TY - JOUR
T1 - Motivational tuning of fronto-subthalamic connectivity facilitates control of action impulses
AU - Herz, Damian M.
AU - Christensen, Mark S.
AU - Bruggemann, Norbert
AU - Hulme, Oliver J.
AU - Richard Ridderinkhof, K.
AU - Madsen, Kristoffer H.
AU - Siebner, Hartwig R.
PY - 2014/1/1
Y1 - 2014/1/1
N2 - It is critical for survival to quickly respond to environmental stimuli with the most appropriate action. This task becomes most challenging when response tendencies induced by relevant and irrelevant stimulus features are in conflict, and have to be resolved in real time. Inputs from the pre-supplementary motor area (pre-SMA) and inferior frontal gyrus (IFG) to the subthalamic nucleus (STN) are thought to support this function, but the connectivity and causality of these regions in calibrating motor control has not been delineated. In this study, we combined off-line noninvasive brain stimulation and functional magnetic resonance imaging, while young healthy human participants performed a modified version of the Simon task. We show that impairing pre-SMA function by noninvasive brain stimulation improved control over impulsive response tendencies, but only when participants were explicitly rewarded for fast and accurate responses. These effects were mediated by enhanced activation and connectivity of the IFG-STN pathway. These results provide causal evidence for a pivotal role of the IFG-STN pathway during action control. Additionally, they suggest a parallel rather than hierarchical organization of the pre-SMA-STN and IFG-STN pathways, since interruption of pre-SMA function can enhance IFG-STN connectivity and improve control over inappropriate responses.
AB - It is critical for survival to quickly respond to environmental stimuli with the most appropriate action. This task becomes most challenging when response tendencies induced by relevant and irrelevant stimulus features are in conflict, and have to be resolved in real time. Inputs from the pre-supplementary motor area (pre-SMA) and inferior frontal gyrus (IFG) to the subthalamic nucleus (STN) are thought to support this function, but the connectivity and causality of these regions in calibrating motor control has not been delineated. In this study, we combined off-line noninvasive brain stimulation and functional magnetic resonance imaging, while young healthy human participants performed a modified version of the Simon task. We show that impairing pre-SMA function by noninvasive brain stimulation improved control over impulsive response tendencies, but only when participants were explicitly rewarded for fast and accurate responses. These effects were mediated by enhanced activation and connectivity of the IFG-STN pathway. These results provide causal evidence for a pivotal role of the IFG-STN pathway during action control. Additionally, they suggest a parallel rather than hierarchical organization of the pre-SMA-STN and IFG-STN pathways, since interruption of pre-SMA function can enhance IFG-STN connectivity and improve control over inappropriate responses.
UR - http://www.scopus.com/inward/record.url?scp=84894429297&partnerID=8YFLogxK
U2 - 10.1523/JNEUROSCI.4081-13.2014
DO - 10.1523/JNEUROSCI.4081-13.2014
M3 - Journal articles
C2 - 24573279
AN - SCOPUS:84894429297
SN - 0270-6474
VL - 34
SP - 3210
EP - 3217
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 9
ER -