Whole-organism characterization of Octopus neural connections

Using centimeter-field, isotropic, micron resolution X-ray histotomography

Abstract

Octopuses exhibit strikingly coordinated sensorimotor control of eight arms and hundreds of suckers, yet the microanatomical basis of this coordination has yet to be fully defined. Comprehensive mapping of the peripheral and central nervous systems in cephalopods and other organisms has been limited by the difficulty of imaging centimeter-scale tissue volumes at high resolution. To address this challenge, we developed a unique lens and camera system for micro-CT with a 10 mm-wide field-of-view (FOV) at 0.7 μm isotropic voxel size, capable of imaging within a single scan the same volume as ~48 scans using a conventional detector of comparable resolution. This system was used to reconstruct a whole-body 3D representation of a fully formed young Octopus bimaculoides with sufficient resolution to explore the entire animal in cytological detail. We were able to trace intricate 3D neurological pathways, including intramuscular nerve cords (INCs), previously uncharacterized linkages between the oral and aboral INCs, arm-to-arm connections through the nerve ring, and neural connections to and from each component. To facilitate further hypothesis generation, we share the full 16-bit 2.6 TB tomographic reconstruction and labeled connections via a customized implementation of Neuroglancer, a multiplanar, multiresolution web interface. This unique organism-wide perspective made possible by wide-field histotomography can be applied to other centimeter-scale organisms, organ systems, and tissues across taxa.

Visualizing Octopus Anatomy

Exploring the intricate neural structures

Authors

Andrew Sugarman1,2*, Daniel Vanselow1*, Stephen L. Senft9, Carolyn Zaino1, Maksim A. Yakovlev1, David Northover1,2, Justin D. Silverman2,3,4,5,6, Mee S. Ngu1, Khai C. Ang1, Steve Wang7, Patrick La Riviere8, Roger T. Hanlon9, Keith C. Cheng1,2,6

*Authors contributed equally

1Department of Pathology, Penn State College of Medicine, Hershey, Pennsylvania, USA; The Jake Gittlen Laboratories for Cancer Research, Penn State College of Medicine, Hershey, Pennsylvania, USA
2Program in Bioinformatics and Genomics, Pennsylvania State University, State College, Pennsylvania, USA
3College of Information Sciences and Technology, Pennsylvania State University, State College, Pennsylvania, USA
4Department of Statistics, Pennsylvania State University, State College, Pennsylvania, USA
5Department of Medicine, Penn State College of Medicine, Hershey, Pennsylvania, USA
6Institute for Computational and Data Science, Pennsylvania State University, State College, Pennsylvania, USA
7Mobile Imaging Innovations, Inc., Palatine, Illinois, USA
8Department of Radiology, The University of Chicago, USA
9The Marine Biological Laboratory, Woods Hole, MA, 02543, USA

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Contact

For inquiries or access to the dataset, please contact:

Daniel Vanselow
Email: dxv46@psu.edu
Andrew Sugarman
Email: aqs6915@psu.edu