Abstract

The dynamics of living organisms are organized across many spatial scales. However, current cost-effective imaging systems can measure only a subset of these scales at once. We have created a scalable multi-camera array microscope (MCAM) that enables comprehensive high-resolution recording from multiple spatial scales simultaneously, ranging from structures that approach the cellular scale to large-group behavioral dynamics. By collecting data from up to 96 cameras, we computationally generate gigapixel-scale images and movies with a field of view over hundreds of square centimeters at an optical resolution of 18 µm. This allows us to observe the behavior and fine anatomical features of numerous freely moving model organisms on multiple spatial scales, including larval zebrafish, fruit flies, nematodes, carpenter ants, and slime mold. Further, the MCAM architecture allows stereoscopic tracking of the z-position of organisms using the overlapping field of view from adjacent cameras. Overall, by removing the bottlenecks imposed by single-camera image acquisition systems, the MCAM provides a powerful platform for investigating detailed biological features and behavioral processes of small model organisms across a wide range of spatial scales.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files;Source Data files and associated analysis code have been provided on https://gitlab.oit.duke.edu/ean26/gigapixelimaging.To view associated MCAM videos with flexible zooming capabilities see https://gigazoom.rc.duke.edu/team/Gigapixel%20behavioral%20and%20neural%20activity%20imaging%20with%20a%20novel%20multi-camera%20array%20microscope/Owl.Other MCAM source data can be viewed at https://gigazoom.rc.duke.edu/Raw MCAM video data as well as other relevant manuscript data for all experiments is publicly available at https://doi.org/10.7924/r4nv9kp8v.

Article and author information

Author details

  1. Eric Thomson

    Department of Neurobiology, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
  2. Mark Harfouche

    Ramona Optics Inc, Durham, United States
    Competing interests
    Mark Harfouche, is scientific co-founder at Ramona Optics Inc. which is commercializing and patenting themulti-camera array microscope..
  3. Kanghyun Kim

    Biomedical Engineering, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4557-9525
  4. Pavan Konda

    Biomedical Engineering, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
  5. Catherine W Seitz

    Department of Neurobiology, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
  6. Colin Cooke

    Biomedical Engineering, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
  7. Shiqi Xu

    Biomedical Engineering, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8450-9001
  8. Whitney S Jacobs

    Department of Neurobiology, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
  9. Robin Blazing

    Department of Neurobiology, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
  10. Yang Chen

    Department of Neurobiology, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
  11. Sunanda Sharma

    Ramona Optics Inc, Durham, United States
    Competing interests
    Sunanda Sharma, was an employee at Ramona Optics Inc., which is commercializing and patenting themulti-camera array microscope..
  12. Timothy W Dunn

    Department of Statistical Science, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9381-4630
  13. Jaehee Park

    Ramona Optics Inc, Durham, United States
    Competing interests
    Jaehee Park, was an employee at Ramona Optics Inc., which is commercializing and patenting themulti-camera array microscope..
  14. Roarke W Horstmeyer

    Biomedical Engineering, Duke University, Durham, United States
    For correspondence
    roarke.w.horstmeyer@duke.edu
    Competing interests
    Roarke W Horstmeyer, is a scientific co-founder at Ramona Optics Inc., which is commercializing and patenting the multi-camera array microscope..
  15. Eva A Naumann

    Department of Neurobiology, Duke University, Durham, United States
    For correspondence
    eva.naumann@duke.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7215-4717

Funding

Alfred P. Sloan Foundation (Sloan Foundation)

  • Eva A Naumann

Office of Research Infrastructure Programs, National Institutes of Health (SBIR R44OD024879)

  • Eric Thomson
  • Mark Harfouche
  • Sunanda Sharma
  • Timothy W Dunn
  • Eva A Naumann

National Cancer Institute (SBIR R44CA250877)

  • Mark Harfouche
  • Sunanda Sharma
  • Jaehee Park

National Science Foundation (NSF 2036439)

  • Mark Harfouche
  • Sunanda Sharma
  • Jaehee Park

National Institute of Biomedical Imaging and Bioengineering (SBIR R43EB030979-01)

  • Mark Harfouche
  • Sunanda Sharma
  • Jaehee Park

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 experiments followed the US Public Health Service Policy on Humane Care and Use of Laboratory Animals, under the protocol A083-21-04 approved by the Institutional Animal Care and Use Committee (IACUC) of Duke University School of Medicine. All experiments on zebrafish were performed according to these standards and every effort was made to minimize suffering.

Copyright

© 2022, Thomson 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

  • 3,242
    views
  • 488
    downloads
  • 19
    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. Eric Thomson
  2. Mark Harfouche
  3. Kanghyun Kim
  4. Pavan Konda
  5. Catherine W Seitz
  6. Colin Cooke
  7. Shiqi Xu
  8. Whitney S Jacobs
  9. Robin Blazing
  10. Yang Chen
  11. Sunanda Sharma
  12. Timothy W Dunn
  13. Jaehee Park
  14. Roarke W Horstmeyer
  15. Eva A Naumann
(2022)
Gigapixel imaging with a novel multi-camera array microscope
eLife 11:e74988.
https://doi.org/10.7554/eLife.74988

Share this article

https://doi.org/10.7554/eLife.74988

Further reading

    1. Neuroscience
    Hohyun Cho, Markus Adamek ... Peter Brunner
    Tools and Resources

    Determining the presence and frequency of neural oscillations is essential to understanding dynamic brain function. Traditional methods that detect peaks over 1/f noise within the power spectrum fail to distinguish between the fundamental frequency and harmonics of often highly non-sinusoidal neural oscillations. To overcome this limitation, we define fundamental criteria that characterize neural oscillations and introduce the cyclic homogeneous oscillation (CHO) detection method. We implemented these criteria based on an autocorrelation approach to determine an oscillation’s fundamental frequency. We evaluated CHO by verifying its performance on simulated non-sinusoidal oscillatory bursts and validated its ability to determine the fundamental frequency of neural oscillations in electrocorticographic (ECoG), electroencephalographic (EEG), and stereoelectroencephalographic (SEEG) signals recorded from 27 human subjects. Our results demonstrate that CHO outperforms conventional techniques in accurately detecting oscillations. In summary, CHO demonstrates high precision and specificity in detecting neural oscillations in time and frequency domains. The method’s specificity enables the detailed study of non-sinusoidal characteristics of oscillations, such as the degree of asymmetry and waveform of an oscillation. Furthermore, CHO can be applied to identify how neural oscillations govern interactions throughout the brain and to determine oscillatory biomarkers that index abnormal brain function.

    1. Neuroscience
    Jing Li, Chao Ning ... Chuan Zhou
    Research Article

    Female sexual receptivity is essential for reproduction of a species. Neuropeptides play the main role in regulating female receptivity. However, whether neuropeptides regulate female sexual receptivity during the neurodevelopment is unknown. Here, we found the peptide hormone prothoracicotropic hormone (PTTH), which belongs to the insect PG (prothoracic gland) axis, negatively regulated virgin female receptivity through ecdysone during neurodevelopment in Drosophila melanogaster. We identified PTTH neurons as doublesex-positive neurons, they regulated virgin female receptivity before the metamorphosis during the third-instar larval stage. PTTH deletion resulted in the increased EcR-A expression in the whole newly formed prepupae. Furthermore, the ecdysone receptor EcR-A in pC1 neurons positively regulated virgin female receptivity during metamorphosis. The decreased EcR-A in pC1 neurons induced abnormal morphological development of pC1 neurons without changing neural activity. Among all subtypes of pC1 neurons, the function of EcR-A in pC1b neurons was necessary for virgin female copulation rate. These suggested that the changes of synaptic connections between pC1b and other neurons decreased female copulation rate. Moreover, female receptivity significantly decreased when the expression of PTTH receptor Torso was reduced in pC1 neurons. This suggested that PTTH not only regulates female receptivity through ecdysone but also through affecting female receptivity associated neurons directly. The PG axis has similar functional strategy as the hypothalamic–pituitary–gonadal axis in mammals to trigger the juvenile–adult transition. Our work suggests a general mechanism underlying which the neurodevelopment during maturation regulates female sexual receptivity.