An Essential Role of the Intraparietal Sulcus in Response Inhibition Predicted by Parcellation-Based Network

Osada, Takahiro; Ohta, Shinri; Ogawa, Akitoshi; Tanaka, Masaki; Suda, Akimitsu; Kamagata, Koji; Hori, Masaaki; Aoki, Shigeki; Shimo, Yasushi; Hattori, Nobutaka; Shimizu, Takahiro; Enomoto, Hiroyuki; Hanajima, Ritsuko; Ugawa, Yoshikazu; Konishi, Seiki

doi:10.1523/jneurosci.2244-18.2019

Cited by 62 publications

(63 citation statements)

References 98 publications

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“…Together these results suggest that targeting parietal cortex may impact frontal circuits, and vice versa. Consistent with this hypothesis, stimulation to the IPS, which shows strong prefrontal connections, lead to impairments on a stop signal task compared to stimulation of the tempoparietal junction, an area not connected to the prefrontal cortex 74 . Also consistent with this network hypothesis of TMS effects, recent work has shown that prefrontal stimulation alters parietal activity 75 , and that the therapeutic effects of prefrontal stimulation may be mediated in part through these changes in parietal activity 76 .…”

Section: Discussionmentioning

confidence: 66%

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Low-frequency parietal repetitive transcranial magnetic stimulation reduces fear and anxiety

et al. 2020

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Anxiety disorders are the most prevalent mental disorders, with few effective neuropharmacological treatments, making treatments development critical. While noninvasive neuromodulation can successfully treat depression, few treatment targets have been identified specifically for anxiety disorders. Previously, we showed that shock threat increases excitability and connectivity of the intraparietal sulcus (IPS). Here we tested the hypothesis that inhibitory repetitive transcranial magnetic stimulation (rTMS) targeting this region would reduce induced anxiety. Subjects were exposed to neutral, predictable, and unpredictable shock threat, while receiving double-blinded, 1 Hz active or sham IPS rTMS. We used global brain connectivity and electric-field modelling to define the single-subject targets. We assessed subjective anxiety with online ratings and physiological arousal with the startle reflex. Startle stimuli (103 dB white noise) probed fear and anxiety during the predictable (fear-potentiated startle, FPS) and unpredictable (anxietypotentiated startle, APS) conditions. Active rTMS reduced both FPS and APS relative to both the sham and no stimulation conditions. However, the online anxiety ratings showed no difference between the stimulation conditions. These results were not dependent on the laterality of the stimulation, or the subjects' perception of the stimulation (i.e. active vs. sham). Results suggest that reducing IPS excitability during shock threat is sufficient to reduce physiological arousal related to both fear and anxiety, and are consistent with our previous research showing hyperexcitability in this region during threat. By extension, these results suggest that 1 Hz parietal stimulation may be an effective treatment for clinical anxiety, warranting future work in anxiety patients.

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Section: Discussionmentioning

confidence: 66%

“…Importantly, frontoparietal interactions may be important for treatment response. Connectivity based parcellation shows that the IPS is strongly connected to prefrontal regions important for attentional processes 74 . Indeed, our previous results suggest that this region may be a cortical connectivity hub 14 .…”

Section: Discussionmentioning

confidence: 99%

Low-frequency parietal repetitive transcranial magnetic stimulation reduces fear and anxiety

et al. 2020

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“…Frontal Eye Field decrease activity in less than 10 ms before SSRT (Hanes et al, 1998), dopaminergic neurons in rodent substantia nigra and striatum increase activity only 12 ms before SSRT (Ogasawara et al, 2018), TMS at ~25 ms before SSRT over human Intraparietal Sulcus prolongs SSRT (Osada et al, 2019), and P300 human EEG activity ~300 ms after the Stop signal relates to the stopping latency (Wessel and Aron, 2015). Whereas the rather late timing of some of these results might be related to processes such as monitoring and feedback (Huster et al, 2019) as has been ascribed to brain signatures that modulate after SSRT (Logan et al, 2015;Schall and Boucher, 2007), our earlier latencies for prefrontal bursts, TMS-MEP and muscle…”

Section: Discussionmentioning

confidence: 98%

Temporal cascade of frontal, motor and muscle processes underlying human action-stopping

Jana

Hannah

Muralidharan

et al. 2020

eLife

131

161

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Action-stopping is a canonical executive function thought to involve top-down control over the motor system. Here we aimed to validate this stopping system using high temporal resolution methods in humans. We show that, following the requirement to stop, there was an increase of right frontal beta (~13 to 30 Hz) at ~120 ms, likely a proxy of right inferior frontal gyrus; then, at 140 ms, there was a broad skeletomotor suppression, likely reflecting the impact of the subthalamic nucleus on basal ganglia output; then, at ~160 ms, suppression was detected in the muscle, and, finally, the behavioral time of stopping was ~220 ms. This temporal cascade supports a physiological model of action-stopping, and partitions it into subprocesses that are isolable to different nodes and are more precise than the behavioral latency of stopping. Variation in these subprocesses, including at the single-trial level, could better explain individual differences in impulse control.

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“…This model specifies the chronometrics of stopping in more detail than extant human models, and, more generally, raises questions about the timing reported in some other studies. For example, other research has shown that movement neurons in monkey Frontal Eye Field decrease activity <10 ms before SSRT 42 , dopaminergic neurons in rodent substantia nigra and striatum increase activity 12 ms prior to SSRT 43 , TMS at ∼25 ms before SSRT over human Intraparietal Sulcus prolongs SSRT 44 , and that P300 human EEG activity ∼300 ms after the Stop signal relates to stopping speed 45 . Our observations of shorter latencies for prefrontal bursts, TMS-MEP and muscle CancelTime, raise questions about what is reflected in these late neural activities.…”

Section: Discussionmentioning

confidence: 99%

Temporal cascade of frontal, motor and muscle processes underlying human action-stopping

Jana

Hannah

Muralidharan

et al. 2019

Preprint

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15Action-stopping is a canonical executive function thought to involve top-down control 16 over the motor system. Here we aimed to validate this stopping system using high temporal 17 resolution methods in humans. We show that, following the requirement to stop, there was an 18 increase of right frontal beta (~13 to 30 Hz) at ~120 ms, likely a proxy of right inferior frontal 19 gyrus; then, at 140 ms, there was a broad skeletomotor suppression, likely reflecting the impact 20 of the subthalamic nucleus on basal ganglia output; then, at ~160 ms, suppression was detected 21 in the muscle, and, finally, the behavioral time of stopping was ~220 ms. This temporal cascade 22 confirms a detailed model of action-stopping, and partitions it into subprocesses that are isolable 23 to different nodes and are more precise than the behavioral speed of stopping. Variation in these 24 subprocesses, including at the single-trial level, could better explain individual differences in 25 impulse control. 26 27 28The ability to control one's actions and thoughts is important for our daily lives; for 29 example: changing gait when there is an obstacle in the path 1 , resisting the temptation to eat 30 when on a diet 2 , overcoming the tendency to say something hurtful 3 . While many processes 31 contribute to such forms of control, one important process is response inhibition -the prefrontal 32 (top-down) stopping of initiated response tendencies 4 . In the laboratory, response inhibition is 33 often studied with the stop-signal task 5 . On each trial, the participant initiates a motor response, 34 and then, when a subsequent Stop signal occurs, tries to stop. From the behavioral data one can 35 estimate a latent variable; the speed of stopping known as Stop Signal Reaction Time (SSRT), 36 which is typically 200-250 ms in healthy adults 5 . SSRT has been useful in neuropsychiatry 37where it is often longer for patients vs. controls [6][7][8][9][10][11] . The task has also provided a rich test-bed, 38 3 across species, for mapping out a putative neural architecture of prefrontal-basal-ganglia-regions 39 for rapidly suppressing motor output areas 6,12,13 . Given this rich literature, this task is one of the 40 few paradigms included in the longitudinal Adolescent Brain Cognitive Development study 14 of 41 10,000 adolescents over 10 years. 42Against this background, a puzzle is that the relation between SSRT and 'real-world' 43 self-reported impulsivity is often weak 15-20 . One explanation is that SSRT may not accurately 44 index the brain's true stopping speed. Indeed, recent mathematical modelling of behavior during 45 the stop-signal task suggests that standard calculations of SSRT may overestimate the brain's 46 stopping speed by ~100 ms 15 [also see 21 ]. Further, in a recent study 22 , electromyographic (EMG) 47 recordings revealed an initial increase in EMG activity in response to the Go cue, followed by a 48 sudden decline at ~150 ms after the Stop signal. This decline in EMG could be because of the 49 Stop process 'kicking in'...

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An Essential Role of the Intraparietal Sulcus in Response Inhibition Predicted by Parcellation-Based Network

Cited by 62 publications

References 98 publications

Low-frequency parietal repetitive transcranial magnetic stimulation reduces fear and anxiety

Low-frequency parietal repetitive transcranial magnetic stimulation reduces fear and anxiety

Temporal cascade of frontal, motor and muscle processes underlying human action-stopping

Temporal cascade of frontal, motor and muscle processes underlying human action-stopping

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