Fast and accurate edge orientation processing during object manipulation

  1. J Andrew Pruszynski  Is a corresponding author
  2. J Randall Flanagan
  3. Roland S Johansson
  1. Western University, Canada
  2. Queen's University, Canada
  3. Umea University, Sweden

Abstract

Quickly and accurately extracting information about a touched object's orientation is a critical aspect of dexterous object manipulation. However, the speed and acuity of tactile edge orientation processing with respect to the fingertips as reported in previous perceptual studies appear inadequate in these respects. Here we directly establish the tactile system's capacity to process edge-orientation information during dexterous manipulation. Participants extracted tactile information about edge orientation very quickly, using it within 200 ms of first touching the object. Participants were also strikingly accurate. With edges spanning the entire fingertip, edge-orientation resolution was better than 3° in our object manipulation task, which is several times better than reported in previous perceptual studies. Performance remained impressive even with edges as short as 2 mm, consistent with our ability to precisely manipulate very small objects. Taken together, our results radically redefine the spatial processing capacity of the tactile system.

Article and author information

Author details

  1. J Andrew Pruszynski

    Department of Physiology and Pharmacology, Western University, London, Canada
    For correspondence
    andrew.pruszynski@uwo.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0786-0081
  2. J Randall Flanagan

    Centre for Neuroscience Studies, Queen's University, Kingston, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Roland S Johansson

    Department of Integrative Medical Biology, Umea University, Umea, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3288-8326

Funding

Canadian Institutes of Health Research (Foundation Grant 3531979)

  • J Andrew Pruszynski

Vetenskapsrådet (Project 22209)

  • J Andrew Pruszynski

Canadian Institutes of Health Research (OOGP 82837)

  • J Randall Flanagan

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

Ethics

Human subjects: Twenty healthy people volunteered for these experiments. All participants provided written informed consent in accordance with the Declaration of Helsinki. The ethics committee at Umea University approved the study.

Copyright

© 2018, Pruszynski 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

  • 3,089
    views
  • 353
    downloads
  • 52
    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. J Andrew Pruszynski
  2. J Randall Flanagan
  3. Roland S Johansson
(2018)
Fast and accurate edge orientation processing during object manipulation
eLife 7:e31200.
https://doi.org/10.7554/eLife.31200

Share this article

https://doi.org/10.7554/eLife.31200

Further reading

    1. Neuroscience
    Ji Eun Ryu, Kyu-Won Shim ... Eun Young Kim
    Research Article

    The circadian clock, an internal time-keeping system orchestrates 24 hr rhythms in physiology and behavior by regulating rhythmic transcription in cells. Astrocytes, the most abundant glial cells, play crucial roles in CNS functions, but the impact of the circadian clock on astrocyte functions remains largely unexplored. In this study, we identified 412 circadian rhythmic transcripts in cultured mouse cortical astrocytes through RNA sequencing. Gene Ontology analysis indicated that genes involved in Ca2+ homeostasis are under circadian control. Notably, Herpud1 (Herp) exhibited robust circadian rhythmicity at both mRNA and protein levels, a rhythm disrupted in astrocytes lacking the circadian transcription factor, BMAL1. HERP regulated endoplasmic reticulum (ER) Ca2+ release by modulating the degradation of inositol 1,4,5-trisphosphate receptors (ITPRs). ATP-stimulated ER Ca2+ release varied with the circadian phase, being more pronounced at subjective night phase, likely due to the rhythmic expression of ITPR2. Correspondingly, ATP-stimulated cytosolic Ca2+ increases were heightened at the subjective night phase. This rhythmic ER Ca2+ response led to circadian phase-dependent variations in the phosphorylation of Connexin 43 (Ser368) and gap junctional communication. Given the role of gap junction channel (GJC) in propagating Ca2+ signals, we suggest that this circadian regulation of ER Ca2+ responses could affect astrocytic modulation of synaptic activity according to the time of day. Overall, our study enhances the understanding of how the circadian clock influences astrocyte function in the CNS, shedding light on their potential role in daily variations of brain activity and health.

    1. Neuroscience
    Gordon H Petty, Randy M Bruno
    Research Article

    Each sensory modality has its own primary and secondary thalamic nuclei. While the primary thalamic nuclei are well understood to relay sensory information from the periphery to the cortex, the role of secondary sensory nuclei is elusive. We trained head-fixed mice to attend to one sensory modality while ignoring a second modality, namely to attend to touch and ignore vision, or vice versa. Arrays were used to record simultaneously from the secondary somatosensory thalamus (POm) and secondary visual thalamus (LP). In mice trained to respond to tactile stimuli and ignore visual stimuli, POm was robustly activated by touch and largely unresponsive to visual stimuli. A different pattern was observed when mice were trained to respond to visual stimuli and ignore touch, with POm now more robustly activated during visual trials. This POm activity was not explained by differences in movements (i.e. whisking, licking, pupil dilation) resulting from the two tasks. Post hoc histological reconstruction of array tracks through POm revealed that subregions varied in their degree of plasticity. LP exhibited similar phenomena. We conclude that behavioral training reshapes activity in secondary thalamic nuclei. Secondary nuclei respond to the same behaviorally relevant, reward-predicting stimuli regardless of stimulus modality.