Elucidating the control and development of skin patterning in cuttlefish

Abstract

Summary Few animals provide as objective a readout of their perceptual state as camouflaging cephalopods. Their skin display system includes an extensive array of pigment cells (chromatophores), each activated by radial muscles controlled by motoneurons. If one could track the individual expansion states of the chromatophores, one would obtain a quantitative description—and potentially even, a neural description by proxy— of the perceptual state of the animal in real time. We developed computational and analytical methods to achieve this in behaving animals, quantifying the state of tens of thousands of chromatophores at sixty frames per second, single-cell resolution, and over weeks. We could infer a statistical hierarchy of motor control, reveal an underlying low-dimensional structure to pattern dynamics, and uncover rules governing skin pattern development. This approach provides an objective description of complex perceptual behaviour, and powerful means to uncover organizational principles underlying neural systems function, dynamics, and morphogenesis.

Viewpoints: Approaches to defining and investigating fear

“…Only a few studies have used high-dimensional, multivariate measures of behavior. For instance, one can measure the change in the body surface over tens of thousands of little chromatophores that cuttlefish use to camouflage themselves, a measure that has been claimed to give us a direct readout of the animal’s perceptual state 91 . Rich measures in humans would also seem achievable: we need to measure in detail people’s movements in 3D space, their whole-body blood flow and so forth.…”

Tissue Transparency In Vivo

“…It is known that xanthine dehydrogenase oxidizes the yellow pteridine xanthopterin to the colorless pteridine leucopterin, and substances that affect this process also affect the chitin color in fly (Forrest et al, 1956) [27]. Many sea mollusks change the light absorption spectrum in different skin patches at will (Demski, 1994; Liuet al, 2017; Reiter et al, 2018) [28,29,30]. Similarly, rapid skin light absorption changes employing different specialized mechanisms are present in some anurans (Saenko et al, 2013; Teyssier et al, 2015) [31,32].…”

A living display system resolved pixel by pixel

“…Although this is undoubtedly beneficial in daily life, it is a serious drawback for neuroscientists: because much brain activity does not translate directly into behaviour, its function is difficult to determine. On page 361, Reiter et al 1 take a step towards circumventing this problem. The authors studied cuttlefish, which can change their appearance on the basis of their perception of the external world -in essence, they display some of their 'thoughts' on their skin.…”

“…See Article p.361 Modulations in muscle contraction determine whether or not the cells' pigments are displayed, producing a changing patterning system that the animal uses for camouflage. Reiter et al 1 used computer-vision tools to track tens of thousands of chromatophores. The authors' investigation reveals how skin pattern is controlled and how it varies over time.…”

“…M any great discoveries in modern physics depend on the invention of sensors based on new principles. For example, in 1887, an optical interferometera sensor based on wave interference -was used to disprove the existence of luminiferous aether, a universal medium through which light waves were thought to propagate 1 . In 1968, radio telescopes were used to discover extreme astronomical objects known as pulsars 2 .…”