Repetitive transcranial magnetic stimulation over inferior frontal cortex impairs the suppression (but not expression) of action impulses during action conflict

Abstract

In the recent literature, the effects of noninvasive neurostimulation on cognitive functioning appear to lack consistency and replicability. We propose that such effects may be concealed unless dedicated, sensitive, and process-specific dependent measures are used. The expression and subsequent suppression of response capture are often studied using conflict tasks. Response-time distribution analyses have been argued to provide specific measures of the susceptibility to make fast impulsive response errors, as well as the proficiency of the selective suppression of these impulses. These measures of response capture and response inhibition are particularly sensitive to experimental manipulations and clinical deficiencies that are typically obfuscated in commonly used overall performance analyses. Recent work using structural and functional imaging techniques links these behavioral outcome measures to the integrity of frontostriatal networks. These studies suggest that the presupplementary motor area (pre-SMA) is linked to the susceptibility to response capture whereas the right inferior frontal cortex (rIFC) is associated with the selective suppression of action impulses. Here, we used repetitive transcranial magnetic stimulation (rTMS) to test the causal involvement of these two cortical areas in response capture and inhibition in the Simon task. Disruption of rIFC function specifically impaired selective suppression of conflicting action tendencies, whereas the anticipated increase of fast impulsive errors after perturbing pre-SMA function was not confirmed. These results provide a proof of principle of the notion that the selection of appropriate dependent measures is perhaps crucial to establish the effects of neurostimulation on specific cognitive functions.

Dynamics of cognitive control: Theoretical bases, paradigms, and a view for the future

“…An important caveat about using brain activation data to inform theories of cognitive control is that these data can only provide correlational rather than causal information. TMS and other methods that can interrupt or otherwise influence cortical activity can provide more specific evidence for causation (see van Campen, Kunert, van den Wildenberg, & Ridderinkhof, 2018). For example, Sauseng, Feldheim, Freunberger, and Hummel (2011) ran a combined EEG/ repetitive TMS study that supported the role of DAN in regulating posterior alpha as an information-gating mechanism.…”

Emerging themes in cognitive control: Commentary on the special issue of Psychophysiology entitled “Dynamics of Cognitive Control: A View Across Methodologies”

“…With regard to the neural underpinnings, Wessel ( ) cites work suggesting that an inhibition network consisting of regions of the presupplementary motor area, right inferior frontal gyrus, and subthalamic nucleus of the basal ganglia are involved in the disruption of behavior. Van Campen, Kunert, van den Wildenberg, & Ridderinkof ( ) present evidence using transcranial magnetic stimulation (TMS) of the critical role of right inferior frontal gyrus in the suppression of such action tendencies. The associated orienting response is thought to occur via locus coeruleus–noradrenergic input to right ventrolateral regions (Corbetta & Shulman, ) as well as the right anterior insular cortex.…”

Dynamics of cognitive control: A view across methodologies

“…Among the paradigms investigated are task switching (Baniqued, Low, Fletcher, Gratton, & Fabiani, ; Barceló & Cooper, ; Provost, Jamadar, Heathcote, Brown, & Karayanidis, ) , error processing ( Boudewyn & Carter, ; Coleman, Watson, & Strayer, ; Drollette et al, ), conflict tasks and conflict adaptation ( Janssens, De Loof, Boehler, Pourtois, & Verguts, 2018; van Campen, Kunert, van den Wildenberg, & Ridderinkhof, ; Von Gunten, Volpert‐Esmond, & Bartholow, ), and stop‐signal and go/no‐go tasks ( Grammer, Gehring, & Morrison, ; Wessel, ). The studies vary in the dependent variables used, including ERPs ( Barceló & Cooper, ; Coleman et al, ; Drollette et al, ; Grammer et al, ; Provost et al, ; Von Gunten et al, ; Wessel, ), oscillations ( Boudewyn & Carter, ; Janssens et al, ), optical imaging (the event‐related optical signal, EROS; Baniqued et al, ), and TMS ( van Campen et al, ). They also vary in the type of analyses used, including trial‐by‐trial variability and multilevel analysis ( Provost et al, ; van Campen et al, ; Von Gunten et al, ), intertask analysis ( Wessel, ), functional connectivity ( Baniqued et al, ), information theory ( Barceló & Cooper, 2018 ), speed‐accuracy instructions ( Coleman et al, ), learning ( Janssens et al, ), fitness intervention ( Drollette et al, ), and clinical and age groups ( Baniqued et al, ; Boudewyn & Carter, ; Drollette et al, ; Grammer et al, ).…”

“…The studies vary in the dependent variables used, including ERPs ( Barceló & Cooper, ; Coleman et al, ; Drollette et al, ; Grammer et al, ; Provost et al, ; Von Gunten et al, ; Wessel, ), oscillations ( Boudewyn & Carter, ; Janssens et al, ), optical imaging (the event‐related optical signal, EROS; Baniqued et al, ), and TMS ( van Campen et al, ). They also vary in the type of analyses used, including trial‐by‐trial variability and multilevel analysis ( Provost et al, ; van Campen et al, ; Von Gunten et al, ), intertask analysis ( Wessel, ), functional connectivity ( Baniqued et al, ), information theory ( Barceló & Cooper, 2018 ), speed‐accuracy instructions ( Coleman et al, ), learning ( Janssens et al, ), fitness intervention ( Drollette et al, ), and clinical and age groups ( Baniqued et al, ; Boudewyn & Carter, ; Drollette et al, ; Grammer et al, ). Together, these articles provide a complex matrix of new data that reflect the varied background and approaches taken by contemporary research on cognitive control.…”

“…The 11 empirical articles focus on different paradigms, measurements, and analytical approaches investigating cognitive control, with particular focus on its fast dynamics. Among the paradigms investigated are task switching (Baniqued, Low, Fletcher, Gratton, & Fabiani, 2018;Barcel o & Cooper, 2018;Provost, Jamadar, Heathcote, Brown, & Karayanidis, 2018), error processing (Boudewyn & Carter, 2018;Coleman, Watson, & Strayer, 2018;Drollette et al, 2018), conflict tasks and conflict adaptation (Janssens, De Loof, Boehler, Pourtois, & Verguts, 2018;van Campen, Kunert, van den Wildenberg, & Ridderinkhof, 2018;Von Gunten, Volpert-Esmond, & Bartholow, 2018), and stopsignal and go/no-go tasks (Grammer, Gehring, & Morrison, 2018;Wessel, 2018b). The studies vary in the dependent variables used, including ERPs (Barcel o & Cooper, 2018;Coleman et al, 2018;Drollette et al, 2018;Grammer et al, 2018;Provost et al, 2018;Von Gunten et al, 2018;Wessel, 2018b), oscillations (Boudewyn & Carter, 2018;Janssens et al, 2018), optical imaging (the event-related optical signal, EROS; Baniqued et al, 2018), and TMS (van Campen et al, 2018).…”