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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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(a) Localization of DBS electrodes contacts on axial and coronal MRI sections of a patient. (b) Microelectrode STN recording and mean waveform (black)±s.d. (gray) of the isolated spike cluster. (c) Stop-signal task. Participants were instructed to respond as fast as they can to the GO cue and to withhold their response when a stop signal occurs. Task difficulty during STOP trials was adjusted by shortening or lengthening the delay between GO and STOP cues (stop-signal delay, SSD) after unsuccessful or successful STOP trials. After each trial, positive and negative feedback was presented for 1 s (see Materials and Methods). CD, caudate nucleus; DBS, deep brain stimulation; GP, globus pallidus; MRI, magnetic resonance imaging; RN, red nucleus; SN, substantia nigra; STN, subthalamic nucleus.
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fig1: (a) Localization of DBS electrodes contacts on axial and coronal MRI sections of a patient. (b) Microelectrode STN recording and mean waveform (black)±s.d. (gray) of the isolated spike cluster. (c) Stop-signal task. Participants were instructed to respond as fast as they can to the GO cue and to withhold their response when a stop signal occurs. Task difficulty during STOP trials was adjusted by shortening or lengthening the delay between GO and STOP cues (stop-signal delay, SSD) after unsuccessful or successful STOP trials. After each trial, positive and negative feedback was presented for 1 s (see Materials and Methods). CD, caudate nucleus; DBS, deep brain stimulation; GP, globus pallidus; MRI, magnetic resonance imaging; RN, red nucleus; SN, substantia nigra; STN, subthalamic nucleus.

Mentions: The SST was used to experimentally dissociate motor action, stopping and error-monitoring signals.1,24,25 It consisted of the random presentation of two trial types (Figure 1c). During GO trials (67% of trials), an imperative GO cue prompted patients to quickly press a button with the right index. During STOP trials (33% of trials), patients were asked to withhold the planned movement. To investigate the hypothesized ‘braking function' of STN neurons during response selection, we contrasted successful stop trials (SS) with GO trials. To isolate error monitoring signals, unsuccessful stop (US) trials were compared with GO and SS trials.24, 25, 26, 27, 28, 29, 30 Furthermore, behavioral responses during the SST allowed the estimation of the stop-signal reaction time (SSRT), which corresponds to the latency at which executive processes underlying successful motor inhibition terminate.1 Thus, STN responses preceding the SSRT may encode stopping signals whereas STN responses occurring after the SSRT may be associated with performance monitoring signals.24,25,31


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)

(a) Localization of DBS electrodes contacts on axial and coronal MRI sections of a patient. (b) Microelectrode STN recording and mean waveform (black)±s.d. (gray) of the isolated spike cluster. (c) Stop-signal task. Participants were instructed to respond as fast as they can to the GO cue and to withhold their response when a stop signal occurs. Task difficulty during STOP trials was adjusted by shortening or lengthening the delay between GO and STOP cues (stop-signal delay, SSD) after unsuccessful or successful STOP trials. After each trial, positive and negative feedback was presented for 1 s (see Materials and Methods). CD, caudate nucleus; DBS, deep brain stimulation; GP, globus pallidus; MRI, magnetic resonance imaging; RN, red nucleus; SN, substantia nigra; STN, subthalamic nucleus.
© Copyright Policy - open-access
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4203004&req=5

fig1: (a) Localization of DBS electrodes contacts on axial and coronal MRI sections of a patient. (b) Microelectrode STN recording and mean waveform (black)±s.d. (gray) of the isolated spike cluster. (c) Stop-signal task. Participants were instructed to respond as fast as they can to the GO cue and to withhold their response when a stop signal occurs. Task difficulty during STOP trials was adjusted by shortening or lengthening the delay between GO and STOP cues (stop-signal delay, SSD) after unsuccessful or successful STOP trials. After each trial, positive and negative feedback was presented for 1 s (see Materials and Methods). CD, caudate nucleus; DBS, deep brain stimulation; GP, globus pallidus; MRI, magnetic resonance imaging; RN, red nucleus; SN, substantia nigra; STN, subthalamic nucleus.
Mentions: The SST was used to experimentally dissociate motor action, stopping and error-monitoring signals.1,24,25 It consisted of the random presentation of two trial types (Figure 1c). During GO trials (67% of trials), an imperative GO cue prompted patients to quickly press a button with the right index. During STOP trials (33% of trials), patients were asked to withhold the planned movement. To investigate the hypothesized ‘braking function' of STN neurons during response selection, we contrasted successful stop trials (SS) with GO trials. To isolate error monitoring signals, unsuccessful stop (US) trials were compared with GO and SS trials.24, 25, 26, 27, 28, 29, 30 Furthermore, behavioral responses during the SST allowed the estimation of the stop-signal reaction time (SSRT), which corresponds to the latency at which executive processes underlying successful motor inhibition terminate.1 Thus, STN responses preceding the SSRT may encode stopping signals whereas STN responses occurring after the SSRT may be associated with performance monitoring signals.24,25,31

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