Membrane invaginations facilitate reversible water flux driving tunable iridescence in a dynamic biophotonic system
Biomolecular Science and Engineering Program, University of California, Santa Barbara, CA 93106-9611.Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 01/2013; 110(7). DOI: 10.1073/pnas.1217260110
Squids have used their tunable iridescence for camouflage and communication for millions of years; materials scientists have more recently looked to them for inspiration to develop new "biologically inspired" adaptive optics. Iridocyte cells produce iridescence through constructive interference of light with intracellular Bragg reflectors. The cell's dynamic control over the apparent lattice constant and dielectric contrast of these multilayer stacks yields the corresponding optical control of brightness and color across the visible spectrum. Here, we resolve remaining uncertainties in iridocyte cell structure and determine how this unusual morphology enables the cell's tunable reflectance. We show that the plasma membrane periodically invaginates deep into the iridocyte to form a potential Bragg reflector consisting of an array of narrow, parallel channels that segregate the resulting high refractive index, cytoplasmic protein-containing lamellae from the low-index channels that are continuous with the extracellular space. In response to control by a neurotransmitter, the iridocytes reversibly imbibe or expel water commensurate with changes in reflection intensity and wavelength. These results allow us to propose a comprehensive mechanism of adaptive iridescence in these cells from stimulation to color production. Applications of these findings may contribute to the development of unique classes of tunable photonic materials.
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Conference Paper: Luminance control of neurally tuneable skin iridescence in squid.[Show abstract] [Hide abstract]
ABSTRACT: Cephalopods create precise skin color and pattern displays for the purpose of signaling and camouflage. In squids, such visual trickery is achieved through the combined action of two color elements: pigmented chromatophores and structural iridophores (which produce iridescence). The neural control of chromatophores was recognized many decades ago but the system controlling dynamic iridescence remained in obscurity (although ACh was known to activate iridophores). To tackle this knowledge gap, we developed a novel physiological preparation in the squid Doryteuthis pealeii. Our results show that stimulation of dermal nerves shifts the spectral peak of the reflected light to shorter wavelengths (>145 nm) and increases the peak reflectance (>245 %) of innervated iridophores (Wardill et al. 2012). We also demonstrate that ACh is released within the iridophore layer and that extensive nerve branching is seen within each iridophore. The dynamic colour shift is significantly faster (17 s) than the peak reflectance increase (32 s) revealing two distinct control mechanisms. Responses from a structurally altered preparation indicate that the reflectin protein condensation mechanism (Izumi et al. 2010, Tao et al. 2010) explains the slower peak reflectance change, while a newly discovered water flux mechanism reducing platelet thickness (DeMartini et al. 2013) may explain the fast colour shift. Next, we traced the skin nerves towards the brain. While the chromatophore motorneurons descend directly from the brain, neural stimulation and dye back-filling revealed that cell bodies of the iridophore 'control' neurons are located in the stellate ganglion. Nonetheless, brain input is necessary for iridescence expression. Lastly, through behavioural tests, we showed that squids turn their iridescence on/off in response to lights on/off, respectively. However, the decline and rise of iridescence is slow, taking up to 1 hour and 5 minutes respectively, suggesting that iridescence may match light intensity during the diurnal cycle. In summary: (1) Squid iridescence is neurally activated. (2) The color and reflectance changes follow different dynamics. (3) Iridophores and chromatophores are innervated by different neurons. (4) The iridescence neural circuit has a relay in the peripheral stellate ganglia. (5) The rise and decline of iridescence is much slower than that of chromatophores and can be elicited by light intensity changes.