1. Neuroscience

Large-scale neural dynamics in a shared low-dimensionalstate space reflect cognitive and attentional dynamics

  1. Hayoung Song  Is a corresponding author
  2. Won Mok Shim  Is a corresponding author
  3. Monica D Rosenberg  Is a corresponding author
  1. University of Chicago, United States
  2. Sungkyunkwan University, Republic of Korea
https://doi.org/10.7554/eLife.85487
Share this article
Cite this article
  1. Hayoung Song
  2. Won Mok Shim
  3. Monica D Rosenberg
(2023)
Large-scale neural dynamics in a shared low-dimensionalstate space reflect cognitive and attentional dynamics
eLife 12:e85487.
https://doi.org/10.7554/eLife.85487
  2. Download BibTeX
  3. Download .RIS

Abstract

Cognition and attention arise from the adaptive coordination of neural systems in response to external and internal demands. The low-dimensional latent subspace that underlies large-scale neural dynamics and the relationships of these dynamics to cognitive and attentional states, however, are unknown. We conducted functional magnetic resonance imaging as human participants performed attention tasks, watched comedy sitcom episodes and an educational documentary, and rested. Whole-brain dynamics traversed a common set of latent states that spanned canonical gradients of functional brain organization, with global desynchronization among functional networks modulating state transitions. Neural state dynamics were synchronized across people during engaging movie watching and aligned to narrative event structures. Neural state dynamics reflected attention fluctuations such that different states indicated engaged attention in task and naturalistic contexts whereas a common state indicated attention lapses in both contexts. Together, these results demonstrate that traversals along large-scale gradients of human brain organization reflect cognitive and attentional dynamics.

Data availability

Raw fMRI data from the SitcOm, Nature documentary, Gradual-onset continuous performance task (SONG) dataset are available on OpenNeuro;https://openneuro.org/datasets/ds004592/versions/1.0.1. Behavioral data, processed fMRI output, and main analysis scripts are published on Github; https://github.com/hyssong/neuraldynamics

The following data sets were generated
    1. Song H
    2. Shim WM
    3. Rosenberg MD
    (2023) SONG dataset
    https://doi.org/10.18112/openneuro.ds004592.v1.0.1.
    https://openneuro.org/datasets/ds004592/versions/1.0.1
The following previously published data sets were used

Article and author information

Author details

  1. Hayoung Song

    Department of Psychology, University of Chicago, Chicago, United States
    For correspondence
    hyssong@uchicago.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5970-8076

  2. Won Mok Shim

    Department of Biomedical Engineering, Sungkyunkwan University, Suwon, Republic of Korea
    For correspondence
    wonmokshim@skku.edu
    Competing interests
    The authors declare that no competing interests exist.

  3. Monica D Rosenberg

    Department of Psychology, University of Chicago, Chicago, United States
    For correspondence
    mdrosenberg@uchicago.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6179-4025

Funding

Institute for Basic Science (R015-D1)

  • Won Mok Shim

National Research Foundation of Korea (NRF-2019M3E5D2A01060299)

  • Won Mok Shim

National Research Foundation of Korea (NRF-2019R1A2C1085566)

  • Won Mok Shim

National Science Foundation (BCS-2043740)

  • Monica D Rosenberg

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: Informed consent and consent to publish were obtained from the participants prior to the experiments, and the possible consequences of the study were explained. The study was approved by the Institutional Review Board of Sungkyunkwan University.

Copyright

© 2023, Song et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 4,279
    views
  • 512
    downloads
  • 33
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Hayoung Song
  2. Won Mok Shim
  3. Monica D Rosenberg
(2023)
Large-scale neural dynamics in a shared low-dimensionalstate space reflect cognitive and attentional dynamics
eLife 12:e85487.
https://doi.org/10.7554/eLife.85487

Share this article

https://doi.org/10.7554/eLife.85487

Categories and tags

Research organism

Further reading

    1. Neuroscience

    Neural mechanisms of credit assignment for delayed outcomes during contingent learning

    Phillip P Witkowski, Lindsay JH Rondot ... Erie Boorman
    Research Article

    Adaptive behavior in complex environments critically relies on the ability to appropriately link specific choices or actions to their outcomes. However, the neural mechanisms that support the ability to credit only those past choices believed to have caused the observed outcomes remain unclear. Here, we leverage multivariate pattern analyses of functional magnetic resonance imaging (fMRI) data and an adaptive learning task to shed light on the underlying neural mechanisms of such specific credit assignment. We find that the lateral orbitofrontal cortex (lOFC) and hippocampus (HC) code for the causal choice identity when credit needs to be assigned for choices that are separated from outcomes by a long delay, even when this delayed transition is punctuated by interim decisions. Further, we show when interim decisions must be made, learning is additionally supported by lateral frontopolar cortex (lFPC). Our results indicate that lFPC holds previous causal choices in a ‘pending’ state until a relevant outcome is observed, and the fidelity of these representations predicts the fidelity of subsequent causal choice representations in lOFC and HC during credit assignment. Together, these results highlight the importance of the timely reinstatement of specific causes in lOFC and HC in learning choice-outcome relationships when delays and choices intervene, a critical component of real-world learning and decision making.

    1. Neuroscience

    Non-allometric expansion and enhanced compartmentalization of Purkinje cell dendrites in the human cerebellum

    Silas E Busch, Christian Hansel
    Research Article

    Purkinje cell (PC) dendrites are optimized to integrate the vast cerebellar input array and drive the sole cortical output. PCs are classically seen as stereotypical computational units, yet mouse PCs are morphologically diverse and those with multi-branched structure can receive non-canonical climbing fiber (CF) multi-innervation that confers independent compartment-specific signaling. While otherwise uncharacterized, human PCs are universally multi-branched. Do they exceed allometry to achieve enhanced integrative capacities relative to mouse PCs? To answer this, we used several comparative histology techniques in adult human and mouse to analyze cellular morphology, parallel fiber (PF) and CF input arrangement, and regional PC demographics. Human PCs are substantially larger than previously described; they exceed allometric constraint by cortical thickness and are the largest neuron in the brain with 6–7 cm total dendritic length. Unlike mouse, human PC dendrites ramify horizontally to form a multi-compartment motif that we show can receive multiple CFs. Human spines are denser (6.9 vs 4.9 spines/μm), larger (~0.36 vs 0.29 μm), and include an unreported ‘spine cluster’ structure—features that may be congruent with enhanced PF association and amplification as human-specific adaptations. By extrapolation, human PCs may receive 500,000 to 1 million synaptic inputs compared with 30–40,000 in mouse. Collectively, human PC morphology and input arrangement is quantitatively and qualitatively distinct from rodent. Multi-branched PCs are more prevalent in posterior and lateral cerebellum, co-varying with functional boundaries, supporting the hypothesis that this morphological motif permits expanded input multiplexing and may subserve task-dependent needs for input association.

    1. Neuroscience

    Food intake enhances hippocampal sharp wave-ripples

    Ekin Kaya, Evan Wegienka ... Gideon Rothschild
    Research Article

    Effective regulation of energy metabolism is critical for survival. Metabolic control involves various nuclei within the hypothalamus, which receive information about the body’s energy state and coordinate appropriate responses to maintain homeostasis, such as thermogenesis, pancreatic insulin secretion, and food-seeking behaviors. It has recently been found that the hippocampus, a brain region traditionally associated with memory and spatial navigation, is also involved in metabolic regulation. Specifically, hippocampal sharp wave-ripples (SWRs), which are high-frequency neural oscillations supporting memory consolidation and foraging decisions, have been shown to reduce peripheral glucose levels. However, whether SWRs are enhanced by recent feeding—when the need for glucose metabolism increases, and if so, whether feeding-dependent modulation of SWRs is communicated to other brain regions involved in metabolic regulation—remains unknown. To address these gaps, we recorded SWRs from the dorsal CA1 region of the hippocampus of mice during sleep sessions before and after consumption of meals of varying caloric values. We found that SWRs occurring during sleep are significantly enhanced following food intake, with the magnitude of enhancement being dependent on the caloric content of the meal. This pattern occurred under both food-deprived and ad libitum feeding conditions. Moreover, we demonstrate that GABAergic neurons in the lateral hypothalamus, which are known to regulate food intake, exhibit a robust SWR-triggered increase in activity. These findings identify the satiety state as a factor modulating SWRs and suggest that hippocampal-lateral hypothalamic communication is a potential mechanism by which SWRs could modulate peripheral metabolism and food intake.