A brain atlas for the camouflaging dwarf cuttlefish, Sepia bandensis

Tessa G. Montague*, Isabelle J. Rieth, Sabrina Gjerswold-Selleck, Daniella Garcia-Rosales, Sukanya Aneja, Dana Elkis, Nanyan Zhu, Sabrina Kentis, Frederick A. Rubino, Adriana Nemes, Katherine Wang, Luke A. Hammond, Roselis Emiliano, Rebecca A. Ober, Jia Guo, Richard Axel*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

9 Scopus citations

Abstract

The coleoid cephalopods (cuttlefish, octopus, and squid) are a group of soft-bodied marine mollusks that exhibit an array of interesting biological phenomena, including dynamic camouflage, complex social behaviors, prehensile regenerating arms, and large brains capable of learning, memory, and problem-solving.1,2,3,4,5,6,7,8,9,10 The dwarf cuttlefish, Sepia bandensis, is a promising model cephalopod species due to its small size, substantial egg production, short generation time, and dynamic social and camouflage behaviors.11 Cuttlefish dynamically camouflage to their surroundings by changing the color, pattern, and texture of their skin. Camouflage is optically driven and is achieved by expanding and contracting hundreds of thousands of pigment-filled saccules (chromatophores) in the skin, which are controlled by motor neurons emanating from the brain. We generated a dwarf cuttlefish brain atlas using magnetic resonance imaging (MRI), deep learning, and histology, and we built an interactive web tool (https://www.cuttlebase.org/) to host the data. Guided by observations in other cephalopods,12,13,14,15,16,17,18,19,20 we identified 32 brain lobes, including two large optic lobes (75% the total volume of the brain), chromatophore lobes whose motor neurons directly innervate the chromatophores of the color-changing skin, and a vertical lobe that has been implicated in learning and memory. The brain largely conforms to the anatomy observed in other Sepia species and provides a valuable tool for exploring the neural basis of behavior in the experimentally facile dwarf cuttlefish.

Original languageEnglish (US)
Pages (from-to)2794-2801.e3
JournalCurrent Biology
Volume33
Issue number13
DOIs
StatePublished - Jul 10 2023

Funding

We wish to thank Connor Gibbons, Sonia Thomas, Telicia Lewis, Sarah Wilson, and Josh Barber for cuttlefish care; the Zuckerman Institute Cellular Imaging platform for instrument use and technical support; Lokke Highstein for IT support; Lucas Pozzo-Miller, Judit Pungor, Barbara Noro, Andrés Bendesky, Bret Grasse, Josh Barber, and Denise Piscopo for Cuttlebase testing; and Carrie Albertin for valuable discussions. This project was funded by a Zuckerman Institute MRI Seed Grant (T.G.M. and R.A.), the Howard Hughes Medical Institute Hanna H. Gray Fellowship (T.G.M.), the Zuckerman Institute BRAINYAC Program (R.E.), and the Howard Hughes Medical Institute (R.A.).

Keywords

  • MRI
  • behavior
  • brain atlas
  • camouflage
  • cephalopod
  • chromatophore
  • cuttlefish
  • deep learning
  • histology
  • mollusk

ASJC Scopus subject areas

  • General Biochemistry, Genetics and Molecular Biology
  • General Agricultural and Biological Sciences

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