Cuttlefish Camouflage: Wearing Thoughts on the Skin and Biological Invisibility

The unique ability of cuttlefish, squid and octopuses to hide by imitating the colors and texture of their environment has fascinated natural scientists since the time of Aristotle. Uniquely among all animals, these mollusks control their appearance by the direct action of neurons onto expandable pixels, numbered in millions, located in their skin. Scientists at the Max Planck Institute for Brain Research and the Frankfurt Institute for Advanced Studies/Goethe University used this neuron-pixel correspondence to peer into the brain of cuttlefish, inferring the putative structure of control networks through analysis of skin pattern dynamics.

A common cuttlefish (Sepia officinalis)

Credit: © MPI for Brain Research / Stephan Junek

Cuttlefish, squid and octopus are a group of marine mollusks called coleoid cephalopods that once included ammonites, today only known as spiral fossils of the Cretaceous era. Modern coleoid cephalopods lost their external shells about 150 million years ago and took up an increasingly active predatory lifestyle. This development was accompanied by a massive increase in the size of their brains: modern cuttlefish and octopus have the largest brains (relative to body size) among invertebrates with a size comparable to that of reptiles and some mammals. They use these large brains to perform a range of intelligent behaviors, including the singular ability to change their skin pattern to camouflage, or hide, in their surroundings.

Cephalopods control camouflage by the direct action of their brain onto specialized skin cells called chromatophores, that act as biological color “pixels” on a soft skin display. Cuttlefish possess up to millions of chromatophores, each of which can be expanded and contracted to produce local changes in skin contrast. By controlling these chromatophores, cuttlefish can transform their appearance in a fraction of a second. They use camouflage to hunt, to avoid predators, but also to communicate.

To camouflage, cuttlefish do not match their local environment pixel by pixel. Instead, they seem to extract, through vision, a statistical approximation of their environment, and use these heuristics to select an adaptive camouflage out of a presumed large but finite repertoire of likely patterns, selected by evolution. The biological solutions to this statistical-matching problem are unknown. But because cuttlefish can solve it as soon as they hatch out of their egg, their solutions are probably innate, embedded in the cuttlefish brain and relatively simple. A team of scientists at the Max Planck Institute for Brain Research and at the Frankfurt Institute for Advanced Studies (FIAS)/Goethe University, led by MPI Director Gilles Laurent, developed techniques that begin to reveal those solutions.

Cuttlefish chromatophores are specialized cells containing an elastic sack of colored pigment granules. Each chromatophore is attached to minute radial muscles, themselves controlled by small numbers of motor neurons in the brain. When these motor neurons are activated, they cause the muscles to contract, expanding the chromatophore and displaying the pigment. When neural activity ceases, the muscles relax, the elastic pigment sack shrinks back, and the reflective underlying skin is revealed. Because single chromatophores receive input from small numbers of motor neurons, the expansion state of a chromatophore could provide an indirect measurement of motor neuron activity.

“We set out to measure the output of the brain simply and indirectly by imaging the pixels on the animal’s skin” says Laurent. Indeed, monitoring cuttlefish behavior with chromatophore resolution provided a unique opportunity to indirectly ‘image’ very large populations of neurons in freely behaving animals. Postdoc Sam Reiter from the Laurent Lab, the first author of this study, and his coauthors inferred motor neuron activity by analyzing the details of chromatophore co-fluctuations. In turn, by analyzing the co-variations of these inferred motor neurons, they could predict the structure of yet higher levels of control, ‘imaging’ increasingly more deeply into the cuttlefish brain through detailed statistical analysis of its chromatophore output.

Credit: © Nature

Cuttlefish: Wearing thoughts on the skin