The role of cortical oscillations in a spiking neural network model of the basal ganglia

Fountas, Zafeirios; Shanahan, Murray

doi:10.1371/journal.pone.0189109

Cited by 25 publications

(112 citation statements)

References 161 publications

(263 reference statements)

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“…Evidence suggests that oscillations in some 34 certain bands in the striatum and the subthalamic nucleus (STN), the input structures 35 of the BG, are driven by cortical regions [22][23][24][25]. Taking this into account, in previous 36 work [26] we explored the impact of cortical rhythmic activity on the BG function and 37 we found that the former can completely shape which areas of the BG circuit are active. 38 Yet, the connection between the BG, cortical oscillations and decision making still 39 remains relatively unexplored.…”

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confidence: 95%

“…To achieve 42 this, we initially defined a number of metrics that enable the assessment of the 43 effectiveness of possible selection mechanisms. Using the biologically plausible neural 44 model of the BG circuitry defined in [26], we then carried out an analysis of the 45 relationship between cortical frequencies, dopamine concentration and BG selectivity. 46 We found that the frequency and phase difference between oscillatory cortical areas, 47 the level of dopamine in the system and the examined time scale, all have a very sequentially perform selection tasks, the strongly-active cortical areas instruct the mode 53 of this selection via their oscillatory activity.…”

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confidence: 99%

“…The basal ganglia model 65 The full model 66 The predominant tool used in this study is a state-of-the-art, large-scale spiking neuron 67 model of the complete motor BG circuitry, presented in detail in [26]. This model 68 integrates fine-tuned models of phenomenological (Izhikevich) spiking neurons that In particular, this model comprises 10 neural populations that correspond to the four 73 major nuclei of the biological BG and form the canonical circuit described in the 74 Introduction.…”

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confidence: 99%

“…As a consequence of its detailed architecture, the neural model in [26] contains a rather 100 high number of parameters that might influence its behaviour and the resulting 101 measurements of selectivity. In order to narrow down this space and establish the most 102 important BG features for selectivity we defined a second, simplified version of this 103 neural model with significantly less differences between nuclei.…”

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confidence: 99%

“…In order to narrow down this space and establish the most 102 important BG features for selectivity we defined a second, simplified version of this 103 neural model with significantly less differences between nuclei. The behaviour of this 104 simplified model is compared against the full version in [26] [30] connections in the system. In addition, no optimization was conducted to fit the firing 117 rates of the model to the corresponding biological nuclei, as it was the case with the 118 original model in [26].…”

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confidence: 99%

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Assessing Selectivity in the Basal Ganglia: The “Gearbox” Hypothesis

Fountas

Shanahan

2017

Preprint

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Despite experimental evidence, the literature so far contains no systematic attempt to address the impact of cortical oscillations on the ability of the basal ganglia (BG) to select. In this study, we employed a state-of-the-art spiking neural model of the BG circuitry and investigated the effectiveness of this circuitry as an action selection device. We found that cortical frequency, phase, dopamine and the examined time scale, all have a very important impact on this process. Our simulations resulted in a canonical profile of selectivity, termed selectivity portraits, which suggests that the cortex is the structure that determines whether selection will be performed in the BG and what strategy will be utilized. Some frequency ranges promote the exploitation of highly salient actions, others promote the exploration of alternative options, while the remaining frequencies halt the selection process. Based on this behaviour, we propose that the BG circuitry can be viewed as the "gearbox" of action selection. Coalitions of rhythmic cortical areas are able to switch between a repertoire of available BG modes which, in turn, change the course of information flow within the cortico-BG-thalamo-cortical loop. Dopamine, akin to "control pedals", either stops or initiates a decision, while cortical frequencies, as a "gear lever", determine whether a decision can be triggered and what type of decision this will be. Finally, we identified a selection cycle with a period of around 200ms, which was used to assess the biological plausibility of the popular cognitive architectures. Author summaryOur brains are continuously called to select the most appropriate action between alternative competing choices. A plethora of evidence and theoretical work indicates that a fundamental brain region called the basal ganglia might be the locus where this competition occurs. But how is the winning choice determined each time? Using a detailed computational model, based on neurophysiological properties of this region, we suggest that, whereas the basal ganglia might indeed contain the circuitry of action selection, the cerebral cortex is, in fact, the brain region that dictates this process. Similarly to a gearbox in a car, the basal ganglia provide modes for the exploitation of the safest option (forward gears), exploration of alternative options (reverse gear) and a neutral state, in case that the selection process needs to be halted. Our results further indicate that the instructions for mode-switching are relayed to the basal ganglia through specific low frequencies of oscillations within cortical areas. Finally, we provide estimations for the frequency ranges that can be used to activate each selectivity mode, as well as the duration of the selection process under various conditions.

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confidence: 95%

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confidence: 99%

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confidence: 99%

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confidence: 99%

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confidence: 99%

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Assessing Selectivity in the Basal Ganglia: The “Gearbox” Hypothesis

Fountas

Shanahan

2017

Preprint

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Making decisions in the dark basement of the brain: A look back at the GPR model of action selection and the basal ganglia

Humphries

Gurney

2021

Biol Cybern

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How does your brain decide what you will do next? Over the past few decades compelling evidence has emerged that the basal ganglia, a collection of nuclei in the fore-and mid-brain of all vertebrates, are vital to action selection. Gurney, Prescott, and Redgrave published an influential computational account of this idea in Biological Cybernetics in 2001. Here we take a look back at this pair of papers, outlining the "GPR" model contained therein, the context of that model's development, and the influence it has had over the past twenty years. Tracing its lineage into models and theories still emerging now, we are encouraged that the GPR model is that rare thing, a computational model of a brain circuit whose advances were directly built on by others.

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