Cephalopod Arms

Arm regeneration in two species of cuttlefish Sepia officinalis and Sepia pharaonis
Jedediah Tressler,Francis Maddox,Eli Goodwin,Zhuobin Zhang,Nathan J. Tublitz August 2013 - Subscription or pay by article required

Abstract

To provide quantitative information on arm regeneration in cuttlefish, the regenerating arms of two cuttlefish species, Sepia officinalis and Sepia pharaonis, were observed at regular intervals after surgical amputation. The third right arm of each individual was amputated to ~10–20 % starting length. Arm length, suction cup number, presence of chromatophores, and behavioral measures were collected every 2–3 days over a 39-day period and compared to the contralateral control arm. By day 39, the regenerating arm reached a mean 95.5 ± 0.3 % of the control for S. officinalis and 94.9 ± 1.3 % for S. pharaonis. The process of regeneration was divided into five separate stages based on macroscopic morphological events: Stage I (days 0–3 was marked by a frayed leading edge; Stage II (days 4–15) by a smooth hemispherical leading edge; Stage III (days 16–20) by the appearance of a growth bud; Stage IV (days 21–24) by the emergence of an elongated tip; and Stage V (days 25–39) by a tapering of the elongated tip matching the other intact arms. Behavioral deficiencies in swimming, body postures during social communication, and food manipulation were observed immediately after arm amputation and throughout Stages I and II, returning to normal by Stage III. New chromatophores and suction cups in the regenerating arm were observed as early as Stage II and by Stage IV suction cup number equaled that of control arms. New chromatophores were used in the generation of complex body patterns by Stage V. These results show that both species of cuttlefish are capable of fully regenerating lost arms, that the regeneration process is predictable and consistent within and across species, and provide the first quantified data on the rate of arm lengthening and suction cup addition during regeneration.
 
Damien;n281833 said:
Is there any data about comparison between arms and tentacules regeneration for a decapod?

Actually this would be very interesting to look into, especially across species where tentacles are lost at early (or late) life stages vs retained throughout. For example, octopoteuthids (and some other families) lose the tentacles as paralarvae and never regenerate them, but must be able to regenerate arms (and arm tips since these can be jettisoned); onychoteuthids often lose the tentacles around maturity and don't regrow them, but will begin to regenerate them if lost earlier (this would be particularly interesting to look at--when does the regeneration cue switch off?), while some others retain tentacles all the way through the lifespan and so presumably will start regenerating them no matter when they're lost.

Hmmmmmmmmm.... :read:
 
For example, octopoteuthids (and some other families) lose the tentacles as paralarvae and never regenerate them, but must be able to regenerate arms

This tidbit is very intriguing considering other animals often see a hyper-regenerative ability at early stages and lose regeneration with aging, especially in muscle. I speak from a vertebrate perspective, but the classical amphibian models even lose their abilities after inducing metamorphosis.

Does anyone know if cephs have a quiescent stem population perhaps similar to pericytes or satellite cells? It'd be interesting to look further into which populations are contributing in that Fossati paper. Maybe they can dedifferentiate like Gymnotiform fishes.
 
The surprising resilience of octopus tentacles [Video]

Self-Recognition Mechanism between Skin and Suckers Prevents Octopus Arms from Interfering with Each Other
Nir Nesher, Guy Levy, Frank W. Grasso, Binyamin Hochner 2014 (subscription)

Highlights
  • •Octopus suckers have a strong tendency to attach to any substrate they contact
  • •This raises the question of why octopus arms do not grab or interfere with each other
  • •Here it is shown that chemical signals from octopus skin inhibit the attachment reflex
  • •Thus, constraining the arms from interfering with each other simplifies motor control
Summary
Controlling movements of flexible arms is a challenging task for the octopus because of the virtually infinite number of degrees of freedom (DOFs) [ 1, 2 ]. Octopuses simplify this control by using stereotypical motion patterns that reduce the DOFs, in the control space, to a workable few [ 2 ]. These movements are triggered by the brain and are generated by motor programs embedded in the peripheral neuromuscular system of the arm [ 3–5 ]. The hundreds of suckers along each arm have a tendency to stick to almost any object they contact [ 6–9 ]. The existence of this reflex could pose significant problems with unplanned interactions between the arms if not appropriately managed. This problem is likely to be accentuated because it is accepted that octopuses are “not aware of their arms” [ 10–14 ]. Here we report of a self-recognition mechanism that has a novel role in motor control, restraining the arms from interfering with each other. We show that the suckers of amputated arms never attach to octopus skin because a chemical in the skin inhibits the attachment reflex of the suckers. The peripheral mechanism appears to be overridden by central control because, in contrast to amputated arms, behaving octopuses sometime grab amputated arms. Surprisingly, octopuses seem to identify their own amputated arms, as they treat arms of other octopuses like food more often than their own. This self-recognition mechanism is a novel peripheral component in the embodied organization of the adaptive interactions between the octopus’s brain, body, and environment [ 15, 16 ].
 
Octobot uses webbed arms to swim faster
by Meghan Rosen September 17, 2014

CHICAGO —Webbed underarms can turn a sluggish robotic octopus into a speed demon.
A squishy membrane connecting the machine’s eight arms helps the bot scoot through water nearly twice as fast as octobots without webs, researchers reported at the IEEE/RSJ International Conference on Intelligent Robots and Systems on September 15.
Inspired by Octopus vulgaris, the well-known sea creature with arms connected by a fleshy, skirtlike mantle, computer scientist Dimitris Tsakiris and colleagues decided to give a makeover to the robotic octopus they had previously developed. The earlier, webless version could propel itself at up to 100 millimeters per second by slowly opening stiff plastic arms and then snapping them together.
But with arms and a web made of soft silicone, the shoe box–sized bot swam at up to 180 millimeters per second. The web helps the octobot generate more force, so it can push through water faster than using arms alone.
Skittish sea animals seem unfrightened by the lifelike bot, said Tsakiris, of the Foundation for Research and Technology- Hellas in Heraklion, Greece. When researchers took the faux octopus for a swim in the Mediterranean, tiny fish tagged along.

 
Bipedal Octopuses Dr. Christine Huffard

HIGHLIGHTS1. Two species of octopuses walk on two of their eight arms using a rolling gait. 2. This is the first example of bipedal locomotion using a hydrostatic skeleton rather than rigid support.3. We hypothesize that this locomotion proceeds with minimal neural feedback from the brain.4. This behavior allows octopuses to move quickly without giving up their primary defense (camouflage).

SUMMARY
We reviewed videotape of octopuses to describe the kinematics of their bipedal locomotion. They walk along the bottom on their ventral (backmost) two arms using a flexible, rolling gait. Amphioctopus marginatus draws six arms up to the rounded body and walks backward. Abdopus aculeatus coils and raises the other arms above the head as it walks, even over rugged terrain.
 
The making of an octopus arm
Marie-Therese NödlSara M FossatiPedro DominguesFrancisco J SánchezLetizia Zullo
Credits/Source: EvoDevo 2015, 6:19 (open source)

Here, we examined the basic dynamics of the Octopus vulgaris arm's formation and differentiation - as a highly evolved member of the lophotrochozoan super phylum - with a special focus on the formation of the arm's musculature.
 
The musculature of coleoid cephalopod arms and tentacles
William M. Kier 2016

Abstract
The regeneration of coleoid cephalopod arms and tentacles is a common occurrence, recognized since Aristotle. The complexity of the arrangement of the muscle and connective tissues of these appendages make them of great interest for research on regeneration. They lack rigid skeletal elements and consist of a three-dimensional array of muscle fibers, relying on a type of skeletal support system called a muscular hydrostat. Support and movement in the arms and tentacles depends on the fact that muscle tissue resists volume change. The basic principle of function is straightforward; because the volume of the appendage is essentially constant, a decrease in one dimension must result in an increase in another dimension. Since the muscle fibers are arranged in three mutually perpendicular directions, all three dimensions can be actively controlled and thus a remarkable diversity of movements and deformations can be produced. In the arms and tentacles of coleoids, three main muscle orientations are observed: 1) transverse muscle fibers arranged in planes perpendicular to the longitudinal axis; 2) longitudinal muscle fibers typically arranged in bundles parallel to the longitudinal axis; and 3) helical or obliquely arranged layers of muscle fibers, arranged in both right- and left-handed helixes. By selective activation of these muscle groups, elongation, shortening, bending, torsion and stiffening of the appendage can be produced. The predominant muscle fiber type is obliquely striated. Cross-striated fibers are found only in the transverse muscle mass of the prey capture tentacles of squid and cuttlefish. These fibers have unusually short myofilaments and sarcomeres, generating the high shortening velocity required for rapid elongation of the tentacles. It is likely that coleoid cephalopods use ultrastructural modifications rather than tissue-specific myosin isoforms to tune contraction velocities.
 
Mechanisms of wound closure following acute arm injury in Octopus vulgaris
Tanya J. Shaw,Molly Osborne,Giovanna Ponte,Graziano Fiorito, Paul L.R. Andrews 2016 (Open Access BioMed Center)

[DWhatley] It would be interesting to know if the severed arm also formed a cellular plug and if it gave any indication of repair attempt.

Abstract
Background
Octopoda utilise their arms for a diverse range of functions, including locomotion, hunting, defence, exploration, reproduction, and grooming. However the natural environment contains numerous threats to the integrity of arms, including predators and prey during capture. Impressively, octopoda are able to close open wounds in an aquatic environment and can fully regenerate arms. The regrowth phase of cephalopod arm regeneration has been grossly described; however, there is little information about the acute local response that occurs following an amputation injury comparable to that which frequently occurs in the wild.

Methods
Adult Octopus vulgaris caught in the Bay of Naples were anaesthetised, the distal 10 % of an arm was surgically amputated, and wounded tissue was harvested from animals sacrificed at 2, 6, and 24 h post-amputation. The extent of wound closure was quantified, and the cell and tissue dynamics were observed histologically, by electron microscopy, as well as using ultrasound.

Results
Macroscopic, ultrasonic and ultrastructural analyses showed extensive and significant contraction of the wound margins from the earliest time-point, evidenced by tissue puckering. By 6 h post amputation, the wound was 64.0 ± 17.2 % closed compared to 0 h wound area. Wound edge epithelial cells were also seen to be migrating over the wound bed, thus contributing to tissue repair. Temporary protection of the exposed tip in the form of a cellular, non-mucus plug was observed, and cell death was apparent within two hours of injury. At earlier time-points this was apparent in the skin and deeper muscle layers, but ultimately extended to the nerve cord by 24 h.

Conclusions
This work has revealed that O. vulgaris ecologically relevant amputation wounds are rapidly repaired via numerous mechanisms that are evolutionarily conserved. The findings provide insights into the early processes of repair preparatory to regeneration. The presence of epithelial, chromatophore, vascular, muscle and neural tissue in the arms makes this a particularly interesting system in which to study acute responses to injury and subsequent regeneration.
 
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Friday Cephalopod: Force of arms
Pharyngula Posted by PZ Myers on June 10, 2016

...
We can get weirder still, though. Let’s look at cephalopods (you knew where this was going): no bones, no joints, no hydrostatic skeleton, just lots and lots of muscle. What are they pulling on? How do tentacles work? They writhe and bend and extend and grasp, bonelessly. From a vertebrate perspective, they’re just freaky.

So I found a good recent review of the musculature of cephalopod arms and tentacles. There were many surprises.

For one, there are no long muscle fibers anywhere — muscle cells are at most 1mm long. This makes sense — we have long fibers to stretch between joints, but cephalopod limbs are just one long series of very tiny, very flexible ‘joints’.

Next surprise: they have a novel (for a vertebrate…other invertebrate phyla show a similar pattern) arrangement of actin and myosin. Instead of all of the bands in a fiber being lined up in register, the filaments are staggered to form obliquely striated muscle. Pretty!

Schematic diagram of a cephalopod obliquely striated muscle fiber. Note that a cross-section of an obliquely striated muscle cell shows an analogous sequence of bands to those seen in a longitudinal section of a cross-striated fiber. A, A-band; I, I-band; M, mitochondria; S, sarcoplasmic reticulum; Z, elements.

Now the big question: how does this work without any kind of skeleton for the muscles to pull on? There is one simple principle at work. The arm has a fixed volume. What that means is that when muscles contract to reduce the diameter of the tentacle, the total volume has to stay the same, so the volume gets displaced longitudinally, causing the tentacle to extend. When longitudinal muscles contract, compressing the length, the cylinder has to get thicker to contain the same volume. When longitudinal muscles contract on one side of the tentacle, but other muscles also contract to keep the diameter constant, the tentacle will bend towards the side with the contracting longitudinal muscle.

That’s it! It’s all about shifting the volume of the whole organ around. So when you look at a section of an octopus arm, you find a lot of transverse muscle fibers, a meshwork of fibers that act in the transverse plane to manage the diameter of the arm, and a lot of longitudinal fibers that can compress the length of the arm. Between them, they can fluidly change the shape of the cylinder from point to point.

Schematic diagram of the arm of Octopus showing the three-dimensional arrangement of muscle fibers and connective tissue fibers. AN, axial nerve cord; AR, artery; CM, circumferential muscle layer; CT, connective tissue; DCT, dermal connective tissue; EP, epidermis; IN, intramuscular nerve; LM, longitudinal muscle fibers; OME, external oblique muscle layer; OMI, internal oblique muscle layer; OMM, median oblique muscle layer; SU, sucker; TM, transverse muscle fibers; TR; trabeculae; V, vein.

One other twist, literally. The arm is also surrounded by thin layers of obliquely oriented muscle fibers which can provide a torsional force, so the arm can also rotate. This is important because an arm has an oral side, with suckers, and an aboral side, lacking suckers. When an octopus wraps its arm around a crab, it also needs to be able to twist it so the sucker side is grasping its prey.

I am envious. I wish I had limbs like that — no more aching knees. But I have to be honest, there are some drawbacks.

One is that the amount of neural control required to regulate an octopus arm has to be massive. Humans, for instance, only have to control 23 muscles in each arm (not to belittle that, though: this is a combinatorial problem with agonist, antagonist, and synergist muscles working together in a coordinated fashion for every movement). Octopus muscle control is much more fine-grained, and while a lot of the maintenance of a motion is farmed out to local networks of neurons — an octopus does not have to consciously think about every sinuousity in its motion, no more than you have to consciously think about each arm muscle independently — it’s still got to involve some fascinatingly complex circuitry.

Another deficiency is that we take advantage of levers as force multipliers. Your forearm pivots on your elbow joint, and a small contraction of a muscle inserting near the joint can produce a much larger motion by your hand. We can punch and throw things with a force no octopus can ever achieve. A cephalopod isn’t going to be able to evolve a hammer like a stomatopod.

But, you know, I’ve never had much cause to punch anyone, so maybe if I adopted a lifestyle of langorous stroking and hugging and touching and sensing, I could be quite happy with an octopus arm transplant.

Kier WM (2016) The Musculature of Coleoid Cephalopod Arms and Tentacles. Front Cell Dev Biol 4:10. doi: 10.3389/fcell.2016.00010.
 
Immunohistochemical and biochemical evidence for the presence of serotonin-containing neurons and nerve fibers in the octopus arm
Jean-Pierre Bellier, Yu Xie, Sameh Mohamed Farouk, Yuko Sakaue, Ikuo Tooyama, Hiroshi Kimura 2017 (Subscription Springer)

Abstract
The octopus arm contains a tridimensional array of muscles with a massive sensory-motor system. We herein provide the first evidence for the existence of serotonin (5-HT) in the octopus arm nervous system and investigated its distribution using immunohistochemistry. 5-HT-like immunoreactive (5-HT-lir) nerve cell bodies were exclusively localized in the cellular layer of the axial nerve cord. Those cell bodies emitted 5-HT-lir nerve fibers in the direction of the sucker, the intramuscular nerves cords, the ganglion of the sucker, and the intrinsic musculature. Others 5-HT-lir nerve fibers were observed in various tissues, including the cerebrobrachial tract, the skin, and the blood vessels. 5-HT was detected by high-performance liquid chromatography in various regions of the octopus arm at levels matching the density of 5-HT-lir staining. The absence of 5-HT-lir interconnections between the cerebrobrachial tract and the other components of the axial nerve cord suggests that two types of 5-HT-lir innervation exist in the arm. One type, which originates from the brain, may innervate the periphery through the cerebrobrachial tract. Another type, which originates in the cellular layer of the axial nerve cord, may form an intrinsic network in the arm. In addition, 5-HT-lir fibers likely emitted from the neuropil of the axial nerve cord were found to project into cells showing staining for peripheral choline acetyltransferase, a marker of sensory cells of the sucker. Taken together, these observations suggest that intrinsic 5-HT-lir innervation may participate in the sensory transmission in the octopus arm.
 
Motor control pathways in the nervous system of Octopus vulgaris arm
Letizia Zullo, Hadas Eichenstein, Federica Maiole, Binyamin Hochner 2019 (subscription Journal of Comparative Physiology A)

Abstract
The octopus’s arms have virtually infinite degrees of freedom, providing a unique opportunity for studying movement control in a redundant motor system. Here, we investigated the organization of the connections between the brain and arms through the cerebrobrachial tracts (CBT). To do this, we analyzed the neuronal activity associated with the contraction of a small muscle strand left connected at the middle of a long isolated CBT. Both electrical activity in the CBT and muscle contraction could be induced at low threshold values irrespective of stimulus direction and distance from the muscle strand. This suggests that axons associated with transmitting motor commands run along the CBT and innervate a large pool of motor neurons en passant. This type of innervation implies that central and peripheral motor commands involve the simultaneous recruitment of large groups of motor neurons along the arm as required, for example, in arm stiffening, and that the site of movement initiation along the arm may be determined through a unique interplay between global central commands and local sensory signals.
 

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