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Inhibitory control and error monitoring by human subthalamic neurons.

Bastin J, Polosan M, Benis D, Goetz L, Bhattacharjee M, Piallat B, Krainik A, Bougerol T, Chabardès S, David O - Transl Psychiatry (2014)

Bottom Line: Extracellular recordings revealed three functionally distinct neuronal populations: the first one fired selectively before and during motor responses, the second one selectively increased their firing rate during successful inhibitory control, and the last one fired selectively during error monitoring.Furthermore, we found that beta band activity (15-35 Hz) rapidly increased during correct and incorrect behavioral stopping.Taken together, our results provide critical electrophysiological support for the hypothesized role of the STN in the integration of motor and cognitive-executive control functions.

View Article: PubMed Central - PubMed

Affiliation: 1] Fonctions Cérébrales et Neuromodulation, Université Joseph Fourier, Grenoble, France [2] Grenoble Institut des Neurosciences, INSERM, U836, Grenoble, France.

ABSTRACT
The subthalamic nucleus (STN) has been shown to be implicated in the control of voluntary action, especially during tasks involving conflicting choice alternatives or rapid response suppression. However, the precise role of the STN during nonmotor functions remains controversial. First, we tested whether functionally distinct neuronal populations support different executive control functions (such as inhibitory control or error monitoring) even within a single subterritory of the STN. We used microelectrode recordings during deep brain stimulation surgery to study extracellular activity of the putative associative-limbic part of the STN while patients with severe obsessive-compulsive disorder performed a stop-signal task. Second, 2-4 days after the surgery, local field potential recordings of STN were used to test the hypothesis that STN oscillations may also reflect executive control signals. Extracellular recordings revealed three functionally distinct neuronal populations: the first one fired selectively before and during motor responses, the second one selectively increased their firing rate during successful inhibitory control, and the last one fired selectively during error monitoring. Furthermore, we found that beta band activity (15-35 Hz) rapidly increased during correct and incorrect behavioral stopping. Taken together, our results provide critical electrophysiological support for the hypothesized role of the STN in the integration of motor and cognitive-executive control functions.

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Subthalamic task-related LFP activity. (a) Trial-averaged time-frequency charts of a STN bipolar recording in a representative patient. Time origin indicates stop cue during SS and US trials and button press during GO trials. (b) Single-trial beta band power of a STN bipolar recording time-locked to stop cue during SS and US trials and to virtual stop cue during GO trials. (c) Grand average beta power time series (n=7 patients, 14 recorded STNs). (d) Beta band maximal power amplitude in the 500-ms period after stop (or virtual stop) cue. Vertical dashed orange line indicates the average latency at which the difference between SS and LMGO trials reached significance. Vertical dashed red line indicates SSRT. Stars indicate significant differences between trial types (post hoc Tukey, P<0.05). LFP, local field potential; LMGO, latency-matched GO; SS, successful stop trial; SSRT, stop-signal reaction time; STN, subthalamic nucleus; US, unsuccessful stop trial.
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fig5: Subthalamic task-related LFP activity. (a) Trial-averaged time-frequency charts of a STN bipolar recording in a representative patient. Time origin indicates stop cue during SS and US trials and button press during GO trials. (b) Single-trial beta band power of a STN bipolar recording time-locked to stop cue during SS and US trials and to virtual stop cue during GO trials. (c) Grand average beta power time series (n=7 patients, 14 recorded STNs). (d) Beta band maximal power amplitude in the 500-ms period after stop (or virtual stop) cue. Vertical dashed orange line indicates the average latency at which the difference between SS and LMGO trials reached significance. Vertical dashed red line indicates SSRT. Stars indicate significant differences between trial types (post hoc Tukey, P<0.05). LFP, local field potential; LMGO, latency-matched GO; SS, successful stop trial; SSRT, stop-signal reaction time; STN, subthalamic nucleus; US, unsuccessful stop trial.

Mentions: For each patient and each hemisphere, we analyzed task-related LFP changes of the pair of adjacent contacts that showed the largest BBA across SS, US and GO trials. LFP responses were characterized by an increase of BBA during correct stopping whereas BBA decreased around motor execution during GO trials (Figure 5a). A single-trial analysis showed that the BBA increase during SS trials was highly reproducible across stop trials (Figure 5b). Grand average (n=14 bipolar recordings) of beta activity confirmed its significant increase during SS and during US as compared with LMGO trials (50% slower GO trials—LMGO trials), in a 500 ms period following the STOP cue or virtual STOP cue (Figure 5c, analysis of variance, F(2,26)=6.1, P=0.0068 and Tukey post hoc tests P<0.05).


Inhibitory control and error monitoring by human subthalamic neurons.

Bastin J, Polosan M, Benis D, Goetz L, Bhattacharjee M, Piallat B, Krainik A, Bougerol T, Chabardès S, David O - Transl Psychiatry (2014)

Subthalamic task-related LFP activity. (a) Trial-averaged time-frequency charts of a STN bipolar recording in a representative patient. Time origin indicates stop cue during SS and US trials and button press during GO trials. (b) Single-trial beta band power of a STN bipolar recording time-locked to stop cue during SS and US trials and to virtual stop cue during GO trials. (c) Grand average beta power time series (n=7 patients, 14 recorded STNs). (d) Beta band maximal power amplitude in the 500-ms period after stop (or virtual stop) cue. Vertical dashed orange line indicates the average latency at which the difference between SS and LMGO trials reached significance. Vertical dashed red line indicates SSRT. Stars indicate significant differences between trial types (post hoc Tukey, P<0.05). LFP, local field potential; LMGO, latency-matched GO; SS, successful stop trial; SSRT, stop-signal reaction time; STN, subthalamic nucleus; US, unsuccessful stop trial.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4203004&req=5

fig5: Subthalamic task-related LFP activity. (a) Trial-averaged time-frequency charts of a STN bipolar recording in a representative patient. Time origin indicates stop cue during SS and US trials and button press during GO trials. (b) Single-trial beta band power of a STN bipolar recording time-locked to stop cue during SS and US trials and to virtual stop cue during GO trials. (c) Grand average beta power time series (n=7 patients, 14 recorded STNs). (d) Beta band maximal power amplitude in the 500-ms period after stop (or virtual stop) cue. Vertical dashed orange line indicates the average latency at which the difference between SS and LMGO trials reached significance. Vertical dashed red line indicates SSRT. Stars indicate significant differences between trial types (post hoc Tukey, P<0.05). LFP, local field potential; LMGO, latency-matched GO; SS, successful stop trial; SSRT, stop-signal reaction time; STN, subthalamic nucleus; US, unsuccessful stop trial.
Mentions: For each patient and each hemisphere, we analyzed task-related LFP changes of the pair of adjacent contacts that showed the largest BBA across SS, US and GO trials. LFP responses were characterized by an increase of BBA during correct stopping whereas BBA decreased around motor execution during GO trials (Figure 5a). A single-trial analysis showed that the BBA increase during SS trials was highly reproducible across stop trials (Figure 5b). Grand average (n=14 bipolar recordings) of beta activity confirmed its significant increase during SS and during US as compared with LMGO trials (50% slower GO trials—LMGO trials), in a 500 ms period following the STOP cue or virtual STOP cue (Figure 5c, analysis of variance, F(2,26)=6.1, P=0.0068 and Tukey post hoc tests P<0.05).

Bottom Line: Extracellular recordings revealed three functionally distinct neuronal populations: the first one fired selectively before and during motor responses, the second one selectively increased their firing rate during successful inhibitory control, and the last one fired selectively during error monitoring.Furthermore, we found that beta band activity (15-35 Hz) rapidly increased during correct and incorrect behavioral stopping.Taken together, our results provide critical electrophysiological support for the hypothesized role of the STN in the integration of motor and cognitive-executive control functions.

View Article: PubMed Central - PubMed

Affiliation: 1] Fonctions Cérébrales et Neuromodulation, Université Joseph Fourier, Grenoble, France [2] Grenoble Institut des Neurosciences, INSERM, U836, Grenoble, France.

ABSTRACT
The subthalamic nucleus (STN) has been shown to be implicated in the control of voluntary action, especially during tasks involving conflicting choice alternatives or rapid response suppression. However, the precise role of the STN during nonmotor functions remains controversial. First, we tested whether functionally distinct neuronal populations support different executive control functions (such as inhibitory control or error monitoring) even within a single subterritory of the STN. We used microelectrode recordings during deep brain stimulation surgery to study extracellular activity of the putative associative-limbic part of the STN while patients with severe obsessive-compulsive disorder performed a stop-signal task. Second, 2-4 days after the surgery, local field potential recordings of STN were used to test the hypothesis that STN oscillations may also reflect executive control signals. Extracellular recordings revealed three functionally distinct neuronal populations: the first one fired selectively before and during motor responses, the second one selectively increased their firing rate during successful inhibitory control, and the last one fired selectively during error monitoring. Furthermore, we found that beta band activity (15-35 Hz) rapidly increased during correct and incorrect behavioral stopping. Taken together, our results provide critical electrophysiological support for the hypothesized role of the STN in the integration of motor and cognitive-executive control functions.

Show MeSH
Related in: MedlinePlus