Investigating working memory updating processes of the human subcortex using 7 Tesla fMRI

eLife

Abstract

Abstract The prefrontal-cortex basal ganglia working memory (PBWM) model (Hazy et al., 2007; O’Reilly & Frank, 2006) proposes that working memory representations are updated via a striatal gating mechanism but lacks conclusive empirical support for the postulated subcortical involvement. A growing body of research suggests that dopamine is also involved in working memory updating (Braver & Cohen, 2000; Cools & D’Esposito, 2011; D’Ardenne et al., 2012; Jongkees, 2020). In this study, we investigated subcortical–in particular, possible dopaminergic–involvement in working memory updating subprocesses using the reference-back task and ultra-high field 7 Tesla fMRI. Using a scanning protocol optimized for BOLD-sensitivity in the subcortex, we found no evidence of subcortical activation during working memory gate opening, which challenges the PBWM model’s striatal gating mechanism. However, during gate closing, subcortical activation was observed. Furthermore, a ready-to-update mode demonstrated large-spread subcortical activation, including basal ganglia nuclei, suggesting that the basal ganglia are engaged in general updating processes rather than specifically controlling the working memory gate. Evidence for activity in dopaminergic midbrain regions was also observed in both contrasts. Also, substituting new information into working memory elicited activation in dopamine-producing midbrain regions along with the striatum, thalamus, and prefrontal cortex, indicating engagement of the basal ganglia-thalamo-cortical loop possibly driven by dopaminergic activity. These findings expand our understanding of subcortical regions involved in working memory updating, providing additional insights into the role of the dopaminergic midbrain.

Authors 12

1. Anne C. Trutti Aachen Cognitive Psychology Unit Institute of Psychology and Leiden Institute for Brain and Cognition

   Leiden University · Norwegian University of Science and Technology · University of Amsterdam

   Affiliation as printed

   Cognitive Psychology Unit, Institute of Psychology & Leiden Institute for Brain and Cognition, Leiden University

   Integrative Model-Based Neuroscience Research Unit, University of Amsterdam

   Cognitive Psychology Unit, Institute of Psychology & Leiden Institute for Brain and Cognition, Leiden University, Leiden, Netherlands

   Full brain picture Analytics, Leiden, The Netherlands

   Norwegian University of Science and Technology, Trondheim, Norway

   Integrative Model-Based Neuroscience Research Unit, University of Amsterdam, Amsterdam, The Netherlands

2. Zsuzsika Sjoerds Aachen Cognitive Psychology Unit Institute of Psychology and Leiden Institute for Brain and Cognition

   Leiden University · Norwegian University of Science and Technology · University of Amsterdam

   Affiliation as printed

   Cognitive Psychology Unit, Institute of Psychology & Leiden Institute for Brain and Cognition, Leiden University

   Cognitive Psychology Unit, Institute of Psychology & Leiden Institute for Brain and Cognition, Leiden University, Leiden, Netherlands

   Full brain picture Analytics, Leiden, The Netherlands

   Norwegian University of Science and Technology, Trondheim, Norway

   Integrative Model-Based Neuroscience Research Unit, University of Amsterdam, Amsterdam, The Netherlands

3. Russell James Boag Aachen Cognitive Psychology Unit Institute of Psychology and Leiden Institute for Brain and Cognition

   Leiden University · Norwegian University of Science and Technology · University of Amsterdam

   Affiliation as printed

   Integrative Model-Based Neuroscience Research Unit, University of Amsterdam

   Cognitive Psychology Unit, Institute of Psychology & Leiden Institute for Brain and Cognition, Leiden University, Leiden, Netherlands

   Full brain picture Analytics, Leiden, The Netherlands

   Norwegian University of Science and Technology, Trondheim, Norway

   Integrative Model-Based Neuroscience Research Unit, University of Amsterdam, Amsterdam, The Netherlands

4. Solenn LY Walstra Aachen Cognitive Psychology Unit Institute of Psychology and Leiden Institute for Brain and Cognition

   Leiden University · Norwegian University of Science and Technology · University of Amsterdam

   Affiliation as printed

   Integrative Model-Based Neuroscience Research Unit, University of Amsterdam

   Cognitive Psychology Unit, Institute of Psychology & Leiden Institute for Brain and Cognition, Leiden University, Leiden, Netherlands

   Full brain picture Analytics, Leiden, The Netherlands

   Norwegian University of Science and Technology, Trondheim, Norway

   Integrative Model-Based Neuroscience Research Unit, University of Amsterdam, Amsterdam, The Netherlands

5. Steven Miletić Aachen Cognitive Psychology Unit Institute of Psychology and Leiden Institute for Brain and Cognition

   Leiden University · Norwegian University of Science and Technology · University of Amsterdam

   Affiliation as printed

   Cognitive Psychology Unit, Institute of Psychology & Leiden Institute for Brain and Cognition, Leiden University

   Integrative Model-Based Neuroscience Research Unit, University of Amsterdam

   Cognitive Psychology Unit, Institute of Psychology & Leiden Institute for Brain and Cognition, Leiden University, Leiden, Netherlands

   Full brain picture Analytics, Leiden, The Netherlands

   Norwegian University of Science and Technology, Trondheim, Norway

   Integrative Model-Based Neuroscience Research Unit, University of Amsterdam, Amsterdam, The Netherlands

6. Scott JS Isherwood Aachen Cognitive Psychology Unit Institute of Psychology and Leiden Institute for Brain and Cognition

   Leiden University · Norwegian University of Science and Technology · University of Amsterdam

   Affiliation as printed

   Integrative Model-Based Neuroscience Research Unit, University of Amsterdam

   Cognitive Psychology Unit, Institute of Psychology & Leiden Institute for Brain and Cognition, Leiden University, Leiden, Netherlands

   Full brain picture Analytics, Leiden, The Netherlands

   Norwegian University of Science and Technology, Trondheim, Norway

   Integrative Model-Based Neuroscience Research Unit, University of Amsterdam, Amsterdam, The Netherlands

7. Pierre‐Louis Bazin Aachen Cognitive Psychology Unit Institute of Psychology and Leiden Institute for Brain and Cognition

   Leiden University · Norwegian University of Science and Technology · University of Amsterdam

   Affiliation as printed

   Full brain picture Analytics

   Cognitive Psychology Unit, Institute of Psychology & Leiden Institute for Brain and Cognition, Leiden University, Leiden, Netherlands

   Full brain picture Analytics, Leiden, The Netherlands

   Norwegian University of Science and Technology, Trondheim, Norway

   Integrative Model-Based Neuroscience Research Unit, University of Amsterdam, Amsterdam, The Netherlands

8. Bernhard Hommel Aachen Cognitive Psychology Unit Institute of Psychology and Leiden Institute for Brain and Cognition

   Leiden University · Norwegian University of Science and Technology · Shandong Normal University · University of Amsterdam

   Affiliation as printed

   Department of Psychology, Shandong Normal University

   Cognitive Psychology Unit, Institute of Psychology & Leiden Institute for Brain and Cognition, Leiden University, Leiden, Netherlands

   Full brain picture Analytics, Leiden, The Netherlands

   Norwegian University of Science and Technology, Trondheim, Norway

   Integrative Model-Based Neuroscience Research Unit, University of Amsterdam, Amsterdam, The Netherlands

9. Sarah Habli Aachen Cognitive Psychology Unit Institute of Psychology and Leiden Institute for Brain and Cognition

   Leiden University · Norwegian University of Science and Technology · University of Amsterdam

   Affiliation as printed

   Norwegian University of Science and Technology

   Cognitive Psychology Unit, Institute of Psychology & Leiden Institute for Brain and Cognition, Leiden University, Leiden, Netherlands

   Full brain picture Analytics, Leiden, The Netherlands

   Norwegian University of Science and Technology, Trondheim, Norway

   Integrative Model-Based Neuroscience Research Unit, University of Amsterdam, Amsterdam, The Netherlands

10. Desmond H. Y. Tse Aachen Cognitive Psychology Unit Institute of Psychology and Leiden Institute for Brain and Cognition

    Leiden University · Norwegian University of Science and Technology · University of Amsterdam

    Affiliation as printed

    Norwegian University of Science and Technology

    Cognitive Psychology Unit, Institute of Psychology & Leiden Institute for Brain and Cognition, Leiden University, Leiden, Netherlands

    Full brain picture Analytics, Leiden, The Netherlands

    Norwegian University of Science and Technology, Trondheim, Norway

    Integrative Model-Based Neuroscience Research Unit, University of Amsterdam, Amsterdam, The Netherlands

11. Asta Kristine Haberg Aachen Cognitive Psychology Unit Institute of Psychology and Leiden Institute for Brain and Cognition

    Leiden University · Norwegian University of Science and Technology · University of Amsterdam

    Affiliation as printed

    Norwegian University of Science and Technology

    Cognitive Psychology Unit, Institute of Psychology & Leiden Institute for Brain and Cognition, Leiden University, Leiden, Netherlands

    Full brain picture Analytics, Leiden, The Netherlands

    Norwegian University of Science and Technology, Trondheim, Norway

    Integrative Model-Based Neuroscience Research Unit, University of Amsterdam, Amsterdam, The Netherlands

12. Birte U. Forstmann

    University of Amsterdam

    Affiliation as printed

    Integrative Model-Based Neuroscience Research Unit, University of Amsterdam