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The study was supported by JSPS, long-term Invitational Fellowship for Research in Japan (L16707); MEXT of Japan, Post-K Application Development for Exploratory Challenges (hp160266, hp170251, hp180223 and hp190157); and OIST.

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Gutierrez, Carlos EnriqueAuthor

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August 2, 2020
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A biologically constrained spiking neural network model of the primate basal ganglia with overlapping pathways exhibits action selection

Publicated to:European Journal Of Neuroscience. 53 (7): 2254-2277 - 2021-04-01 53(7), DOI: 10.1111/ejn.14869

Authors: Girard, Benoit; Lienard, Jean; Gutierrez, Carlos Enrique; Delord, Bruno; Doya, Kenji

Affiliations

Okinawa Inst Sci & Technol, Neural Computat Unit, Onna, Okinawa, Japan - Author
Sorbonne Univ, Inst Syst Intelligent & Robot ISIR, CNRS, Paris, France - Author

Abstract

Action selection has been hypothesized to be a key function of the basal ganglia, yet the nuclei involved, their interactions and the importance of the direct/indirect pathway segregation in such process remain debated. Here, we design a spiking computational model of the monkey basal ganglia derived from a previously published population model, initially parameterized to reproduce electrophysiological activity at rest and to embody as much quantitative anatomical data as possible. As a particular feature, both models exhibit the strong overlap between the direct and indirect pathways that has been documented in non-human primates. Here, we first show how the translation from a population to an individual neuron model was achieved, with the addition of a minimal number of parameters. We then show that our model performs action selection, even though it was built without any assumption on the activity carried out during behaviour. We investigate the mechanisms of this selection through circuit disruptions and found an instrumental role of the off-centre/on-surround structure of the MSN-STN-GPi circuit, as well as of the MSN-MSN and FSI-MSN projections. This validates their potency in enabling selection. We finally study the pervasive centromedian and parafascicular thalamic inputs that reach all basal ganglia nuclei and whose influence is therefore difficult to anticipate. Our model predicts that these inputs modulate the responsiveness of action selection, making them a candidate for the regulation of the speed-accuracy trade-off during decision-making.

Keywords

Action selectionAnimalsBasal gangliaCell dischargeCentromedianCentromedian/parafascicular thalamusComputational modelCortical inputsEfferent projectionsExternal segmentGlobus-pallidusMonkeyMotor cortexNeural networks, computerNeural pathwaysParafascicular thalamusPattern-formationPrimatesSquirrel-monkeySubthalamic nucleusThalamus

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal European Journal Of Neuroscience due to its progression and the good impact it has achieved in recent years, according to the agency Scopus (SJR), it has become a reference in its field. In the year of publication of the work, 2021, it was in position , thus managing to position itself as a Q2 (Segundo Cuartil), in the category Neuroscience (Miscellaneous). Notably, the journal is positioned en el Cuartil Q3 for the agency WoS (JCR) in the category Neurosciences.

From a relative perspective, and based on the normalized impact indicator calculated from World Citations provided by WoS (ESI, Clarivate), it yields a value for the citation normalization relative to the expected citation rate of: 1.24. This indicates that, compared to works in the same discipline and in the same year of publication, it ranks as a work cited above average. (source consulted: ESI Nov 14, 2024)

This information is reinforced by other indicators of the same type, which, although dynamic over time and dependent on the set of average global citations at the time of their calculation, consistently position the work at some point among the top 50% most cited in its field:

  • Field Citation Ratio (FCR) from Dimensions: 4.85 (source consulted: Dimensions Sep 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-09-07, the following number of citations:

  • WoS: 18
  • Europe PMC: 9

Impact and social visibility

From the perspective of influence or social adoption, and based on metrics associated with mentions and interactions provided by agencies specializing in calculating the so-called "Alternative or Social Metrics," we can highlight as of 2025-09-07:

  • The use, from an academic perspective evidenced by the Altmetric agency indicator referring to aggregations made by the personal bibliographic manager Mendeley, gives us a total of: 33.
  • The use of this contribution in bookmarks, code forks, additions to favorite lists for recurrent reading, as well as general views, indicates that someone is using the publication as a basis for their current work. This may be a notable indicator of future more formal and academic citations. This claim is supported by the result of the "Capture" indicator, which yields a total of: 33 (PlumX).

With a more dissemination-oriented intent and targeting more general audiences, we can observe other more global scores such as:

  • The Total Score from Altmetric: 11.
  • The number of mentions on the social network X (formerly Twitter): 1 (Altmetric).
  • The number of mentions in news outlets: 1 (Altmetric).

Leadership analysis of institutional authors

This work has been carried out with international collaboration, specifically with researchers from: France; Japan.