1. Neuroscience
Download icon

Conservation of preparatory neural events in monkey motor cortex regardless of how movement is initiated

  1. Antonio Homero Lara
  2. Gamaleldin F Elsayed
  3. Andrew J Zimnik
  4. John Cunningham
  5. Mark M Churchland  Is a corresponding author
  1. Columbia University Medical Center, United States
  2. Columbia University, United States
Research Article
  • Cited 30
  • Views 2,050
  • Annotations
Cite this article as: eLife 2018;7:e31826 doi: 10.7554/eLife.31826

Abstract

A time-consuming preparatory stage is hypothesized to precede voluntary movement. A putative neural substrate of motor preparation occurs when a delay separates instruction and execution cues. When readiness is sustained during the delay, sustained neural activity is observed in motor and premotor areas. Yet whether delay-period activity reflects an essential preparatory stage is controversial. In particular, it has remained ambiguous whether delay-period-like activity appears before non-delayed movements. To overcome that ambiguity, we leveraged a recently developed analysis method that parses population responses into putatively preparatory and movement-related components. We examined cortical responses when reaches were initiated after an imposed delay, at a self-chosen time, or reactively with low latency and no delay. Putatively preparatory events were conserved across all contexts. Our findings support the hypothesis that an appropriate 'preparatory state' is consistently achieved before movement onset. However, our results reveal that this process can consume surprisingly little time.

Data availability

The data supporting this work is available via Dryad (http://dx.doi.org/10.5061/dryad.cf66jb7).

The following data sets were generated

Article and author information

Author details

  1. Antonio Homero Lara

    Department of Neuroscience, Columbia University Medical Center, New York, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Gamaleldin F Elsayed

    Department of Neuroscience, Columbia University Medical Center, New York, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Andrew J Zimnik

    Department of Neuroscience, Columbia University Medical Center, New York, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. John Cunningham

    Center for Theoretical Neuroscience, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Mark M Churchland

    Department of Neuroscience, Columbia University Medical Center, New York, United States
    For correspondence
    mc3502@columbia.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9123-6526

Funding

Alfred P. Sloan Foundation

  • Mark M Churchland

Kavli Foundation

  • Mark M Churchland

Klingenstein Third Generation Foundation

  • Mark M Churchland

Kinship Foundation

  • Mark M Churchland

National Institute of Neurological Disorders and Stroke (NS092350)

  • Antonio Homero Lara

Gatsby Charitable Foundation

  • John Cunningham
  • Mark M Churchland

Simons Foundation (SCGB#325171)

  • John Cunningham
  • Mark M Churchland

Simons Foundation (SCGB#325233)

  • John Cunningham
  • Mark M Churchland

Grossman Center for the Statistics of Mind

  • John Cunningham
  • Mark M Churchland

McKnight Endowment Fund for Neuroscience

  • John Cunningham
  • Mark M Churchland

National Institute of Neurological Disorders and Stroke (DP2 NS083037)

  • Mark M Churchland

National Institute of Neurological Disorders and Stroke (R01NS100066)

  • John Cunningham
  • Mark M Churchland

National Institute of Neurological Disorders and Stroke (NS104649)

  • John Cunningham
  • Mark M Churchland

National Eye Institute (P30 EY-019007)

  • Mark M Churchland

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

Ethics

Animal experimentation: All procedures were in accord with the US National Institutes of Health guidelines and were approved by the Columbia University Institutional Animal Care and Use Committee (AC-AAAQ7409).

Reviewing Editor

  1. Jennifer L Raymond, Stanford School of Medicine, United States

Publication history

  1. Received: September 8, 2017
  2. Accepted: July 26, 2018
  3. Accepted Manuscript published: August 22, 2018 (version 1)
  4. Version of Record published: August 28, 2018 (version 2)

Copyright

© 2018, Lara 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

  • 2,050
    Page views
  • 404
    Downloads
  • 30
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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)

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

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

Categories and tags

Research organism

Further reading

    1. Neuroscience

    Decoding the brain state-dependent relationship between pupil dynamics and resting state fMRI signal fluctuation

    Filip Sobczak et al.
    Research Article Updated

    Pupil dynamics serve as a physiological indicator of cognitive processes and arousal states of the brain across a diverse range of behavioral experiments. Pupil diameter changes reflect brain state fluctuations driven by neuromodulatory systems. Resting-state fMRI (rs-fMRI) has been used to identify global patterns of neuronal correlation with pupil diameter changes; however, the linkage between distinct brain state-dependent activation patterns of neuromodulatory nuclei with pupil dynamics remains to be explored. Here, we identified four clusters of trials with unique activity patterns related to pupil diameter changes in anesthetized rat brains. Going beyond the typical rs-fMRI correlation analysis with pupil dynamics, we decomposed spatiotemporal patterns of rs-fMRI with principal component analysis (PCA) and characterized the cluster-specific pupil–fMRI relationships by optimizing the PCA component weighting via decoding methods. This work shows that pupil dynamics are tightly coupled with different neuromodulatory centers in different trials, presenting a novel PCA-based decoding method to study the brain state-dependent pupil–fMRI relationship.

    1. Neuroscience

    Task-specific roles of local interneurons for inter- and intraglomerular signaling in the insect antennal lobe

    Debora Fusca, Peter Kloppenburg
    Research Article

    Local interneurons (LNs) mediate complex interactions within the antennal lobe, the primary olfactory system of insects, and the functional analog of the vertebrate olfactory bulb. In the cockroach Periplaneta americana, as in other insects, several types of LNs with distinctive physiological and morphological properties can be defined. Here, we combined whole-cell patch-clamp recordings and Ca2+ imaging of individual LNs to analyze the role of spiking and nonspiking LNs in inter- and intraglomerular signaling during olfactory information processing. Spiking GABAergic LNs reacted to odorant stimulation with a uniform rise in [Ca2+]i in the ramifications of all innervated glomeruli. In contrast, in nonspiking LNs, glomerular Ca2+ signals were odorant specific and varied between glomeruli, resulting in distinct, glomerulus-specific tuning curves. The cell type-specific differences in Ca2+ dynamics support the idea that spiking LNs play a primary role in interglomerular signaling, while they assign nonspiking LNs an essential role in intraglomerular signaling.

    1. Neuroscience

    Dendritic osmosensors modulate activity-induced calcium influx in oxytocinergic magnocellular neurons of the mouse PVN

    Wanhui Sheng et al.
    Research Article Updated

    Hypothalamic oxytocinergic magnocellular neurons have a fascinating ability to release peptide from both their axon terminals and from their dendrites. Existing data indicates that the relationship between somatic activity and dendritic release is not constant, but the mechanisms through which this relationship can be modulated are not completely understood. Here, we use a combination of electrical and optical recording techniques to quantify activity-induced calcium influx in proximal vs. distal dendrites of oxytocinergic magnocellular neurons located in the paraventricular nucleus of the hypothalamus (OT-MCNs). Results reveal that the dendrites of OT-MCNs are weak conductors of somatic voltage changes; however, activity-induced dendritic calcium influx can be robustly regulated by both osmosensitive and non-osmosensitive ion channels located along the dendritic membrane. Overall, this study reveals that dendritic conductivity is a dynamic and endogenously regulated feature of OT-MCNs that is likely to have substantial functional impact on central oxytocin release.