Role of the Indirect Pathway of the Basal Ganglia in Perceptual Decision Making

Wei, Wei; Rubin, Jonathan E.; Wang, Xiao Jing

doi:10.1523/jneurosci.3611-14.2015

Cited by 91 publications

(116 citation statements)

References 104 publications

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“…Our results are broadly consistent with models suggesting that basal ganglia (BG) nuclei play a role in setting decision thresholds [19–26]. However, our patients showed impairments in the ability to combine prior information with sensory information to guide decisions.…”

Section: Discussionsupporting

confidence: 91%

Patients with Parkinson’s Disease Show Impaired Use of Priors in Conditions of Sensory Uncertainty

2016

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Summary Perceptual decisions arise after considering the available sensory evidence [1]. When sensory information is unreliable, a good strategy is to rely on previous experience in similar situations to guide decisions [2–6]. It is well-known that patients with Parkinson’s disease (PD) are impaired at value-based decision-making [7–11]. How patients combine past experience and sensory information to make perceptual decisions is unknown. We developed a novel, perceptual decision-making task and manipulated the statistics of the sensory stimuli presented to patients with PD and healthy participants to determine the influence of past experience on decision-making. We show that patients with PD are impaired at combining previously learned information with current sensory information to guide decisions. We modeled the results using the drift-diffusion model (DDM) and found that the impairment corresponds to a failure in adjusting the amount of sensory evidence needed to make a decision. Our modeling results also show that two complementary mechanisms operate to implement a bias when two sets of priors are learned concurrently. Asymmetric decision threshold adjustments, as reflected by changes in the starting point of evidence accumulation, are responsible for a general choice bias, whereas the adjustment of a dynamic bias that develops over the course of a trial, as reflected by a drift rate offset, provides the stimulus-specific component of the prior. A proper interplay between these two processes is required to implement a bias based on concurrent, stimulus-specific priors in decision-making. We show here that patients with PD are impaired in these across-trial decision threshold adjustments.

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Section: Discussionsupporting

confidence: 91%

Patients with Parkinson’s Disease Show Impaired Use of Priors in Conditions of Sensory Uncertainty

2016

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“…This finding highlights the importance of a network perspective on brain activity, whereby the basal ganglia show their role in defining the whole-brain dynamical repertoire. This evidence speaks to a vast literature on the basal ganglia as part of a distributed forebrain network with a prominent role in innate behavioral routines as well as learning (retrieving) new (previously acquired) functional repertoires (64)(65)(66). Previous evidence has shown that extreme specificity is necessary in the connections between the basal ganglia, thalamus and cortex (67)(68)(69), and that the basal ganglia play a prominent role in the fine tuning of such connections (70).…”

Section: Discussionsupporting

confidence: 63%

Extensive functional repertoire underpins complex behaviours: insights from Parkinson’s disease

Sorrentino

Rucco

Baselice

et al. 2019

Preprint

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Rapid reconfigurations of brain activity support efficient neuronal communication and flexible behaviour. Suboptimal brain dynamics impair this adaptability, possibly leading to functional deficiencies. We hypothesize that impaired flexibility in brain activity can lead to motor and cognitive symptoms of Parkinson's disease (PD). To test this hypothesis, we studied the 'functional repertoire' the number of distinct configurations of neural activityusing source-reconstructed magnetoencephalography in PD patients and controls. We found stereotyped brain dynamics and reduced flexibility in PD. The intensity of this reduction was proportional to symptoms severity, and explained by beta-band hyper-synchronization. Moreover, the basal ganglia were prominently involved in the abnormal patterns of brain activity. Our findings support the hypotheses that: symptoms in PD reflect impaired brain flexibility, this impairment preferentially involves the basal ganglia, and beta-band hypersynchronization is associated with reduced brain flexibility. These findings highlight the importance of extensive functional repertoires for behaviour and motor.Parkinson's disease (PD) is a severe and disabling neurodegenerative disorder. It is characterized by reduced amplitude of movements, and slowing of cognitive processes, imposing major individual and social burden (24). The main histopathological finding in PD is a severe nigrostriatal dopamine depletion (25,26). PD has traditionally been regarded predominantly as a motor disease. However, recent clinical and neuroimaging findings have questioned these views (27). For example, the first symptoms to appear are often not motor, and the clinical phenotype clearly goes well beyond the motor impairment, with other domains, such as executive functioning, involved (28,29). Structural Magnetic Resonance Imaging (MRI) has also confirmed that PD is more widespread than previously thought (27). Although functional magnetic resonance (fMRI) studies have identified impairment in the corticostriatal network in PD patients, the observed changes in functional connectivity extend into many other brain systems (30). Similarly, magnetoencephalography (MEG) studies have also reported widespread functional connectivity alterations in PD (31-34) .The brain can be represented as a network, with, at the macro-scale, brain areas as 'nodes' and structural or functional relationships between the brain areas as 'edges ' (35, 36), following which the topology of the network can be characterised using graph theory. A rapidly growing body of research now uses graph theory to characterize large-scale patterns of brain activation in health (37) and disease (38). Graph theory has highlighted the multifaceted nature of large-scale interactions in PD, with studies reporting more-connected networks (39-42), less-connected networks (43-48), and a combination of both (49,50). However, most research in this area has assumed brain activity to be stationary, and did not explore the structure of dynamic fluctuations in activity...

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“…The Cx is the same as described in previous work (Wang, 2002), but with a lower background input to support distributed attractor state. The present model extends an earlier one (Wei et al, 2015) by including the thalamus and replacing the effect of SC in that model by a constant threshold in the Cx. We used the leaky integrate-and-fire model for all the neurons.…”

Section: Methodsmentioning

confidence: 57%

“…Interruption of the disinhibition mechanism of the BG lied in the core of our model for inhibitory control, and has been supported by recent experiments (Schmidt et al, 2013). The indirect pathway of the BG has important roles in proactive inhibitory control (Majid et al, 2013) and perceptual decision making (Wei et al, 2015). Here we showed that modulation of the relative weights of the BG pathways could effectively modulate the SSRT, which provides a possible source for individual difference of the SSRT.…”

Section: Discussionmentioning

confidence: 99%

Inhibitory Control in the Cortico-Basal Ganglia-Thalamocortical Loop: Complex Regulation and Interplay with Memory and Decision Processes

Wei

Wang

2016

Neuron

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Summary We developed a circuit model of spiking neurons that includes multiple pathways in the basal ganglia (BG) and is endowed with feedback mechanisms at three levels: cortical microcircuit, corticothalamic loop and cortico-BG-thalamocortical system. We focused on executive control in a stop-signal task, which is known to depend on BG across species. The model reproduces a range of experimental observations, and shows that the newly discovered feedback projection from external globus pallidus to striatum is crucial for inhibitory control. Moreover, stopping process is enhanced by the cortico-subcortical reverberatory dynamics underlying persistent activity, establishing an inter-dependence between working memory and inhibitory control. Surprisingly, the stop signal reaction time (SSRT) can be adjusted by weights of certain connections but is insensitive to other connections in this complex circuit, suggesting novel circuit-based intervention for inhibitory control deficits associated with mental illness. Our model provides a unified framework for inhibitory control, decision-making and working memory.

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Role of the Indirect Pathway of the Basal Ganglia in Perceptual Decision Making

Cited by 91 publications

References 104 publications

Patients with Parkinson’s Disease Show Impaired Use of Priors in Conditions of Sensory Uncertainty

Patients with Parkinson’s Disease Show Impaired Use of Priors in Conditions of Sensory Uncertainty

Extensive functional repertoire underpins complex behaviours: insights from Parkinson’s disease

Inhibitory Control in the Cortico-Basal Ganglia-Thalamocortical Loop: Complex Regulation and Interplay with Memory and Decision Processes

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