Widespread nociceptive maps in the human neonatal somatosensory cortex

  1. Laura Jones  Is a corresponding author
  2. Madeleine Verriotis
  3. Robert J Cooper
  4. Maria Pureza Laudiano-Dray
  5. Mohammed Rupawala
  6. Judith Meek
  7. Lorenzo Fabrizi
  8. Maria Fitzgerald  Is a corresponding author
  1. University College London, United Kingdom
  2. University College London Hospitals NHS Foundation Trust, United Kingdom

Abstract

Topographic cortical maps are essential for spatial localisation of sensory stimulation and generation of appropriate task-related motor responses. Somatosensation and nociception are finely mapped and aligned in the adult somatosensory (S1) cortex, but in infancy, when pain behaviour is disorganised and poorly directed, nociceptive maps may be less refined. We compared the topographic pattern of S1 activation following noxious (clinically required heel lance) and innocuous (touch) mechanical stimulation of the same skin region in newborn infants (n=32) using multi-optode functional near-infrared spectroscopy (fNIRS). Within S1 cortex, touch and lance of the heel elicit localised, partially overlapping increases in oxygenated haemoglobin concentration (D[HbO]), but while touch activation was restricted to the heel area, lance activation extended into cortical hand regions. The data reveals a widespread cortical nociceptive map in infant S1, consistent with their poorly directed pain behaviour.

Data availability

All raw data files are open access and are available to download from Figshare (https://doi.org/10.6084/m9.figshare.13252388.v2).

The following data sets were generated

Article and author information

Author details

  1. Laura Jones

    Department of Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom
    For correspondence
    laura.a.jones@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5755-4977
  2. Madeleine Verriotis

    Department of Developmental Neuroscience, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3019-0370
  3. Robert J Cooper

    Department of Medical Physics and Biomedical Engineering, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Maria Pureza Laudiano-Dray

    Department of Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Mohammed Rupawala

    Department of Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Judith Meek

    Elizabeth Garrett Anderson Obstetric Wing, University College London Hospitals NHS Foundation Trust, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Lorenzo Fabrizi

    Department of Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9582-0727
  8. Maria Fitzgerald

    Department of Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom
    For correspondence
    m.fitzgerald@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4188-0123

Funding

Medical Research Council (MR/M006468/1)

  • Judith Meek
  • Lorenzo Fabrizi
  • Maria Fitzgerald

Medical Research Council (MR/L019248/1)

  • Lorenzo Fabrizi

Engineering and Physical Sciences Research Council (EP/N025946/1)

  • Robert J Cooper

Medical Research Council (MR/S003207/1)

  • Judith Meek
  • Lorenzo Fabrizi
  • Maria Fitzgerald

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

Ethics

Human subjects: Ethical approval for this study was given by the NHS Health Research Authority (London - Surrey Borders) and the study conformed to the standards set by the Declaration of Helsinki. Informed written parental consent was obtained before each study (REC no: 11/LO/0350; NIHR Portfolio Study ID: 12036). Separate media consent was obtained from the parent to use a photo of their child in academic publications (Figure 4a).

Copyright

© 2022, Jones 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

  • 1,034
    views
  • 248
    downloads
  • 10
    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. Laura Jones
  2. Madeleine Verriotis
  3. Robert J Cooper
  4. Maria Pureza Laudiano-Dray
  5. Mohammed Rupawala
  6. Judith Meek
  7. Lorenzo Fabrizi
  8. Maria Fitzgerald
(2022)
Widespread nociceptive maps in the human neonatal somatosensory cortex
eLife 11:e71655.
https://doi.org/10.7554/eLife.71655

Share this article

https://doi.org/10.7554/eLife.71655

Further reading

    1. Neuroscience
    Célian Bimbard, Flóra Takács ... Philip Coen
    Tools and Resources

    Electrophysiology has proven invaluable to record neural activity, and the development of Neuropixels probes dramatically increased the number of recorded neurons. These probes are often implanted acutely, but acute recordings cannot be performed in freely moving animals and the recorded neurons cannot be tracked across days. To study key behaviors such as navigation, learning, and memory formation, the probes must be implanted chronically. An ideal chronic implant should (1) allow stable recordings of neurons for weeks; (2) allow reuse of the probes after explantation; (3) be light enough for use in mice. Here, we present the ‘Apollo Implant’, an open-source and editable device that meets these criteria and accommodates up to two Neuropixels 1.0 or 2.0 probes. The implant comprises a ‘payload’ module which is attached to the probe and is recoverable, and a ‘docking’ module which is cemented to the skull. The design is adjustable, making it easy to change the distance between probes, the angle of insertion, and the depth of insertion. We tested the implant across eight labs in head-fixed mice, freely moving mice, and freely moving rats. The number of neurons recorded across days was stable, even after repeated implantations of the same probe. The Apollo implant provides an inexpensive, lightweight, and flexible solution for reusable chronic Neuropixels recordings.

    1. Neuroscience
    Georgin Jacob, RT Pramod, SP Arun
    Research Article

    Most visual tasks involve looking for specific object features. But we also often perform property-based tasks where we look for specific property in an image, such as finding an odd item, deciding if two items are same, or if an object has symmetry. How do we solve such tasks? These tasks do not fit into standard models of decision making because their underlying feature space and decision process is unclear. Using well-known principles governing multiple object representations, we show that displays with repeating elements can be distinguished from heterogeneous displays using a property we define as visual homogeneity. In behavior, visual homogeneity predicted response times on visual search, same-different and symmetry tasks. Brain imaging during visual search and symmetry tasks revealed that visual homogeneity was localized to a region in the object-selective cortex. Thus, property-based visual tasks are solved in a localized region in the brain by computing visual homogeneity.