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

  • 3,744
    views
  • 535
    downloads
  • 20
    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
    Sven Ohl, Martin Rolfs
    Research Article

    Detecting causal relations structures our perception of events in the world. Here, we determined for visual interactions whether generalized (i.e. feature-invariant) or specialized (i.e. feature-selective) visual routines underlie the perception of causality. To this end, we applied a visual adaptation protocol to assess the adaptability of specific features in classical launching events of simple geometric shapes. We asked observers to report whether they observed a launch or a pass in ambiguous test events (i.e. the overlap between two discs varied from trial to trial). After prolonged exposure to causal launch events (the adaptor) defined by a particular set of features (i.e. a particular motion direction, motion speed, or feature conjunction), observers were less likely to see causal launches in subsequent ambiguous test events than before adaptation. Crucially, adaptation was contingent on the causal impression in launches as demonstrated by a lack of adaptation in non-causal control events. We assessed whether this negative aftereffect transfers to test events with a new set of feature values that were not presented during adaptation. Processing in specialized (as opposed to generalized) visual routines predicts that the transfer of visual adaptation depends on the feature similarity of the adaptor and the test event. We show that the negative aftereffects do not transfer to unadapted launch directions but do transfer to launch events of different speeds. Finally, we used colored discs to assign distinct feature-based identities to the launching and the launched stimulus. We found that the adaptation transferred across colors if the test event had the same motion direction as the adaptor. In summary, visual adaptation allowed us to carve out a visual feature space underlying the perception of causality and revealed specialized visual routines that are tuned to a launch’s motion direction.

    1. Neuroscience
    Gergely F Turi, Sasa Teng ... Yueqing Peng
    Research Article

    Synchronous neuronal activity is organized into neuronal oscillations with various frequency and time domains across different brain areas and brain states. For example, hippocampal theta, gamma, and sharp wave oscillations are critical for memory formation and communication between hippocampal subareas and the cortex. In this study, we investigated the neuronal activity of the dentate gyrus (DG) with optical imaging tools during sleep-wake cycles in mice. We found that the activity of major glutamatergic cell populations in the DG is organized into infraslow oscillations (0.01–0.03 Hz) during NREM sleep. Although the DG is considered a sparsely active network during wakefulness, we found that 50% of granule cells and about 25% of mossy cells exhibit increased activity during NREM sleep, compared to that during wakefulness. Further experiments revealed that the infraslow oscillation in the DG was correlated with rhythmic serotonin release during sleep, which oscillates at the same frequency but in an opposite phase. Genetic manipulation of 5-HT receptors revealed that this neuromodulatory regulation is mediated by Htr1a receptors and the knockdown of these receptors leads to memory impairment. Together, our results provide novel mechanistic insights into how the 5-HT system can influence hippocampal activity patterns during sleep.