a living display system - nature researchgating how the geometry of these modules gives rise to the...

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Cloud by other objects in this galaxy. Either way, MACHOs cannot account for all of the dark matter in spiral galaxies, and the identity of this mysterious matter remains unknown. The microlensing experi- ments ultimately gave a negative result. How- ever, they have had a huge impact on many fields of modern astrophysics and have pro- vided a lot of excitement and stimulation for the whole astronomical community. Grzegorz Pietrzyński is at the Nicolaus Copernicus Astronomical Center, 00-716 Warsaw, Poland. e-mail: pietrzyn.at.camk.edu.pl 1. Planck Collaboration. Astron. Astrophys. 594, A13 (2016). 2. Trimble, V. Annu. Rev. Astron. Astrophys. 25, ADRIEN JOUARY & CHRISTIAN K. MACHENS O ur thoughts are hidden from sight, buried deep in the brain. Although this is undoubtedly beneficial in daily life, it is a serious drawback for neuro- scientists: because much brain activity does not translate directly into behaviour, its func- tion is difficult to determine. On page 361, Reiter et al. 1 take a step towards circum- venting this problem. The authors studied cuttlefish, which can change their appearance on the basis of their perception of the exter- nal world — in essence, they display some of their ‘thoughts’ on their skin. Using a range of state-of-the art techniques for computer vision, spectrometry and biomathematics, together with electrophysiology, the group exposes one of the most complex systems of motor coordination ever recorded. Cuttlefish, like squid and octopuses, are cephalopods. They have one of the largest brains among invertebrates, and can memo- rize complex spatial relationships or episodic events — abilities conventionally associ- ated with mammals and birds 2 . These brainy molluscs lack a protective shell, but have evolved a sophisticated display system that enables them to quickly transform the colour and patterning of their skin in response to a changing perception of the world around them, generating a broad range of patterns used for camouflage, deception of prey or sexual communication 3 . The cuttlefish skin contains millions of cells called chromatophores, which can pro- duce tiny dots of colour (yellow, orange, red, brown or black). If the radial muscles that control a chromatophore are relaxed, the pig- ments are imperceptible. But muscle contrac- tion produces a colourful pixel several tens of micrometres wide 4 (Fig. 1). When viewed at a distance, the millions of individual pixels form a complex image in the style of a poin- tillist painting, displayed on the animal’s skin. This process is orchestrated by many motor neurons, which innervate the radial muscles of individual chromatophores to control their contraction. Cuttlefish move rapidly, and because they are soft-bodied, frequently change shape. This constant flux presents a huge technical chal- lenge for studies of individual chromatophores, because such analyses require imaging tech- niques that can keep track of individual cells between frames of video footage. Reiter et al. found that each chromatophore is surrounded by a unique arrangement of neighbouring chromatophores, akin to a fingerprint that could be picked out in a single frame, despite changes in skin pattern. By following the char- acteristic fingerprint of each chromatophore in the video footage, the researchers were able to simultaneously track tens of thousands of cells over time. This enabled them to study how the control of individual chromatophores produces the complex skin patterns formed by the cell population as a whole. The authors first investigated the emergence of local skin motifs in which dark chromato- phores are surrounded by more-colourful ones. Observations over several weeks led to a surprising discovery: the difference in colour reflects a difference in age. The pigment of every chromatophore starts as yellow before turning red, then brown, and ending up as black. New chromatophores are generated throughout the life of the cuttlefish, and the group found that the ratio of black to coloured chromatophores is maintained by keeping a tight balance between the birth rate of new cells and the time it takes them to mature to a black colour. Reiter et al. showed that new chromatophores are generated in regions in which there are no existing ones, with a simple local-repulsion rule ensuring an even spread of the cells across the skin. The authors found that the same rule could explain the patterns of chromatophore formation seen in other species of cephalo- pod. These findings suggest that evolution- arily conserved molecular interactions govern chromatophore positioning — a proposal that should be investigated in the future. The rule also explains how the cuttlefish display system NEUROSCIENCE A living display system Pigmented cells in the skin of cuttlefish can contract or relax to produce different skin-colour patterns. Tracking the dynamics of these cells reveals how this display system develops, and how it is controlled. See Article p.361 Figure 1 | Thoughts on display. Chromatophores are pigmented cells found on the skin of cuttlefish. 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. In response to changes in the cuttlefish’s surroundings, the muscles that control groups of chromatophores contract or relax in unison, to produce a coordinated alteration in skin appearance. Relaxed chromatophore Contracted chromatophore 425–472 (1987). 3. Rubin, V. C., Ford, W. K. Jr & Thonnard, N. Astrophys. J. 238, 471–487 (1980). 4. Alcock, C. et al. Nature 365, 621–623 (1993). 5. Aubourg, E. et al. Nature 365, 623–625 (1993). 6. Paczyński, B. Astrophys. J. 304, 1–5 (1986). 7. Udalski, A. EPJ Web Conf. 152, 01002 (2017). 8. Soszyński, I. EPJ Web Conf. 152, 01001 (2017). 9. Gaudi, B. S. Annu. Rev. Astron. Astrophys. 50, 411–453 (2012). 10.Wyrzykowski, Ł. et al. Mon. Not. R. Astron. Soc. 413, 493–508 (2011). 350 | NATURE | VOL 562 | 18 OCTOBER 2018 NEWS & VIEWS RESEARCH ©2018SpringerNatureLimited.Allrightsreserved.

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Page 1: A living display system - Nature Researchgating how the geometry of these modules gives rise to the camouflage motifs seen in cuttlefish in their natural environment. Finally, the

Cloud by other objects in this galaxy.Either way, MACHOs cannot account

for all of the dark matter in spiral galaxies, and the identity of this mysterious matter remains unknown. The microlensing experi-ments ultimately gave a negative result. How-ever, they have had a huge impact on many fields of modern astrophysics and have pro-vided a lot of excitement and stimulation

for the whole astronomical community. ■

Grzegorz Pietrzyński is at the Nicolaus Copernicus Astronomical Center, 00-716 Warsaw, Poland.e-mail: pietrzyn.at.camk.edu.pl

1. Planck Collaboration. Astron. Astrophys. 594, A13 (2016).

2. Trimble, V. Annu. Rev. Astron. Astrophys. 25,

A D R I E N J O U A R Y & C H R I S T I A N K . M A C H E N S

Our thoughts are hidden from sight, buried deep in the brain. Although this is undoubtedly beneficial in

daily life, it is a serious drawback for neuro-scientists: because much brain activity does not translate directly into behaviour, its func-tion is difficult to determine. On page 361, Reiter et al.1 take a step towards circum-venting this problem. The authors studied cuttlefish, which can change their appearance on the basis of their perception of the exter-nal world — in essence, they display some of their ‘thoughts’ on their skin. Using a range of state-of-the art techniques for computer vision, spectrometry and biomathematics, together with electrophysiology, the group exposes one of the most complex systems of

motor coordination ever recorded.Cuttlefish, like squid and octopuses, are

cephalopods. They have one of the largest brains among invertebrates, and can memo-rize complex spatial relationships or episodic events — abilities conventionally associ-ated with mammals and birds2. These brainy molluscs lack a protective shell, but have evolved a sophisticated display system that enables them to quickly transform the colour and patterning of their skin in response to a changing perception of the world around them, generating a broad range of patterns used for camouflage, deception of prey or sexual communication3.

The cuttlefish skin contains millions of cells called chromatophores, which can pro-duce tiny dots of colour (yellow, orange, red, brown or black). If the radial muscles that

control a chromatophore are relaxed, the pig-ments are imperceptible. But muscle contrac-tion produces a colourful pixel several tens of micro metres wide4 (Fig. 1). When viewed at a distance, the millions of individual pixels form a complex image in the style of a poin-tillist painting, displayed on the animal’s skin. This process is orchestrated by many motor neurons, which innervate the radial muscles of individual chromatophores to control their contraction.

Cuttlefish move rapidly, and because they are soft-bodied, frequently change shape. This constant flux presents a huge technical chal-lenge for studies of individual chromato phores, because such analyses require imaging tech-niques that can keep track of individual cells between frames of video footage. Reiter et al. found that each chromatophore is surrounded by a unique arrangement of neighbouring chromatophores, akin to a fingerprint that could be picked out in a single frame, despite changes in skin pattern. By following the char-acteristic fingerprint of each chromato phore in the video footage, the researchers were able to simultaneously track tens of thousands of cells over time. This enabled them to study how the control of individual chromatophores produces the complex skin patterns formed by the cell population as a whole.

The authors first investigated the emergence of local skin motifs in which dark chromato-phores are surrounded by more-colourful ones. Observations over several weeks led to a surprising discovery: the difference in colour reflects a difference in age. The pigment of every chromatophore starts as yellow before turning red, then brown, and ending up as black. New chromatophores are generated throughout the life of the cuttlefish, and the group found that the ratio of black to coloured chromatophores is maintained by keeping a tight balance between the birth rate of new cells and the time it takes them to mature to a black colour.

Reiter et al. showed that new chromatophores are generated in regions in which there are no existing ones, with a simple local-repulsion rule ensuring an even spread of the cells across the skin. The authors found that the same rule could explain the patterns of chromato phore formation seen in other species of cephalo-pod. These findings suggest that evolution-arily conserved molecular inter actions govern chromatophore positioning — a proposal that should be investigated in the future. The rule also explains how the cuttlefish display system

N E U R O S C I E N C E

A living display systemPigmented cells in the skin of cuttlefish can contract or relax to produce different skin-colour patterns. Tracking the dynamics of these cells reveals how this display system develops, and how it is controlled. See Article p.361

Figure 1 | Thoughts on display. Chromatophores are pigmented cells found on the skin of cuttlefish. 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. In response to changes in the cuttlefish’s surroundings, the muscles that control groups of chromatophores contract or relax in unison, to produce a coordinated alteration in skin appearance.

Relaxedchromatophore

Contractedchromatophore

425–472 (1987).3. Rubin, V. C., Ford, W. K. Jr & Thonnard, N.

Astrophys. J. 238, 471–487 (1980).4. Alcock, C. et al. Nature 365, 621–623 (1993).5. Aubourg, E. et al. Nature 365, 623–625 (1993).6. Paczyński, B. Astrophys. J. 304, 1–5 (1986).7. Udalski, A. EPJ Web Conf. 152, 01002 (2017).8. Soszyński, I. EPJ Web Conf. 152, 01001 (2017).9. Gaudi, B. S. Annu. Rev. Astron. Astrophys. 50,

411–453 (2012).10. Wyrzykowski, Ł. et al. Mon. Not. R. Astron. Soc. 413,

493–508 (2011).

3 5 0 | N A T U R E | V O L 5 6 2 | 1 8 O C T O B E R 2 0 1 8

NEWS & VIEWSRESEARCH

© 2018

Springer

Nature

Limited.

All

rights

reserved. ©

2018

Springer

Nature

Limited.

All

rights

reserved.

Page 2: A living display system - Nature Researchgating how the geometry of these modules gives rise to the camouflage motifs seen in cuttlefish in their natural environment. Finally, the

L I A N G L I U

Many great discoveries in modern physics depend on the invention of sensors based on new principles. For

example, in 1887, an optical interferometer — a sensor based on wave interference — was used to disprove the existence of luminiferous aether, a universal medium through which light waves were thought to propagate1. In 1968, radio telescopes were used to discover

extreme astronomical objects known as pulsars2. And in 2016, a laser interferometer was used to detect gravitational waves3. On page 391, Becker et al.4 demonstrate how space-borne sensors based on an exotic state of matter called a Bose–Einstein condensate might provide the next big discovery.

A fundamental principle of quantum physics is wave–particle duality, which describes elementary particles in terms of quantum-mechanical waves (de Broglie

Q U A N T U M P H Y S I C S

Exploring the Universe with matter wavesAn exotic ultracold gas known as a Bose–Einstein condensate has been produced and studied in space. Such gases could be used to build quantum sensors that probe the properties of the Universe with extreme precision. See Letter p.391

Figure 1 | Production and application of a Bose–Einstein condensate. a, In quantum physics, matter can behave like a wave that has a particular wavelength. For a cloud of hot atoms, these wavelengths are so short that each atom can be regarded as an individual object. If the atoms are cooled, the wavelengths become longer. And if the atoms are cooled to a critical temperature, the wavelengths are large enough to cover the extent of the atomic cloud. Most of the atoms condense into a state known as a Bose–Einstein condensate (BEC), in which they can be regarded as a single matter wave (red). Becker et al.4 have produced and analysed a BEC in space. b, BECs can be used in sensors known as atom interferometers, in which laser beams cause a matter wave to split into two and then recombine to generate an interference pattern that is sensitive to external perturbations.

Hot atom

Laser beam

Matter wave

Cooling Cooling

Interference pattern

a

b

maintains a steady functionality despite the animal’s continuously increasing body size.

Next, the researchers investigated the dynamics of radial-muscle contrac-tion and relaxation around tens of thou-sands of chromato phores. They discovered co-variations in muscle movements at many spatial scales, indicating that chromatophores are regulated by modules of motor neurons that function in synchrony, and that operate on skin patches of different sizes. The smallest modules consisted of fewer than ten adjacent chromato-phores of the same colour. By contrast, larger modules, when contracted in synchrony, dis-played more-complex shapes, such as rings, rectangles or disjointed structures resembling eye spots. These results pave the way to investi-gating how the geometry of these modules gives rise to the camouflage motifs seen in cuttlefish in their natural environment.

Finally, the authors studied chromatophore responses to changes in the cephalopod’s visual environment, for instance when an investiga-tor passed a hand above the animal, causing its skin pattern to change. They found that chromatophores display a highly coordi-nated choreography over time — remini scent of the choreography of neuronal-popula-tion activity during movement5. Strikingly, chromato phores went through the same sequence of contractions and relaxations each time the test was repeated. This indicates a remarkable level of fine control by motor neu-rons, and highlights the potential of cuttlefish studies to deepen our understanding of com-plex motor systems.

Reiter et al. have achieved a breakthrough that will allow researchers to study this motor system in much more detail than was previ-ously possible. The next challenge will be to determine how cuttlefish change the 3D texture of their skin for camouflage on sand, algae or corals. This process involves sets of muscles called papillae that create bumps and lumps. To gain a complete understanding of the animal’s display system, chromatophores and papillae should be studied together.

The authors’ advance also has implications for visual perception and motor control more generally. For instance, we should now be able to gain a better understanding of texture per-ception in both cephalopods and their verte-brate predators, by investigating which visual features in the cuttlefish environment drive skin-pattern choices. Given that we can read the perceptual state of cuttlefish on their skin, it might also become easier to investigate the brain activity that translates visual perceptions into motor outputs.

Furthermore, because cuttlefish coordinate millions of muscles simultaneously, they could provide insights into the principles under ly ing motor coordination. The authors’ findings suggest a hierarchical organization of motor-neuron modules, in which higher-level modules control complex, global skin patterns and lower-level modules control simple, local

motifs. Such a hierarchy of motor controllers has long been thought to be a key principle underlying behaviour in most animals, includ-ing humans6. However, recording the activity of every muscle in a human is currently impos-sible. The simple readout provided by the skin-display system of cuttlefish could well lead us to a greater understanding of motor control. ■

Adrien Jouary and Christian K. Machens are in the Champalimaud Neuroscience Programme, Champalimaud Centre for the

Unknown, 1400–038 Lisbon, Portugal.e-mails: [email protected]; [email protected]

1. Reiter, S. et al. Nature 562, 361–366 (2018).2. Mather, J. A. & Dickel, L. Curr. Opin. Behav. Sci. 16,

131–137 (2017).3. Hanlon, R. T. & Messenger, J. B. Phil. Trans. R. Soc. B

320, 437–487 (1988).4. Messenger, J. B. Biol. Rev. 76, 473–528 (2001).5. Churchland, M. M. et al. Nature 487, 51–56 (2012).6. Lashley, K. S. in Cerebral Mechanisms in Behavior

(ed. Jefffries, L. A.) 112–136 (Wiley, 1951).

1 8 O C T O B E R 2 0 1 8 | V O L 5 6 2 | N A T U R E | 3 5 1

NEWS & VIEWS RESEARCH

© 2018

Springer

Nature

Limited.

All

rights

reserved. ©

2018

Springer

Nature

Limited.

All

rights

reserved.