Neural Control of Dynamic 3-Dimensional Skin Papillae for Cuttlefish Camouflage

Gonzalez-Bellido, Paloma T.; Scaros, Alexia T.; Hanlon, Roger T.; Wardill, Trevor J.

doi:10.1016/j.isci.2018.01.001

Cited by 29 publications

(9 citation statements)

References 48 publications

(76 reference statements)

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“…Octopuses are among the largest brained invertebrates and demonstrate a range of sophisticated behaviours 16 , making them ideal for testing the generality of two-stage sleep. Sleeping cephalopods 17 have been observed to undergo rhythmic bouts of body twitches and rapid changes in skin patterning 6 , 18 , mediated by neural control of large populations of skin pigment cells (chromatophores) 19 among other specialized cell types 20 . In octopus, this has been termed ‘active sleep’ (AS) and is accompanied by an increased arousal threshold, one of several criteria of sleep 15 , 21 .…”

Section: Mainmentioning

confidence: 99%

Wake-like skin patterning and neural activity during octopus sleep

Pophale,

Shimizu,

Mano

et al. 2023

Nature

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While sleeping, many vertebrate groups alternate between at least two sleep stages: rapid eye movement and slow wave sleep1–4, in part characterized by wake-like and synchronous brain activity, respectively. Here we delineate neural and behavioural correlates of two stages of sleep in octopuses, marine invertebrates that evolutionarily diverged from vertebrates roughly 550 million years ago (ref. 5) and have independently evolved large brains and behavioural sophistication. ‘Quiet’ sleep in octopuses is rhythmically interrupted by approximately 60-s bouts of pronounced body movements and rapid changes in skin patterning and texture6. We show that these bouts are homeostatically regulated, rapidly reversible and come with increased arousal threshold, representing a distinct ‘active’ sleep stage. Computational analysis of active sleep skin patterning reveals diverse dynamics through a set of patterns conserved across octopuses and strongly resembling those seen while awake. High-density electrophysiological recordings from the central brain reveal that the local field potential (LFP) activity during active sleep resembles that of waking. LFP activity differs across brain regions, with the strongest activity during active sleep seen in the superior frontal and vertical lobes, anatomically connected regions associated with learning and memory function7–10. During quiet sleep, these regions are relatively silent but generate LFP oscillations resembling mammalian sleep spindles11,12 in frequency and duration. The range of similarities with vertebrates indicates that aspects of two-stage sleep in octopuses may represent convergent features of complex cognition.

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Section: Mainmentioning

confidence: 99%

Wake-like skin patterning and neural activity during octopus sleep

Pophale,

Shimizu,

Mano

et al. 2023

Nature

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“…Since the pioneering work of Florey on cephalopod chromatophores7,8, Hanlon, Messenger and colleagues have revealed the remarkable complexity of this system,9–11. Pigment-carrying chromatophores—the pixels of this 2D texture generation system— expand and contract in direct response to the activity of motoneurons8, which project from the brain12 and make excitatory glutamatergic synaptic connections13 onto sets of muscles arranged radially14.…”

mentioning

confidence: 99%

Elucidating the control and development of skin patterning in cuttlefish

Reiter

Hülsdunk

Woo

et al. 2018

Nature

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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.

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“…[ 270 ] More detail on neural control of the skin papillae can be found elsewhere. [ 306 ] Undoubtedly, while research on cephalopods’ brain is still ongoing, technology can move astray, without the need of consistently replicate living beings. Interestingly, there are great expectations on the studies related to the learning approaches of cephalopods, due to their advanced cognitive abilities, and their large nervous system that rivals that of many mammals.…”

Section: Proprioception and Control System For Soft Robotsmentioning

confidence: 99%

A Perspective on Cephalopods Mimicry and Bioinspired Technologies toward Proprioceptive Autonomous Soft Robots

Giordano

Carlotti

Mazzolai

2021

Adv Materials Technologies

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scientific community. [1][2][3][4][5][6][7] Regardless, every time a living being reveals novel adaptive and dynamically reactive mimicry behavior, it inspires and fosters futuristic and unexpected technological outcomes. [8][9][10][11][12] At the biological level, the visual crypsis is the ability of a species to resemble the surroundings by matching the coloration and the geometrical patterns of the habitat. In this sense, a living being can control its appearance optically (thanks to arranged and optimized structures at the mesoscopic scale, by means of pigmentation, or emissive elements) and morphologically (it can show wrinkles and textures on the body to evade detection or observation). [13][14][15][16][17][18] Both these mechanisms are characterized by a time response that ranges from milliseconds to hundreds of seconds. In nature, several species take advantage of cryptic abilities, as, e.g., in cephalopods, [7] crustaceans, [19] reptilians, [1,20,21] insects, [22,23] birds, [24,25] shells, [26,27] plants, [28,29] among many. The biotic color changing and body patterning relate to reproductive, communicative, and defensive and/or predatory strategies. Unfortunately, the nervous or central control-chain system that steers these behaviors in animals and plants, is still somehow fogged for scientists. [7,[30][31][32] A complete knowledge about their central information process systems, can open to astonishing developments in many scientific branches, from neurobiology [33,34] to quantum biology. [35] Undoubtedly, the most debated case of study in the natural world are cephalopods, which not only are highly evolved and specialized in fast adaptive color changing displays, but also are able to actuate their skin to generate 3D patterns, when exposed to specific mechanical, thermal, optical, or chemical stimuli. Soft muscular arrangements, [36][37][38] spatially distributed and expandable absorbing components (namely chromatophores), [39,40] iridescent elements (namely irido phores), [41,42] and bright white scatterers (namely leucophores) [43] are responsible for textural, postural and color changing. Moreover, octopuses are a remarkable intelligent species, able, for example, to open a jar or avoid predators in the order of seconds. [44] Thus, cephalopods are usually regarded as a perfect example of embodied intelligence, [45] thanks to the symbiosis between their body's mechanics and morphology, and the distributed sensory neuro-motor-control system. Their "learning", "mechanical" and "material intelligence" will be our lodestars along this review, resulting in a fascinating connection between Octopus skin is an amazing source of inspiration for bioinspired sensors, actuators and control solutions in soft robotics. Soft organic materials, biomacromolecules and protein ingredients in octopus skin combined with a distributed intelligence, result in adaptive displays that can control emerging optical behavior, and 3D surface textures with rough geometries, with a remarkably high control speed (≈ms). To be able ...

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Neural Control of Dynamic 3-Dimensional Skin Papillae for Cuttlefish Camouflage

Cited by 29 publications

References 48 publications

Wake-like skin patterning and neural activity during octopus sleep

Wake-like skin patterning and neural activity during octopus sleep

Elucidating the control and development of skin patterning in cuttlefish

A Perspective on Cephalopods Mimicry and Bioinspired Technologies toward Proprioceptive Autonomous Soft Robots

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