Visual thalamocortical mechanisms of waking state-dependent activity and alpha oscillations

Nestvogel, Dennis; McCormick, David A.

doi:10.1016/j.neuron.2021.10.005

Cited by 61 publications

(99 citation statements)

References 84 publications

(126 reference statements)

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“…The low-frequency regime referred to in rodent work (2–10 Hz; e.g., McGinley et al, 2015b ) includes activity that shares characteristics with human alpha rhythms (3–6 Hz; e.g., Nestvogel and McCormick, 2022 ; Senzai et al, 2019 ). The human equivalent however clearly separates from activity in lower frequency bands and, here, showed idiosyncratic relationships with pupil-linked arousal.…”

Section: Discussionmentioning

confidence: 99%

“…This short-lag positive correlation may stem from interactions between the LC and regions of the thalamus ( McCormick, 1989 ; McCormick et al, 1991 ; Stitt et al, 2018 ), in particular those implicated in the generation of occipital alpha-band activity via thalamo-cortical feedback loops (e.g., the pulvinar; Saalmann et al, 2012 ). These loops may therefore be sensitive to noradrenergic ( Dahl et al, 2022 ) or even BF regulated cholinergic modulation ( Nestvogel and McCormick, 2022 ; Zagha and McCormick, 2014 ). Both scenarios posit indirect multi-synaptic routes to the neuromodulation of alpha activity that may delay the lag relative to other effects and put it closer to the time of maximum pupil dilation.…”

Section: Discussionmentioning

confidence: 99%

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Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing

Pfeffer

Keitel

Kluger

et al. 2022

eLife

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Fluctuations in arousal, controlled by subcortical neuromodulatory systems, continuously shape cortical state, with profound consequences for information processing. Yet, how arousal signals influence cortical population activity in detail has so far only been characterized for a few selected brain regions. Traditional accounts conceptualize arousal as a homogeneous modulator of neural population activity across the cerebral cortex. Recent insights, however, point to a higher specificity of arousal effects on different components of neural activity and across cortical regions. Here, we provide a comprehensive account of the relationships between fluctuations in arousal and neuronal population activity across the human brain. Exploiting the established link between pupil size and central arousal systems, we performed concurrent magnetoencephalographic (MEG) and pupillographic recordings in a large number of participants, pooled across three laboratories. We found a cascade of effects relative to the peak timing of spontaneous pupil dilations: Decreases in low-frequency (2-8 Hz) activity in temporal and lateral frontal cortex, followed by increased high-frequency (>64 Hz) activity in mid-frontal regions, followed by monotonic and inverted-U relationships with intermediate frequency-range activity (8-32 Hz) in occipito-parietal regions. Pupil-linked arousal also coincided with widespread changes in the structure of the aperiodic component of cortical population activity, indicative of changes in the excitation-inhibition balance in underlying microcircuits. Our results provide a novel basis for studying the arousal modulation of cognitive computations in cortical circuits.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing

Pfeffer

Keitel

Kluger

et al. 2022

eLife

View full text Add to dashboard Cite

show abstract

“…This short-lag positive correlation may stem from interactions between the locus coeruleus and regions of the thalamus (McCormick, 1989;McCormick et al, 1991;Stitt et al, 2018), in particular those implicated in the generation of occipital alpha-band activity via thalamocortical feedback loops (e.g., the Pulvinar; Saalmann et al, 2012). These loops may therefore be sensitive to noradrenergic (Dahl et al, 2022) or even basal-forebrain regulated cholinergic modulation (Nestvogel & McCormick, 2021;Zagha & McCormick, 2014). Both scenarios posit indirect multi-synaptic routes to the neuromodulation of alpha activity that may delay the lag relative to other effects and put it closer to the time of maximum pupil dilation.…”

Section: Arousal Modulates Cortical Activity Across Space Time and Frequenciesmentioning

confidence: 99%

Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing

Pfeffer

Keitel

Kluger

et al. 2021

Preprint

View full text Add to dashboard Cite

Fluctuations in arousal, controlled by subcortical neuromodulatory systems, continuously shape cortical state, with profound consequences for information processing. Yet, how arousal signals influence cortical population activity in detail has only been characterized for a few selected brain regions so far. Traditional accounts conceptualize arousal as a homogeneous modulator of neural population activity across the cerebral cortex. Recent insights, however, point to a higher specificity of arousal effects on different components of neural activity and across cortical regions. Here, we provide a comprehensive account of the relationships between fluctuations in arousal and neuronal population activity across the human brain. Exploiting the established link between pupil size and central arousal systems, we performed concurrent magnetoencephalographic (MEG) and pupillographic recordings in a large number of participants, pooled across three laboratories. We found a cascade of effects relative to the peak timing of spontaneous pupil dilations: Decreases in low-frequency (2-8 Hz) activity in temporal and lateral frontal cortex, followed by increased high-frequency (>64 Hz) activity in mid-frontal regions, followed by linear and non-linear relationships with intermediate frequency-range activity (8-32 Hz) in occipito-parietal regions. The non-linearity resembled an inverted U-shape whereby intermediate pupil sizes coincided with maximum 8-32 Hz activity. Pupil-linked arousal also coincided with widespread changes in the structure of the aperiodic component of cortical population activity, indicative of changes in the excitation-inhibition balance in underlying microcircuits. Our results provide a novel basis for studying the arousal modulation of cognitive computations in cortical circuits.

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“…Although it is, to the best of our knowledge, the most detailed model of its kind created so far, it is only a first step. Future studies will further refine the thalamoreticular model to take into account newly observed cellular and synaptic properties (Li et al, 2020;Martinez-Garcia et al, 2020), and explore thalamoreticular contributions to other functions, such as attention and the generation of the alpha rhythm (Ahrens et al, 2015;Chen et al, 2016;Gu et al, 2021;Makinson and Huguenard, 2015;Nestvogel and McCormick, 2021), when considered in the broader context of the thalamocortical loop. Video 3: Transition from wakefulness-like states to simulated cortical UP and DOWN activity, with spindle-like oscillations appearing during the UP state (related to Fig.…”

Section: Simulating the Effects Of Neuromodulation On Thalamic And Re...mentioning

confidence: 99%

“…• Spontaneous in vivo-like activity, characterized by uncorrelated firing and low firing rates in TC and Rt cells (Born et al, 2021;Hartings et al, 2000;Nestvogel and McCormick, 2021).…”

Section: Validations At the Network Levelmentioning

confidence: 99%

Thalamic control of sensory enhancement and sleep spindle properties in a biophysical model of thalamoreticular microcircuitry

Iavarone

Simko

Shi

et al. 2022

Preprint

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Thalamoreticular circuitry is central to sensory processing, attention, and sleep, and is implicated in numerous brain disorders, but the cellular and synaptic mechanisms remain intractable. Therefore, we developed the first detailed microcircuit model of mouse thalamus and thalamic reticular nucleus that captures morphological and biophysical properties of ~14,000 neurons connected via ~6M synapses, and recreates biological synaptic and gap junction connectivity. Realistic spontaneous and evoked activity during wakefulness and sleep emerge allowing dissection of cellular and synaptic contributions. Computer simulations suggest that reticular inhibition shapes thalamic responses and cortex can drive frequency-selective thalamic enhancement during wakefulness, whereas in sleep, reticular inhibition and cortical UP-states can trigger thalamic bursts and spindles. Gap junctions and short-term synaptic plasticity underlie spindle properties such as waxing and waning, and neuromodulation influences the occurrence of spindles. The model is openly available to support testing hypotheses of thalamoreticular circuitry in normal brain function and in disease.

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Visual thalamocortical mechanisms of waking state-dependent activity and alpha oscillations

Cited by 61 publications

References 84 publications

Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing

Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing

Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing

Thalamic control of sensory enhancement and sleep spindle properties in a biophysical model of thalamoreticular microcircuitry

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