Neural Control of Dynamic 3-Dimensional Skin Papillae for Cuttlefish Camouflage

Paloma T. Gonzalez-Bellido; Alexia T. Scaros; Roger T. Hanlon; Trevor J. Wardill

doi:10.1016/j.isci.2018.01.001

Neural Control of Dynamic 3-Dimensional Skin Papillae for Cuttlefish Camouflage

Paloma T. Gonzalez-Bellido, Alexia T. Scaros, Roger T. Hanlon, Trevor J. Wardill

Research output: Contribution to journal › Article › peer-review

22 Scopus citations

Abstract

The color and pattern changing abilities of octopus, squid, and cuttlefish via chromatophore neuro-muscular organs are unparalleled. Cuttlefish and octopuses also have a unique muscular hydrostat system in their skin. When this system is expressed, dermal bumps called papillae disrupt body shape and imitate the fine texture of surrounding objects, yet the control system is unknown. Here we report for papillae: (1)the motoneurons and the neurotransmitters that control activation and relaxation, (2)a physiologically fast expression and retraction system, and (3)a complex of smooth and striated muscles that enables long-term expression of papillae through sustained tension in the absence of neural input. The neural circuits controlling acute shape-shifting skin papillae in cuttlefish show homology to the iridescence circuits in squids. The sustained tension in papillary muscles for long-term camouflage utilizes muscle heterogeneity and points toward the existence of a “catch-like” mechanism that would reduce the necessary energy expenditure.

Original language	English (US)
Pages (from-to)	24-34
Number of pages	11
Journal	iScience
Volume	1
DOIs	https://doi.org/10.1016/j.isci.2018.01.001
State	Published - Mar 23 2018
Externally published	Yes

Bibliographical note

Funding Information:
This work was funded by an AFOSR grant no. FA9550-14-1-0134 , Isaac Newton Trust/Wellcome Trust ISSF/University of Cambridge Joint Research Grant ( 097814/Z/11/Z ) to P.T.G-B., and a Biotechnology and Biological Sciences Research Council David Phillips Fellowship (BBSRC, BB/L024667/1 ) to T.J.W. We thank MBL Equipment Resources, MBL Apparatus Department, and Zeiss Microscopes for assistance with equipment. We thank the MBL Central Microscopy facility for providing imaging resources and the Aquatic Resources Division of MBL for supplying squid. We thank Kate Feller for helping prepare electrodes for the filling and stimulation of nerves and Donovan Ventimiglia for fruitful discussions on logistical challenges.

Publisher Copyright:
© 2018 The Authors

Keywords

Animal Physiology
Evolutionary Biology
Neuroanatomy

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abstract = "The color and pattern changing abilities of octopus, squid, and cuttlefish via chromatophore neuro-muscular organs are unparalleled. Cuttlefish and octopuses also have a unique muscular hydrostat system in their skin. When this system is expressed, dermal bumps called papillae disrupt body shape and imitate the fine texture of surrounding objects, yet the control system is unknown. Here we report for papillae: (1)the motoneurons and the neurotransmitters that control activation and relaxation, (2)a physiologically fast expression and retraction system, and (3)a complex of smooth and striated muscles that enables long-term expression of papillae through sustained tension in the absence of neural input. The neural circuits controlling acute shape-shifting skin papillae in cuttlefish show homology to the iridescence circuits in squids. The sustained tension in papillary muscles for long-term camouflage utilizes muscle heterogeneity and points toward the existence of a “catch-like” mechanism that would reduce the necessary energy expenditure.",

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Neural Control of Dynamic 3-Dimensional Skin Papillae for Cuttlefish Camouflage

Abstract

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