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

Paloma T. Gonzalez-Bellido, Alexia T. Scaros + Show 2 more

Open Access

https://doi.org/10.1016/j.isci.2018.01.001

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Abstract

SummaryThe 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.

Highlights

Coleoid cephalopods internalized their shell more than 400 Mya (Tanner et al, 2017)
The fin nerve provides an ideal substrate to test if the papillae motoneurons project parallel to the chromatophore motoneurons because (1) it is relatively easy to access in live anesthetized animals and (2) chromatophore motoneurons that target the posterior part of the mantle and the fins travel directly through the fin nerve (Gaston and Tublitz, 2004)
We severed the fin nerve in vivo under anesthesia, and upon recovery we noted that the fin was paralyzed and chromatophore activity had ceased from the posterior mantle tip to the posterior bar, but papillae expression was not affected (Figure 1F; n = 2; Movie S1A)

Summary

Introduction

Coleoid cephalopods (squid, cuttlefish, and octopus) internalized their shell more than 400 Mya (Tanner et al, 2017) Their soft bodies provided a unique set of opportunities related to motor control and rendered them more susceptible to predation. Different levels of structural complexity lead to larger and more intricate papillary shapes, with each species having a fixed repertoire of papillae shapes (Allen et al, 2013, 2014) This ability allows these benthic animals to be cryptic on substrates or masquerade as nearby objects, such as kelp, algae, or coral (Panetta et al, 2017), but the neural circuit and muscular anatomy that underlie it are unknown to date

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