If you want to see a truly remarkable example of convergence, then present an octopus with a piece of food and have a high-speed camera ready…

Lever-like locomotory limb systems have evolved independently many times in animals. The extent of evolutionary convergence is, however, difficult to appreciate unless one considers the octopus. What could be more different from a human arm than the eight arms of this cephalopod mollusc? Almost alien-like, they writhe around – until they are given a piece of food. What we then see is a remarkable example of convergence…

Motor control

Human arms are relatively simple in terms of motor control, as they are rigid with three skeletal joints. This reduces the number of variables as well as the degrees of freedom that have to be controlled. Octopus arms are very different. They can bend in all directions, vary their stiffness and elongate rapidly. All this is made possible by their muscular structure: densely packed muscle fibres of different orientation and connective tissue fibres enclose an axial nerve cord. Together this serves to provide an effectively incompressible arrangement known as a muscular hydrostat (vertebrate examples include elephant trunks and the tongues of mammals and reptiles).

In principle, the flexibility of the octopus arm makes motor control much more difficult. However, with the help of high-speed photography it has been shown that, when an octopus uses one of its arms to move a piece of food to its mouth, it does so in a surprisingly vertebrate-like fashion. It reconfigures its arm into a stiffened structure consisting of three elements that articulate via “pseudo-joints”, which are reminiscent of our shoulder, elbow and wrist. A rotation around these “pseudo-joints” brings the food to the mouth, with the central “elbow” usually showing the greatest degree of mobility. As a result, only three degrees of freedom need to be controlled and the arm movements become highly stereotypical. In contrast to a vertebrate arm, the configuration of the structure can be adjusted dynamically. As the “pseudo-joints” are formed where two waves of muscle activation propagating in opposite directions collide, the length of the segments can be varied depending on where an object is grasped. However, “upper arm” and “forearm” remain remarkably similar in length – when one becomes more elongate, so does the other. The octopus thus achieves through neural control what vertebrates achieve through morphology, and “this functional convergence suggests that a kinematically constrained, articulated limb with two segments of almost equal length is the optimal design for accurately moving an object from one point to another” (Sumbre et al. 2005, Nature, vol. 433, p. 595).

Neural mechanisms

Motor control in the octopus nervous system is organised hierarchically. The higher motor centres are the basal lobes of the brain, which integrate visual and tactile information and issue commands to the lower motor centres that control arm movement. Brain microstimulation in freely behaving animals provided evidence that complex movements such as arm extension are built up of sets of basic components. Accordingly, when stimulating the basal lobes, the elicited response resembled that obtained by stimulation of integrative areas in vertebrate brains. Surprisingly and uniquely, however, the octopus higher motor centres are apparently not somatotopically organised (a somatotopic arrangement maintains the spatial organisation of body parts in the brain), but movements seem to be represented by several overlapping circuits. In other words, there is no site where stimulation elicited movement of a single body part, so indicating that the components of a movement are distributed over wide regions of the brain.

A single extension command generated by the higher motor centres seems to be issued to several arms at once, which might simplify central motor control. It has been observed that octopuses typically recruit neighbouring arms for investigating an object. As information is transferred quickly through a ring-shaped connection at the arm base, this is usually considered a reflex. Thus, several arms are often used together, but sensory input can be used to guide a single arm towards a stimulus.

Laterality

The phenomenon of handedness is well known from humans and other vertebrates, and many animals (including birds and toads) also exhibit an equivalent footedness. Octopuses have not only two but eight arms that are apparently identical, so do they show motoric lateralisation as well and if so, how they choose which arm to use for a task? In laboratory experiments, common octopuses (Octopus vulgaris) preferred their anterior arms to initiate contact with an object. Furthermore, the individuals used seemed to have a favoured arm when retrieving food from a maze, and half of them exhibited a lateral bias. However, octopuses also show lateralisation of eye use, and a more recent study found a connection between arm and eye preference. Here, there was no evidence for lateralised arm use, but individuals preferentially employed an arm that was in direct line between the object and the eye used to look at it (which seems anatomically logical). Thus, arm choice in octopuses is probably affected by the direction from which an object is approached, which in turn is determined by monocular eye use. Hence, this eye-arm coordination is reminiscent of primates, which show visual control of hand movements to grasp objects.

Octopus arms are being used as models for soft (or continuum) robots that possess mobility in all directions. In the future, such robots might be employed for search and rescue operations in complex environments or even in the human body for medical purposes.