2023Current BiologyOpen access

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

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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.

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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.

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Available 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.

Key concepts: Cuttlefish, Sepia, Cephalopod, Camouflage, Biology, octopus (software), Chromatophore, Squid

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