetting. The findings describe a non-oscillatory mechanism how human REM sleep modulates neural population activity to enhance long-term memory.

Authors:

• Janna D. Lendner

• Niels Niethard

• Bryce A. Mander

• Frank J. van Schalkwijk

• Sigrid Schuh-Hofer

• Hannah Schmidt

• Robert T. Knight

• Jan Born

• Matthew P. Walker

• Jack J. Lin

• Randolph F. Helfrich

Date: 2023

DOI: DOI: 10.1126/sciadv.adj1895

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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

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Neural mechanisms of sustained attention are rhythmic

ABSTRACT

Classic models of attention suggest that sustained neural firing constitutes a neural correlate of sustained attention. However, recent evidence indicates that behavioral performance fluctuates over time, exhibiting temporal dynamics that closely resemble the spectral features of ongoing, oscillatory brain activity. Therefore, it has been proposed that periodic neuronal excitability fluctuations might shape attentional allocation and overt behavior. However, empirical evidence to support this notion is sparse. Here, we address this issue by examining data from large-scale subdural recordings, using two different attention tasks that track perceptual ability at high temporal resolution. Our results reveal that perceptual outcome varies as a function of the theta phase even in states of sustained spatial attention. These effects were robust at the single-subject level, suggesting that rhythmic perceptual sampling is an inherent property of the frontoparietal attention network. Collectively, these findings support the notion that the functional architecture of top-down attention is intrinsically rhythmic.

AUTHORS

• Randolph F. Helfrich

• Ian C. Fiebelkorn

• Sara M. Szczepanski

• Jack J. Lin

• Josef Parvizi

• Robert T. Knight

• Sabine Kastner

Date: 2018

DOI: 10.1016/j.neuron.2018.07.032

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Human in vivo tau pathology, impaired NREM sleep oscillations and memory decline in aging

Abstract:

Aging disrupts sleep. Moreover, these sleep impairments are exaggerated in Alzheimer’s disease, and are proposed to contribute to cognitive decline. Recent human studies have linked β-amyloid with non-rapid eye-movement (NREM) sleep disruption. However, the impact of tau pathology on human sleep oscillations and cognition remains uninvestigated. Here, we tested the hypothesis that tau burden within medial temporal lobe (MTL) impairs the coupled relationship between the two key NREM sleep oscillations—sleep spindles and slow waves, and their known support of hippocampal memory.

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: 2018

DOI: 10.1016/j.jalz.2018.06.2344

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Old brains come uncoupled in sleep: slow wave-spindle synchrony, brain atrophy, and forgetting

ABSTRACT

The coupled interaction between slow-wave oscillations and sleep spindles during non-rapid-eye-movement (NREM) sleep has been proposed to support memory consolidation. However, little evidence in humans supports this theory. Moreover, whether such dynamic coupling is impaired as a consequence of brain aging in later life, contributing to cognitive and memory decline, is unknown. Combining electroencephalography (EEG), structural MRI, and sleep-dependent memory assessment, we addressed these questions in cognitively normal young and older adults. Directional cross-frequency coupling analyses demonstrated that the slow wave governs a precise temporal coordination of sleep spindles, the quality of which predicts overnight memory retention. Moreover, selective atrophy within the medial frontal cortex in older adults predicted a temporal dispersion of this slow wave-spindle coupling, impairing overnight memory consolidation and leading to forgetting. Prefrontal-dependent deficits in the spatiotemporal coordination of NREM sleep oscillations therefore represent one pathway explaining age-related memory decline.

AUTHORS

• Randolph F. Helfrich

• Bryce A. Mander

• William J. Jagust

• Robert T. Knight

• Matthew P. Walker

Date: 2018

DOI: 10.1016/j.neuron.2017.11.020

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Prefrontal cortex modulates posterior alpha oscillations during top-down guided visual perception

ABSTRACT

Conscious visual perception is proposed to arise from the selective synchronization of functionally specialized but widely distributed cortical areas. It has been suggested that different frequency bands index distinct canonical computations. Here, we probed visual perception on a fine-grained temporal scale to study the oscillatory dynam- ics supporting prefrontal-dependent sensory processing. We tested whether a predictive context that was embedded in a rapid visual stream modulated the perception of a subsequent near-threshold target. The rapid stream was presented either rhythmically at 10 Hz, to entrain parietooccipital alpha oscillations, or arrhythmically. We identified a 2- to 4-Hz delta signature that modulated posterior alpha activity and behavior during predictive trials. Importantly, delta-mediated top-down control diminished the behavioral effects of bottom-up alpha entrainment. Simultaneous source-reconstructed EEG and cross-frequency directionality analyses revealed that this delta activity originated from prefrontal areas and modulated posterior alpha power. Taken together, this study presents converging behavioral and electrophysiological evidence for frontal delta-mediated top-down control of posterior alpha activity, selectively facilitating visual perception.

AUTHORS

• Randolph F. Helfrich

• Melody Huang

• Guy Wilson

• Robert T. Knight

Date: 2017

DOI: 10.1073/pnas.1705965114

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Oscillatory Dynamics of Prefrontal Cognitive Control

ABSTRACT

The prefrontal cortex (PFC) provides the structural basis for numerous higher cognitive functions. However, it is still largely unknown which mechanisms provide the functional basis for flexible cognitive control of goal-directed behavior. Here, we review recent findings that suggest that the functional architecture of cognition is profoundly rhythmic and propose that the PFC serves as a conductor to orchestrate task-relevant large-scale networks. We highlight several studies that demonstrated that oscillatory dynamics, such as phase resetting, cross-frequency coupling (CFC), and entrainment, support PFC-dependent recruitment of task-relevant regions into coherent functional networks. Importantly, these findings support the notion that distinct spectral signatures reflect different cortical computations supporting effective multiplexing on different temporal channels along the same anatomical pathways.

AUTHORS

• Randolph Helfrich

• Robert T. Knight

Date: 2016

DOI: dx.doi.org/10.1016/j.tics.2016.09.007

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