A deep learning pipeline for three-dimensional brain-wide mapping of local neuronal ensembles in teravoxel light-sheet microscopy.

Journal: Nature methods
PMID:

Abstract

Teravoxel-scale, cellular-resolution images of cleared rodent brains acquired with light-sheet fluorescence microscopy have transformed the way we study the brain. Realizing the potential of this technology requires computational pipelines that generalize across experimental protocols and map neuronal activity at the laminar and subpopulation-specific levels, beyond atlas-defined regions. Here, we present artficial intelligence-based cartography of ensembles (ACE), an end-to-end pipeline that employs three-dimensional deep learning segmentation models and advanced cluster-wise statistical algorithms, to enable unbiased mapping of local neuronal activity and connectivity. Validation against state-of-the-art segmentation and detection methods on unseen datasets demonstrated ACE's high generalizability and performance. Applying ACE in two distinct neurobiological contexts, we discovered subregional effects missed by existing atlas-based analyses and showcase ACE's ability to reveal localized or laminar neuronal activity brain-wide. Our open-source pipeline enables whole-brain mapping of neuronal ensembles at a high level of precision across a wide range of neuroscientific applications.

Authors

  • Ahmadreza Attarpour
  • Jonas Osmann
    Physical Sciences, Sunnybrook Research Institute, Toronto, Ontario, Canada.
  • Anthony Rinaldi
    Physical Sciences, Sunnybrook Research Institute, Toronto, Ontario, Canada.
  • Tianbo Qi
    Department of Neuroscience, Dorris Neuroscience Center, The Scripps Research Institute, San Diego, CA, USA.
  • Neeraj Lal
    Department of Neuroscience, Dorris Neuroscience Center, The Scripps Research Institute, San Diego, CA, USA.
  • Shruti Patel
    Physical Sciences, Sunnybrook Research Institute, Toronto, Ontario, Canada.
  • Matthew Rozak
    Department of Medical Biophysics, University of Toronto, Toronto, Ontario, Canada.
  • Fengqing Yu
    Physical Sciences, Sunnybrook Research Institute, Toronto, Ontario, Canada.
  • Newton Cho
    Defitech Center for Interventional Neurotherapies (.NeuroRestore), CHUV/UNIL/EPFL, Lausanne, Switzerland.
  • Jordan Squair
    Defitech Center for Interventional Neurotherapies (.NeuroRestore), CHUV/UNIL/EPFL, Lausanne, Switzerland.
  • JoAnne McLaurin
    Biological Sciences, Sunnybrook Research Institute, Toronto, Ontario, Canada.
  • Misha Raffiee
    Department of Bioengineering, Stanford University, Stanford, CA, USA.
  • Karl Deisseroth
    Department of Bioengineering, Stanford University, Stanford, CA 94305, USA. Department of Psychiatry and Behavioral Sciences and the Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA.
  • GrĂ©goire Courtine
  • Li Ye
    Guangxi Key Laboratory of AIDS Prevention and Treatment & Guangxi Universities Key Laboratory of Prevention and Control of Highly Prevalent Disease, School of Public Health, Guangxi Medical University, Nanning 530021, Guangxi, China.
  • Bojana Stefanovic
    Department of Medical Biophysics, University of Toronto, Toronto, Ontario, Canada.
  • Maged Goubran
    Imaging Research Laboratories, Robarts Research Institute, London, ON, Canada N6A 5K8; Biomedical Engineering Graduate Program, Western University, London, ON, Canada. Electronic address: mgoubran@robarts.ca.