The Human Basal Ganglia Mediate the Interplay between Reactive and Proactive Control of Response through Both Motor Inhibition and Sensory Modulation

Abstract

The basal ganglia (BG) have long been known for contributing to the regulation of motor behaviour by means of a complex interplay between tonic and phasic inhibitory mechanisms. However, after having focused for a long time on phasic reactive mechanisms, it is only recently that psychological research in healthy humans has modelled tonic proactive mechanisms of control. Mutual calibration between anatomo-functional and psychological models is still needed to better understand the unclear role of the BG in the interplay between proactive and reactive mechanisms of control. Here, we implemented an event-related fMRI design allowing proper analysis of both the brain activity preceding the target-stimulus and the brain activity induced by the target-stimulus during a simple go/nogo task, with a particular interest in the ambiguous role of the basal ganglia. Post-stimulus activity was evoked in the left dorsal striatum, the subthalamus nucleus and internal globus pallidus by any stimulus when the situation was unpredictable, pinpointing its involvement in reactive, non-selective inhibitory mechanisms when action restraint is required. Pre-stimulus activity was detected in the ventral, not the dorsal, striatum, when the situation was unpredictable, and was associated with changes in functional connectivity with the early visual, not the motor, cortex. This suggests that the ventral striatum supports modulatory influence over sensory processing during proactive control.

The Subthalamic Nucleus: A Hub for Sensory Control via Short Three- Lateral Loop Connections with the Brainstem?

“…emotional processing [9], behavioral interruption and switching between actions [10][11][12][13][14][15].…”

Noradrenaline and Movement Initiation Disorders in Parkinson’s Disease: A Pharmacological Functional MRI Study with Clonidine

“…Impairment in initiating movements in PD might also be related to executive dysfunctions [ 14 ]; in particular, to abnormal proactive inhibitory control [ 12 , 15 , 16 ]. Proactive inhibition is a pivotal mechanism which gates movement initiation in anticipation of stimulation when the context is uncertain and requires action restraint ( Figure 1 B) [ 17 , 18 , 19 , 20 ]. Proactive inhibition has been considered the default state of the executive system [ 19 , 20 , 21 ].…”

“…Proactive inhibition is a pivotal mechanism which gates movement initiation in anticipation of stimulation when the context is uncertain and requires action restraint ( Figure 1 B) [ 17 , 18 , 19 , 20 ]. Proactive inhibition has been considered the default state of the executive system [ 19 , 20 , 21 ]. In healthy subjects, it takes less than 300 ms to release proactive inhibition and allow response triggering after an appropriate stimulus has been identified [ 21 ].…”

Inhibitory framing in hypersexual patients with Parkinson’s disease. An fMRI pilot study

“…In contrast, the term "response inhibition" is more focused and often used psychometrically to describe the suppression of a (prepotent) motor response. Several neuroimaging studies examined response inhibition in healthy participants and PD patients with ICB with paradigms that do not involve reward processing highlighting the involvement of similar regions, such as the ventral striatum and cingulate cortex (Criaud et al 2017(Criaud et al , 2021Meyer et al 2020). However, how the dynamic interplay of inhibitory context and cue-reactivity is changed following dopaminergic stimulation is not well understood.…”

“…A key feature of ICB is an impaired inhibitory control (Probst and van Eimeren 2013 ). Inhibitory control is the ability to suppress undesired or inappropriate actions, which largely overlaps with response inhibition (Criaud et al 2021 ). The term “inhibitory control” is often used as an umbrella term in psychology describing the objectively and subjectively perceived ability to suppress behavioral responses or thoughts, particularly when the lack of control is associated with negative long-term consequences.…”