Bio-inspired chromatophore network model generates dynamic skin patterns akin to those observed in cephalopods
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Cephalopod skin exhibits a wide range of dynamic visual displays, including traveling waves, light/dark flashes, and flickering, all generated by muscle-regulated expansion and retraction of pigment-filled elastic sacs known as chromatophores. While central neural control is essential for high-level body-wide pattern coordination, experimental evidence from excised and denervated skin reveals that intricate spatiotemporal patterns can also emerge spontaneously in the skin. This raises questions about the respective roles of central versus peripheral control. To determine the simplest control necessary to generate such patterns, we developed ChromatoNet, a biophysical model of chromatophore arrays that includes mechanical interactions on 1- and 2-dimensional lattices with the excitability properties of radial muscles. With minimal external input, our modified Morris–Lecar model reproduces a rich repertoire of skin dynamics, including spontaneous flickering as well as traveling and spiral waves. Both spontaneous and stimulus-evoked waves emerge at an intrinsic resonant frequency, determined by model parameters. Propagation speeds remain stable across conditions and are consistent with the range observed in denervated skin preparations. The model generates diverse output states in response to local couplings and the time-dependence and shape of the input stimulation, with little top-down direction. The results provide a proof-of-principle that chromatophore/muscle dynamics with minimal central neural driving can produce rich dynamic patterns.
Author summary
Cephalopods are capable of a wide variety of dynamic patterns for camouflage and communication, although much about how these effects are physically generated in the skin remains unknown. Cuttlefish and other cephalopods can alter their appearance with remarkable speed, producing body-wide changes in less than one second [12]. At a granular level this relies on thousands of pigment-filled saccules, “chromatophores” that expand and retract to generate shifting coordinated patterns that provide the optical illusion of movement across the skin. Each sacculus is actuated by 18-30 radial muscles whose orchestrated contraction pulls it out horizontally into a flat disc of visible pigment. While a rich variety of such coordinated changes in chromatophore actuation can be generated by electrical stimulation of the brain, and by active behavior, similar patterns also occur in excised and denervated skin, pointing to at least some role for purely local control. To investigate whether that role might be substantial, we built a simple model that includes core features of the known electrical activity of the muscles as well as experimentally motivated underlying geometrical connections that capture the way neighboring chromatophores may directly influence one another. Our system produces traveling waves, flickering, and other dynamic motifs observed in cephalopods in the wild, without requiring detailed instructions from a “brain.” Small changes to how the system is wired or perturbed lead to large shifts in modeled skin patterning and dynamics, suggesting that in nature, across species and even within an animal, the skin itself may be tuned to display a wide space of possible patterns.
