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Research Articles, Behavioral/Cognitive

Pharmacological Manipulations of Physiological Arousal and Sleep-Like Slow Waves Modulate Sustained Attention

Elaine Pinggal, Paul M. Dockree, Redmond G. O'Connell, Mark A. Bellgrove and Thomas Andrillon
Journal of Neuroscience 26 October 2022, 42 (43) 8113-8124; DOI: https://doi.org/10.1523/JNEUROSCI.0836-22.2022
Elaine Pinggal
1School of Psychological Sciences, Turner Institute for Brain and Mental Health, Monash University, Melbourne, Victoria 3168, Australia
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Paul M. Dockree
2Trinity College Institute of Neuroscience and School of Psychology, Trinity College Dublin, Dublin D02 PN40, Ireland
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Redmond G. O'Connell
2Trinity College Institute of Neuroscience and School of Psychology, Trinity College Dublin, Dublin D02 PN40, Ireland
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Mark A. Bellgrove
1School of Psychological Sciences, Turner Institute for Brain and Mental Health, Monash University, Melbourne, Victoria 3168, Australia
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Thomas Andrillon
3School of Philosophical, Historical, and International Studies, Centre for Consciousness and Contemplative Studies, Monash University, Melbourne, Victoria 3168, Australia
4Paris Brain Institute, Sorbonne Université, Institut National de la Santé et de la Recherche Médicale-Centre National de la Recherche Scientifique, Paris 75013, France
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Abstract

Sustained attention describes our ability to keep a constant focus on a given task. This ability is modulated by our physiological state of arousal. Although lapses of sustained attention have been linked with dysregulations of arousal, the underlying physiological mechanisms remain unclear. An emerging body of work proposes that the intrusion during wakefulness of sleep-like slow waves, a marker of the transition toward sleep, could mechanistically account for attentional lapses. This study aimed to expose, via pharmacological manipulations of the monoamine system, the relationship between the occurrence of sleep-like slow waves and the behavioral consequences of sustained attention failures. In a double-blind, randomized-control trial, 32 healthy human male participants received methylphenidate, atomoxetine, citalopram or placebo during four separate experimental sessions. During each session, electroencephalography (EEG) was used to measure neural activity while participants completed a visual task requiring sustained attention. Methylphenidate, which increases wake-promoting dopamine and noradrenaline across cortical and subcortical areas, improved behavioral performance whereas atomoxetine, which increases dopamine and noradrenaline predominantly over frontal cortices, led to more impulsive responses. Additionally, citalopram, which increases sleep-promoting serotonin, led to more missed trials. Based on EEG recording, citalopram was also associated with an increase in sleep-like slow waves. Importantly, compared with a classical marker of arousal such as α power, only slow waves differentially predicted both misses and faster responses in a region-specific fashion. These results suggest that a decrease in arousal can lead to local sleep intrusions during wakefulness which could be mechanistically linked to impulsivity and sluggishness.

SIGNIFICANCE STATEMENT We investigated whether the modulation of attention and arousal could not only share the same neuromodulatory pathways but also rely on similar neuronal mechanisms; for example, the intrusion of sleep-like activity within wakefulness. To do so, we pharmacologically manipulated noradrenaline, dopamine, and serotonin in a four-arm, randomized, placebo-controlled trial and examined the consequences on behavioral and electroencephalography (EEG) indices of attention and arousal. We showed that sleep-like slow waves can predict opposite behavioral signatures: impulsivity and sluggishness. Slow waves may be a candidate mechanism for the occurrence of attentional lapses since the relationship between slow-wave occurrence and performance is region-specific and the consequences of these local sleep intrusions are in line with the cognitive functions carried by the underlying brain regions.

  • arousal
  • attention
  • electroencephalography
  • neuromodulation
  • sleep
  • vigilance

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The Journal of Neuroscience: 42 (43)
Journal of Neuroscience
Vol. 42, Issue 43
26 Oct 2022
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Pharmacological Manipulations of Physiological Arousal and Sleep-Like Slow Waves Modulate Sustained Attention
Elaine Pinggal, Paul M. Dockree, Redmond G. O'Connell, Mark A. Bellgrove, Thomas Andrillon
Journal of Neuroscience 26 October 2022, 42 (43) 8113-8124; DOI: 10.1523/JNEUROSCI.0836-22.2022

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Pharmacological Manipulations of Physiological Arousal and Sleep-Like Slow Waves Modulate Sustained Attention
Elaine Pinggal, Paul M. Dockree, Redmond G. O'Connell, Mark A. Bellgrove, Thomas Andrillon
Journal of Neuroscience 26 October 2022, 42 (43) 8113-8124; DOI: 10.1523/JNEUROSCI.0836-22.2022
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Keywords

  • arousal
  • attention
  • electroencephalography
  • neuromodulation
  • sleep
  • vigilance

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