Attentional amplification of neural codes for number independent of other quantities along the dorsal visual stream

  1. Elisa Castaldi  Is a corresponding author
  2. Manuela Piazza
  3. Stanislas Dehaene
  4. Alexandre Vignaud
  5. Evelyn Eger
  1. INSERM, France
  2. University of Trento, Italy
  3. INSERM-CEA, France

Abstract

Humans and other animals base important decisions on estimates of number, and intraparietal cortex is thought to provide a crucial substrate of this ability. However, it remains debated whether an independent neuronal processing mechanism underlies this 'number sense' or whether number is instead judged indirectly on the basis of other quantitative features. We performed high-resolution 7 Tesla fMRI while adult human volunteers attended either to the numerosity or an orthogonal dimension (average item size) of visual dot arrays. Along the dorsal visual stream, numerosity explained a significant amount of variance in activation patterns, above and beyond non-numerical dimensions. Its representation was selectively amplified and progressively enhanced across the hierarchy when task relevant. Our results reveal a sensory extraction mechanism yielding information on numerosity separable from other dimensions already at early visual stages and suggest that later regions along the dorsal stream are most important for explicit manipulation of numerical quantity.

Data availability

Individual subjects' data points for behavioural and fMRI results for all regions of interest, corresponding to figure 2A, 3C, 5, 3-supplementary 1 and 2, 5-supplementary 1-2 are provided as .csv files. The maps displayed in figure 2B-D and 3B are provided in a format readable with Freesurfer/Freeview, one of the most widely used free neuroimaging softwares. The functional imaging dataset is available via the Open Science Framework (osf.io/6zch2).

The following data sets were generated

Article and author information

Author details

  1. Elisa Castaldi

    Cognitive Neuroimaging Unit, CEA DRF/JOLIOT, INSERM, Université Paris-Sud, Université Paris-Saclay, NeuroSpin center, INSERM, Gif/Yvette, France
    For correspondence
    elisa.castaldi@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0327-6697
  2. Manuela Piazza

    Center for Mind/Brain Sciences, University of Trento, Trento, Italy
    Competing interests
    The authors declare that no competing interests exist.
  3. Stanislas Dehaene

    Cognitive Neuroimaging Unit, CEA DRF/JOLIOT, INSERM, Université Paris-Sud, Université Paris-Saclay, NeuroSpin center, INSERM, Gif/Yvette, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Alexandre Vignaud

    UNIRS, CEA DRF/JOLIOT, Université Paris-Saclay, NeuroSpin center, France, INSERM-CEA, Gif/Yvette, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Evelyn Eger

    Cognitive Neuroimaging Unit, CEA DRF/JOLIOT, INSERM, Université Paris-Sud, Université Paris-Saclay, NeuroSpin center, INSERM, Gif/Yvette, France
    Competing interests
    The authors declare that no competing interests exist.

Funding

Agence Nationale de la Recherche (ANR-14-CE13-0020-01)

  • Evelyn Eger

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

Ethics

Human subjects: The study was approved by the regional ethics committee (CPP Ile de France VII, Hôpital de Bicêtre, No. 15-007) and all participants gave written informed consent.

Copyright

© 2019, Castaldi 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

  • 2,712
    views
  • 347
    downloads
  • 53
    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. Elisa Castaldi
  2. Manuela Piazza
  3. Stanislas Dehaene
  4. Alexandre Vignaud
  5. Evelyn Eger
(2019)
Attentional amplification of neural codes for number independent of other quantities along the dorsal visual stream
eLife 8:e45160.
https://doi.org/10.7554/eLife.45160

Share this article

https://doi.org/10.7554/eLife.45160

Further reading

    1. Neuroscience
    Sainan Liu, Jiepin Huang ... Yan Yang
    Research Article

    Social relationships guide individual behavior and ultimately shape the fabric of society. Primates exhibit particularly complex, differentiated, and multidimensional social relationships, which form interwoven social networks, reflecting both individual social tendencies and specific dyadic interactions. How the patterns of behavior that underlie these social relationships emerge from moment-to-moment patterns of social information processing remains unclear. Here, we assess social relationships among a group of four monkeys, focusing on aggression, grooming, and proximity. We show that individual differences in social attention vary with individual differences in patterns of general social tendencies and patterns of individual engagement with specific partners. Oxytocin administration altered social attention and its relationship to both social tendencies and dyadic relationships, particularly grooming and aggression. Our findings link the dynamics of visual information sampling to the dynamics of primate social networks.

    1. Neuroscience
    Mihály Vöröslakos, Yunchang Zhang ... György Buzsáki
    Tools and Resources

    Brain states fluctuate between exploratory and consummatory phases of behavior. These state changes affect both internal computation and the organism’s responses to sensory inputs. Understanding neuronal mechanisms supporting exploratory and consummatory states and their switching requires experimental control of behavioral shifts and collecting sufficient amounts of brain data. To achieve this goal, we developed the ThermoMaze, which exploits the animal’s natural warmth-seeking homeostatic behavior. By decreasing the floor temperature and selectively heating unmarked areas, we observed that mice avoided the aversive state by exploring the maze and finding the warm spot. In its design, the ThermoMaze is analogous to the widely used water maze but without the inconvenience of a wet environment and, therefore, allows the collection of physiological data in many trials. We combined the ThermoMaze with electrophysiology recording, and report that spiking activity of hippocampal CA1 neurons during sharp-wave ripple events encode the position of mice. Thus, place-specific firing is not confined to locomotion and associated theta oscillations but persist during waking immobility and sleep at the same location. The ThermoMaze will allow for detailed studies of brain correlates of immobility, preparatory–consummatory transitions, and open new options for studying behavior-mediated temperature homeostasis.