Neural control of tuneable skin iridescence in squid

Abstract

Fast dynamic control of skin coloration is rare in the animal kingdom, whether it be pigmentary or structural. Iridescent structural coloration results when nanoscale structures disrupt incident light and selectively reflect specific colours. Unlike animals with fixed iridescent coloration (e.g. butterflies), squid iridophores (i.e. aggregations of iridescent cells in the skin) produce dynamically tuneable structural coloration, as exogenous application of acetylcholine (ACh) changes the colour and brightness output. Previous efforts to stimulate iridophores neurally or to identify the source of endogenous ACh were unsuccessful, leaving researchers to question the activation mechanism. We developed a novel neurophysiological preparation in the squid Doryteuthis pealeii and demonstrated that electrical stimulation of neurons in the skin shifts the spectral peak of the reflected light to shorter wavelengths (greater than 145 nm) and increases the peak reflectance (greater than 245%) of innervated iridophores. We show ACh is released within the iridophore layer and that extensive nerve branching is seen within the iridophore. The dynamic colour shift is significantly faster (17 s) than the peak reflectance increase (32 s), revealing two distinct mechanisms. Responses from a structurally altered preparation indicate that the reflectin protein condensation mechanism explains peak reflectance change, while an undiscovered mechanism causes the fast colour shift.

Structures, Organization, and Function of Reflectin Proteins in Dynamically Tunable Reflective Cells

“…The iridocyte's optical responsiveness driven by ACh shows a strong correlation (Fig. 9), with the dorsal iridocytes displaying the most dramatic changes in iridescence (temporally progressing from transparent to red, then continuing through the spectrum to blue (13,23)). Iridocytes toward the ventral surface are less responsive to ACh, and the ventral iridocytes blush only slightly, an effect barely noticeable to the eye and not distinguishable above background in the recorded spectra.…”

Expression of squid iridescence depends on environmental luminance and peripheral ganglion control

“…(E) At maximum excitation, the iridophore color in animals whose stellate connective was severed 7 and 15 days previous to the experiment (data for both groups pooled; supplementary material Fig. S2) was not significantly different to that obtained in intact animals (dark solid line) (data from Wardill et al, 2012). Gray shading represents the standard deviation.…”

“…The animals were tested either 7 (N=9) or 15 days (N=8) post-denervation. The same protocol as that of Wardill et al (Wardill et al, 2012) was used, so that results between the two studies could be compared. Briefly, nerve fascicles named dermal nerves, which radiate from the base of the large fin nerve and innervate the skin, were exposed and stimulated via suction electrode.…”

Membrane invaginations facilitate reversible water flux driving tunable iridescence in a dynamic biophotonic system

“…For this reason, the tunable photonics of squids have long been a source of intrigue and inspiration to materials scientists (10)(11)(12). Although it is known that the neurotransmitter acetylcholine (ACh) activates a signal-transduction cascade to drive the changes in periodicity of the reflectors (7,13), and the nerve cells delivering this signal recently have been identified (14), details of the molecular mechanisms and cellular architectures governing the biophotonic processes themselves have remained elusive.…”