Chromatophore Activity during Natural Pattern Expression by the Squid Sepioteuthis lessoniana: Contributions of Miniature Oscillation

Mamiko Suzuki,Tetsuya Kimura,Kotaro Oka,Hiroto Ogawa,Kohji Hotta,Wulfila Gronenberg

doi:10.1371/journal.pone.0018244

Mamiko Suzuki, Tetsuya Kimura + Show 4 more

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https://doi.org/10.1371/journal.pone.0018244

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Abstract

Squid can rapidly change the chromatic patterns on their body. The patterns are created by the expansion and retraction of chromatophores. The chromatophore consists of a central pigment-containing cell surrounded by radial muscles that are controlled by motor neurons located in the central nervous system (CNS). In this study we used semi-intact squid (Sepioteuthis lessoniana) displaying centrally controlled natural patterns to analyze spatial and temporal activities of chromatophores located on the dorsal mantle skin. We found that chromatophores oscillated with miniature expansions/retractions at various frequencies, even when the chromatic patterns appear macroscopically stable. The frequencies of this miniature oscillation differed between “feature” and “background” areas of chromatic patterns. Higher frequencies occurred in feature areas, whereas lower frequencies were detected in background areas. We also observed synchronization of the oscillation during chromatic pattern expression. The expansion size of chromatophores oscillating at high frequency correlated with the number of synchronized chromatophores but not the oscillation frequency. Miniature oscillations were not observed in denervated chromatophores. These results suggest that miniature oscillations of chromatophores are driven by motor neuronal activities in the CNS and that frequency and synchrony of this oscillation determine the chromatic pattern and the expansion size, respectively.

Highlights

Unshelled cephalopods have the extraordinary ability to change their body color pattern in less than a second for camouflage and intraspecies communication, and the color patterning is often sustained for seconds or minutes [1]
We recorded three chromatic patterns – mottled dorsal mantle (MDM), fin edge spots (FES), and all dark (AD) (Fig. 1A) – spontaneously displayed by three un-anesthetized squid loosely fixed in a container
It is difficult to observe normal chromatic patterns at the single chromatophore level, we succeeded in observing chromatophore behavior in semi-intact squid displaying MDM, FES, and AD patterns (Fig. 1)

Summary

Introduction

Unshelled cephalopods have the extraordinary ability to change their body color pattern in less than a second for camouflage and intraspecies communication, and the color patterning is often sustained for seconds or minutes [1]. A chromatophore consists of a central pigment-containing cell surrounded by 19–27 radial muscles that are controlled by motor neurons in the brain [2,3,4,5]. In isolated skin preparations or in semi-intact preparations that contain the mantle and the brain, electrical stimulation of a chromatophore motor nerve induces twitch-like contractions of the radial muscles in several chromatophores [6,7,8]. Chromatophores can exhibit full expansion and intermediate expansion in which the muscles produce graded contractions These variations in the state of expansion (rather than intensity of pigment) of dark chromatophores are responsible for variations in contrast of the chromatic patterns produced [9,10,11,12]. Firing frequencies in motor neurons control the chromatic pattern

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