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Research Articles, Behavioral/Cognitive

Transcutaneous Vagus Nerve Stimulation in Humans Induces Pupil Dilation and Attenuates Alpha Oscillations

Omer Sharon, Firas Fahoum and Yuval Nir
Journal of Neuroscience 13 January 2021, 41 (2) 320-330; DOI: https://doi.org/10.1523/JNEUROSCI.1361-20.2020
Omer Sharon
1Department of Physiology and Pharmacology, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv-Yafo 69978, Israel
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Firas Fahoum
2Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv-Yafo 69978, Israel
3EEG and Epilepsy Unit, Department of Neurology, Tel Aviv Sourasky Medical Center, Tel Aviv-Yafo 64239, Israel
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Yuval Nir
1Department of Physiology and Pharmacology, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv-Yafo 69978, Israel
4Sagol School of Neuroscience, Tel Aviv-Yafo 69978, Israel
5Functional Neurophysiology and Sleep Research Laboratory, Sagol Brain Institute Tel Aviv, Tel-Aviv Sourasky Medical Center, Tel Aviv- Yafo 64239, Israel
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Abstract

Vagus nerve stimulation (VNS) is widely used to treat drug-resistant epilepsy and depression. While the precise mechanisms mediating its long-term therapeutic effects are not fully resolved, they likely involve locus coeruleus (LC) stimulation via the nucleus of the solitary tract, which receives afferent vagal inputs. In rats, VNS elevates LC firing and forebrain noradrenaline levels, whereas LC lesions suppress VNS therapeutic efficacy. Noninvasive transcutaneous VNS (tVNS) uses electrical stimulation that targets the auricular branch of the vagus nerve at the cymba conchae of the ear. However, the extent to which tVNS mimics VNS remains unclear. Here, we investigated the short-term effects of tVNS in healthy human male volunteers (n = 24), using high-density EEG and pupillometry during visual fixation at rest. We compared short (3.4 s) trials of tVNS to sham electrical stimulation at the earlobe (far from the vagus nerve branch) to control for somatosensory stimulation. Although tVNS and sham stimulation did not differ in subjective intensity ratings, tVNS led to robust pupil dilation (peaking 4–5 s after trial onset) that was significantly higher than following sham stimulation. We further quantified, using parallel factor analysis, how tVNS modulates idle occipital alpha (8–13Hz) activity identified in each participant. We found greater attenuation of alpha oscillations by tVNS than by sham stimulation. This demonstrates that tVNS reliably induces pupillary and EEG markers of arousal beyond the effects of somatosensory stimulation, thus supporting the hypothesis that tVNS elevates noradrenaline and other arousal-promoting neuromodulatory signaling, and mimics invasive VNS.

SIGNIFICANCE STATEMENT Current noninvasive brain stimulation techniques are mostly confined to modulating cortical activity, as is typical with transcranial magnetic or transcranial direct/alternating current electrical stimulation. Transcutaneous vagus nerve stimulation (tVNS) has been proposed to stimulate subcortical arousal-promoting nuclei, though previous studies yielded inconsistent results. Here we show that short (3.4 s) tVNS pulses in naive healthy male volunteers induced transient pupil dilation and attenuation of occipital alpha oscillations. These markers of brain arousal are in line with the established effects of invasive VNS on locus coeruleus–noradrenaline signaling, and support that tVNS mimics VNS. Therefore, tVNS can be used as a tool for studying how endogenous subcortical neuromodulatory signaling affects human cognition, including perception, attention, memory, and decision-making; and also for developing novel clinical applications.

  • alpha oscillations
  • EEG
  • noradrenaline
  • pupil
  • transcutaneous vagus nerve stimulation
  • tVNS

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The Journal of Neuroscience: 41 (2)
Journal of Neuroscience
Vol. 41, Issue 2
13 Jan 2021
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Transcutaneous Vagus Nerve Stimulation in Humans Induces Pupil Dilation and Attenuates Alpha Oscillations
Omer Sharon, Firas Fahoum, Yuval Nir
Journal of Neuroscience 13 January 2021, 41 (2) 320-330; DOI: 10.1523/JNEUROSCI.1361-20.2020

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Transcutaneous Vagus Nerve Stimulation in Humans Induces Pupil Dilation and Attenuates Alpha Oscillations
Omer Sharon, Firas Fahoum, Yuval Nir
Journal of Neuroscience 13 January 2021, 41 (2) 320-330; DOI: 10.1523/JNEUROSCI.1361-20.2020
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Keywords

  • alpha oscillations
  • EEG
  • noradrenaline
  • pupil
  • transcutaneous vagus nerve stimulation
  • tVNS

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