Anodal tDCS affects neuromodulatory effects of the norepinephrine system on superior frontal theta activity during response inhibition
Medial and superior frontal theta oscillations are important for response inhibition. The norepinephrine (NE) system has been shown to modulate these oscillations possibly via gain control mechanisms, which depend on the modulation of neuron membrane potentials. Because the latter are also modulated by tDCS, the interrelation of tDCS and NE effects on superior frontal theta band activity needs investigation. We test the hypothesis that anodal tDCS affects modulatory effects of the NE system on theta band activity during inhibitory control in superior frontal regions. Using EEG beamforming, theta band activity in the superior frontal gyrus (SFG) was integrated (correlated) with the pupil diameter data as an indirect index of NE activity. In a within-subject design, healthy participants completed a response inhibition task in two sessions in which they received 2 mA anodal tDCS over the vertex, or sham stimulation. There were no behavioral effects of anodal tDCS. Yet, tDCS affected correlations between SFG theta band activity time course and the pupil diameter time course. Correlations were evident after sham stimulation (r = .701; p < .004), but absent after anodal tDCS. The observed power of this dissociation was above 95%. The data suggest that anodal tDCS may eliminate neuromodulatory effects, likely of the NE system, on theta band activity during response inhibition in a structure of the response inhibition network. The NE system and tDCS seem to target similar mechanisms important for cognitive control in the prefrontal cortex. The results provide a hint why tDCS often fails to induce overt behavioral effects and shows that neurobiological systems, which may exert similar effects as tDCS on neural processes should closely be monitored in tDCS experiments.
KeywordsAnodal tDCS EEG Pupil diameter Norepinephrine system Beamforming Superior frontal gyrus
We thank all participants.
Compliance with ethical standards
There are no conflicts of interest. The study was approved by the IRB of the TU Dresden. Written informed consent was obtained from all subjects before any of the study’s procedures were commenced. This work was supported by Grants from the Deutsche Forschungsgemeinschaft (DFG) BE4045/26-1 and SFB 940 project B8 to C.B.
- Aston-Jones G, Cohen JD (2005) An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci 28:403–450. https://doi.org/10.1146/annurev.neuro.28.061604.135709 CrossRefGoogle Scholar
- Beste C, Ness V, Falkenstein M, Saft C (2011) On the role of fronto-striatal neural synchronization processes for response inhibition–evidence from ERP phase-synchronization analyses in pre-manifest Huntington’s disease gene mutation carriers. Neuropsychologia 49:3484–3493. https://doi.org/10.1016/j.neuropsychologia.2011.08.024 CrossRefGoogle Scholar
- Dippel G, Mückschel M, Ziemssen T, Beste C (2017) Demands on response inhibition processes determine modulations of theta band activity in superior frontal areas and correlations with pupillometry—implications for the norepinephrine system during inhibitory control. NeuroImage 157:575–585. https://doi.org/10.1016/j.neuroimage.2017.06.037 CrossRefGoogle Scholar
- Evans JD (1996) Straightforward statistics for the behavioral sciences. Brooks/Cole Publishing Company, Pacific GroveGoogle Scholar
- Naicker P, Anoopkumar-Dukie S, Grant GD et al (2016) Central cholinergic pathway involvement in the regulation of pupil diameter, blink rate and cognitive function. Neuroscience 334:180–190. https://doi.org/10.1016/j.neuroscience.2016.08.009 CrossRefGoogle Scholar