The human cerebellum is essential for modulating perceptual sensitivity based on temporal expectations

  1. Assaf Breska  Is a corresponding author
  2. Richard B Ivry
  1. University of California, Berkeley, United States

Abstract

A functional benefit of attention is to proactively enhance perceptual sensitivity in space and time. Although attentional orienting has traditionally been associated with cortico-thalamic networks, recent evidence has shown that individuals with cerebellar degeneration (CD) show a reduced reaction time benefit from cues that enable temporal anticipation. The present study examined whether the cerebellum contributes to the proactive attentional modulation in time of perceptual sensitivity. We tested CD participants on a non-speeded, challenging perceptual discrimination task, asking if they benefit from temporal cues. Strikingly, the CD group showed no duration-specific perceptual sensitivity benefit when cued by repeated but aperiodic presentation of the target interval. In contrast, they performed similar to controls when cued by a rhythmic stream. This dissociation further specifies the functional domain of the cerebellum and establishes its role in the attentional adjustment of perceptual sensitivity in time in addition to its well-documented role in motor timing.

Data availability

De-identified source data files for all figures and analyses in the article have been provided. Additional demographic information was not uploaded as it was not used in any analysis reported in the text, and can be provided upon request in personal communication with the corresponding author, without additional restrictions.

Article and author information

Author details

  1. Assaf Breska

    Psychology, Helen Wills neuroscience institute, University of California, Berkeley, Berkeley, CA, United States
    For correspondence
    assaf.breska@berkeley.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6233-073X
  2. Richard B Ivry

    University of California, Berkeley, Berkeley, United States
    Competing interests
    Richard B Ivry, Senior editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4728-5130

Funding

National Institutes of Health (NS092079)

  • Richard B Ivry

National Institutes of Health (NS116883)

  • Richard B Ivry

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

Reviewing Editor

  1. Marisa Carrasco, New York University, United States

Ethics

Human subjects: All participants provided informed consent to participate in the study and for the publication of de-identified data. The study was approved by the Institutional Review Board at the University of California, Berkeley (CPHS# 2016-02-8439).

Version history

  1. Received: January 21, 2021
  2. Accepted: June 23, 2021
  3. Accepted Manuscript published: June 24, 2021 (version 1)
  4. Version of Record published: June 30, 2021 (version 2)

Copyright

© 2021, Breska & Ivry

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

  • 1,938
    views
  • 248
    downloads
  • 23
    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. Assaf Breska
  2. Richard B Ivry
(2021)
The human cerebellum is essential for modulating perceptual sensitivity based on temporal expectations
eLife 10:e66743.
https://doi.org/10.7554/eLife.66743

Share this article

https://doi.org/10.7554/eLife.66743

Further reading

    1. Neuroscience
    Alexandra L Jellinger, Rebecca L Suthard ... Steve Ramirez
    Research Article

    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.

    1. Neuroscience
    Alexandra H Leighton, Juliette E Cheyne, Christian Lohmann
    Research Article

    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.