The temporal representation of experience in subjective mood
- National Institutes of Health / National Institute of Mental Health, United States
- University College London, United Kingdom
Abstract
Humans refer to their mood state regularly in day-to-day as well as clinical interactions. Theoretical accounts suggest that when reporting on our mood we integrate over the history of our experiences; yet, the temporal structure of this integration remains unexamined. Here we use a computational approach to quantitatively answer this question and show that early events exert a stronger influence on reported mood compared to recent events. We show that a Primacy model accounts better for mood reports compared to a range of alternative temporal representations across random, consistent or dynamic reward environments, different age groups and in both healthy and depressed participants. Moreover, we find evidence for neural encoding of the Primacy, but not the Recency, model in frontal brain regions related to mood regulation. These findings hold implications for the timing of events in experimental or clinical settings and suggest new directions for individualized mood interventions.
Data availability
To enable the reproducibility of this study we made scripts and datasets available online at: https://osf.io/vw7sz/?view_only=e8cb4ef6782e4735815867203971994a.This repository includes: Mood modeling code; Source-data of Figure 2 (tasks trial-wise values and mood ratings values of all participants); Neural analyses code; Files of the whole-brain neural images presented in Figure 4.The link to this repository is provided in the Methods (section 7. Availability of code and datasets), and figure captions as well as other sections of the Methods refer to it.
Article and author information
Author details
Funding
National Institute of Mental Health (Intramural Research Program,ZIAMH002957-01)
- Hanna Keren
Brain and Behavior Research Foundation
- Robb B Rutledge
National Institute of Mental Health (Intramural Research Program)
- Charles Zheng
National Institute of Mental Health (Intramural Research Program)
- David C Jangraw
National Institute of Mental Health (Intramural Research Program,ZIAMH002957-01)
- Katharine Chang
National Institute of Mental Health (Intramural Research Program,ZIAMH002957-01)
- Aria Vitale
National Institute of Mental Health (Intramural Research Program,ZIAMH002957-01)
- Dylan Nielson
National Institute of Mental Health (Intramural Research Program)
- Francisco Pereira
National Institute of Mental Health (Intramural Research Program,ZIAMH002957-01)
- Argyris Stringaris
Wellcome Trust
- Robb B Rutledge
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Jonathan Roiser, University College London, United Kingdom
Ethics
Human subjects: All participants signed informed consent to a protocol approved by the NIH Institutional Review Board. The protocol is registered under the clinical trial no. NCT03388606.
Version history
- Received: August 12, 2020
- Accepted: June 2, 2021
- Accepted Manuscript published: June 15, 2021 (version 1)
- Accepted Manuscript updated: June 18, 2021 (version 2)
- Version of Record published: June 29, 2021 (version 3)
Copyright
This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
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The temporal representation of experience in subjective mood
eLife 10:e62051.
https://doi.org/10.7554/eLife.62051
Further reading
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- Neuroscience
Negative memories engage a brain and body-wide stress response in humans that can alter cognition and behavior. Prolonged stress responses induce maladaptive cellular, circuit, and systems-level changes that can lead to pathological brain states and corresponding disorders in which mood and memory are affected. However, it is unclear if repeated activation of cells processing negative memories induces similar phenotypes in mice. In this study, we used an activity-dependent tagging method to access neuronal ensembles and assess their molecular characteristics. Sequencing memory engrams in mice revealed that positive (male-to-female exposure) and negative (foot shock) cells upregulated genes linked to anti- and pro-inflammatory responses, respectively. To investigate the impact of persistent activation of negative engrams, we chemogenetically activated them in the ventral hippocampus over 3 months and conducted anxiety and memory-related tests. Negative engram activation increased anxiety behaviors in both 6- and 14-month-old mice, reduced spatial working memory in older mice, impaired fear extinction in younger mice, and heightened fear generalization in both age groups. Immunohistochemistry revealed changes in microglial and astrocytic structure and number in the hippocampus. In summary, repeated activation of negative memories induces lasting cellular and behavioral abnormalities in mice, offering insights into the negative effects of chronic negative thinking-like behaviors on human health.
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- Neuroscience
Synaptic inputs to cortical neurons are highly structured in adult sensory systems, such that neighboring synapses along dendrites are activated by similar stimuli. This organization of synaptic inputs, called synaptic clustering, is required for high-fidelity signal processing, and clustered synapses can already be observed before eye opening. However, how clustered inputs emerge during development is unknown. Here, we employed concurrent in vivo whole-cell patch-clamp and dendritic calcium imaging to map spontaneous synaptic inputs to dendrites of layer 2/3 neurons in the mouse primary visual cortex during the second postnatal week until eye opening. We found that the number of functional synapses and the frequency of transmission events increase several fold during this developmental period. At the beginning of the second postnatal week, synapses assemble specifically in confined dendritic segments, whereas other segments are devoid of synapses. By the end of the second postnatal week, just before eye opening, dendrites are almost entirely covered by domains of co-active synapses. Finally, co-activity with their neighbor synapses correlates with synaptic stabilization and potentiation. Thus, clustered synapses form in distinct functional domains presumably to equip dendrites with computational modules for high-capacity sensory processing when the eyes open.
