Hyperreactivity to uncertainty is a key feature of subjective cognitive impairment

Abstract

With an increasingly ageing global population, more people are presenting with concerns about their cognitive function, but not all have an underlying neurodegenerative diagnosis. Subjective cognitive impairment (SCI) is a common condition describing self-reported deficits in cognition without objective evidence of cognitive impairment. Many individuals with SCI suffer from depression and anxiety, which have been hypothesised to account for their cognitive complaints. Despite this association between SCI and affective features, the cognitive and brain mechanisms underlying SCI are poorly understood. Here, we show that people with SCI are hyperreactive to uncertainty and that this might be a key mechanism accounting for their affective burden. Twenty-seven individuals with SCI performed an information sampling task, where they could actively gather information prior to decisions. Across different conditions, SCI participants sampled faster and obtained more information than matched controls to resolve uncertainty. Remarkably, despite their 'urgent' sampling behaviour, SCI participants were able to maintain their efficiency. Hyperreactivity to uncertainty indexed by this sampling behaviour correlated with the severity of affective burden including depression and anxiety. Analysis of MRI resting functional connectivity revealed that SCI participants had stronger insular-hippocampal connectivity compared to controls, which also correlated with faster sampling. These results suggest that altered uncertainty processing is a key mechanism underlying the psycho-cognitive manifestations in SCI and implicate a specific brain network target for future treatment.

Data availability

Anonymised data and code for replicating the main results in the manuscript have been deposited on the Open Science Framework platform: https://osf.io/7ysqu/.

The following data sets were generated

Article and author information

Author details

  1. Bahaaeddin Attaallah

    Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom
    For correspondence
    Bahaaeddin.Attaallah@ndcn.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7842-7974
  2. Pierre Petitet

    Department of Experimental Psychology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1422-5326
  3. Elista Slavkova

    Department of Experimental Psychology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Vicky Turner

    Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Youssuf Saleh

    Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Sanjay G Manohar

    Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Masud Husain

    Department of Experimental Psychology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

Funding

Wellcome Trust (206330/Z/17/Z)

  • Masud Husain

Rhodes Scholarships

  • Bahaaeddin Attaallah

Medical Research Council (MR/P00878/X)

  • Sanjay G Manohar

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

Ethics

Human subjects: All participants gave written consent to take part in the study. The study was approved by the University of Oxford ethics committee (RAS ID: 248379, Ethics Approval Reference: 18/SC/0448).

Reviewing Editor

  1. Valentin Wyart, École normale supérieure, PSL University, INSERM, France

Publication history

  1. Received: November 24, 2021
  2. Accepted: May 9, 2022
  3. Accepted Manuscript published: May 10, 2022 (version 1)

Copyright

© 2022, Attaallah 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.

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  1. Bahaaeddin Attaallah
  2. Pierre Petitet
  3. Elista Slavkova
  4. Vicky Turner
  5. Youssuf Saleh
  6. Sanjay G Manohar
  7. Masud Husain
(2022)
Hyperreactivity to uncertainty is a key feature of subjective cognitive impairment
eLife 11:e75834.
https://doi.org/10.7554/eLife.75834
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