Limits...
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.

Show MeSH

Related in: MedlinePlus

Selective response of STN neurons during motor responses, shown as rastergrams (black dots), SDF (continuous lines) and PSTH across trial types (US, GO and SS trials). (a) Representative GO unit. Time origin indicates button presses (BP) during US and fast GO trials and stop cue during SS trials. (b) Population activity of all recorded GO units (n=10). The conventions are as in Figure 5. PSTH, peri-stimulus spike histogram; SDF, spike density function; SS, successful stop trial; STN, subthalamic nucleus; US, unsuccessful stop trial.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4203004&req=5

fig4: Selective response of STN neurons during motor responses, shown as rastergrams (black dots), SDF (continuous lines) and PSTH across trial types (US, GO and SS trials). (a) Representative GO unit. Time origin indicates button presses (BP) during US and fast GO trials and stop cue during SS trials. (b) Population activity of all recorded GO units (n=10). The conventions are as in Figure 5. PSTH, peri-stimulus spike histogram; SDF, spike density function; SS, successful stop trial; STN, subthalamic nucleus; US, unsuccessful stop trial.

Mentions: After spike sorting, a total of 75 STN units were identified (52 single units and 23 multiunits). The average baseline firing rate of STN units, which was measured during 500-ms epochs of fixation, did not differ between single unit and multiunit (two-tailed unpaired student's t-test, t(73)=0.24; P=0.81; single unit: 19.5±11.2 Hz; multiunit: 20.2±13.7 Hz) and were in accordance with STN neurophysiology known in human12 and nonhuman20 primates. Thirty-two of the 75 units (43%) showed a significant task-related response (P<0.05, resampling test). We pooled the task-responsive cells into three functional classes according to their activity profile across the different conditions (GO, US, SS trials). Figure 2a shows a single cell that increased its firing rate selectively during SS trials, 167 ms before SSRT, suggesting that this neuron could in principle support a fast stopping signal. Note that this cell did not respond during US trials and GO trials. Figure 3a shows a single unit that responded after behavioral errors: it significantly increased its firing rate only during US trials (P<0.05) after incorrect responses, but exhibited no significant change of activity during SS trials and showed a transient decrease of activity before correct GO button presses. Figure 4a shows a third type of cell that increased its activity during motor control, that is, around correct or incorrect button presses (this increase was absent during SS trials during which there was no motor response).


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)

Selective response of STN neurons during motor responses, shown as rastergrams (black dots), SDF (continuous lines) and PSTH across trial types (US, GO and SS trials). (a) Representative GO unit. Time origin indicates button presses (BP) during US and fast GO trials and stop cue during SS trials. (b) Population activity of all recorded GO units (n=10). The conventions are as in Figure 5. PSTH, peri-stimulus spike histogram; SDF, spike density function; SS, successful stop trial; 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

fig4: Selective response of STN neurons during motor responses, shown as rastergrams (black dots), SDF (continuous lines) and PSTH across trial types (US, GO and SS trials). (a) Representative GO unit. Time origin indicates button presses (BP) during US and fast GO trials and stop cue during SS trials. (b) Population activity of all recorded GO units (n=10). The conventions are as in Figure 5. PSTH, peri-stimulus spike histogram; SDF, spike density function; SS, successful stop trial; STN, subthalamic nucleus; US, unsuccessful stop trial.
Mentions: After spike sorting, a total of 75 STN units were identified (52 single units and 23 multiunits). The average baseline firing rate of STN units, which was measured during 500-ms epochs of fixation, did not differ between single unit and multiunit (two-tailed unpaired student's t-test, t(73)=0.24; P=0.81; single unit: 19.5±11.2 Hz; multiunit: 20.2±13.7 Hz) and were in accordance with STN neurophysiology known in human12 and nonhuman20 primates. Thirty-two of the 75 units (43%) showed a significant task-related response (P<0.05, resampling test). We pooled the task-responsive cells into three functional classes according to their activity profile across the different conditions (GO, US, SS trials). Figure 2a shows a single cell that increased its firing rate selectively during SS trials, 167 ms before SSRT, suggesting that this neuron could in principle support a fast stopping signal. Note that this cell did not respond during US trials and GO trials. Figure 3a shows a single unit that responded after behavioral errors: it significantly increased its firing rate only during US trials (P<0.05) after incorrect responses, but exhibited no significant change of activity during SS trials and showed a transient decrease of activity before correct GO button presses. Figure 4a shows a third type of cell that increased its activity during motor control, that is, around correct or incorrect button presses (this increase was absent during SS trials during which there was no motor response).

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