The Hebrew University of Jerusalem

A.The octopus as a model for a successful control of movements in flexible arms

Octopuses are considered to be among the most developed and intelligent animals in the invertebrate kingdom. For many years scientists were attracted by their abilities to learn, memorize, and even to solve rather complicated behavioral problems. At least part of these skills can be attributed to the high maneuverability of the arms and the capacity of the peripheral nervous system to perceive and process chemical and tactile information. In contrast to the movements produced by appendages that contain skeletal support, the impressive motor performances of the octopus are executed by bone-less and highly flexible arms. This flexibility and the need to coordinate between eight arms, requires a high degree of motor-control. Therefore, it is conceivable that the strategy and principles of the arm motor control are based on unique and novel mechanisms. Elucidating the mechanisms and principles of the arm motor control at the cellular and behavioral levels, is the long term goal of our research. The information gathered in this research will be utilized, in the future, to construct a flexible robotic arm.
In our research we combine behavioral, physiological and theoretical studies to investigate the motor-control and motor function of the flexible arm of the octopus.
In the behavioral part we aim at identifying general principles in the organization of arm movement. We concentrated on a basic motion pattern which we identified in arm extension. The octopus extends its arm by a wave-like propagation of a bend that travels toward the arm tip. Kinematic measurements revealed that the bend tends to move within a single linear plane with a stereotypical velocity profile. We suggested that this strategy simplifies the complexity of motor control by reducing the excessively large number of degrees of freedom involved in the movement of flexible arms.
In a study that combined kinematic analysis with recordings of the muscle activities (EMG) we explore the neuronal control of the arm. Arm extension is generated by a wave of muscle activity and therefore is not a passive phenomenon. The amplitude of the integrated EMG is best correlated with the global parameters of the movement profile, i.e. with maximum acceleration and maximum velocity, and to a lesser extent with the local velocity and acceleration. These results led us to suggest that the motor program for arm extension is based on a built in feed forward program, that is simply scaled to produce different speeds. The coordinated propagation of the bend and the neuronal activity is achieved by local feedback from propreioceptors in the muscles.
Physiological methods are used to examine the neuromuscular mechanism of the octopus arm in order to understand how the nervous system controls the mechanical performance. The muscle fibers are exceptionally compact in their electrical dimensions, making each cell a temporal integrator of the synaptic inputs. Each cell in the arm receives three distinct types of excitatory synaptic inputs that are mediated by acetylcholine. The muscle fibers have excitable membrane properties. We conclude that the different muscle groups of the arm are composed of motor-units with similar properties. Together with the fact that each muscle cell functions as a temporal integrator, these findings suggest that the mechanical output of the arm is primarily under control of the output of the nervous system.
In the theoretical part of the project we are constructing a bio-mechanical model of the arm. The octopus arm belongs to a group of biological organs defined as muscular-hydrostats because they are composed almost entirely of muscles. This fundamental property confers the main constraint on the model because the volume of a muscular-hydrostat remains constant. The model simulates muscle function as a spring with activity-dependent stiffness. It also includes damping elements, mass and interaction with water. At this stage, we are using the model to evaluate alternative patterns of muscle activation and to demonstrate possible patterns that can generate a propagating bend along the arm. We have already confirmed that a stiffening wave can cause arm extension, an hypothesis raised consequent to the experimental results.

B. Evolutionary approach to the exploration of the neural basis of learning and memory

Nature has provided several examples of convergent evolutionary processes where similar functions are mediated by analogous systems in evolutionary remote species. This evolution of analogous systems, believed to be driven by the same selection forces, results in independent arrival at the most optimal solution for a particular task. Use of a comparative approach to study an invertebrate with vertebrate-like behavior may therefore advance our analysis of brain mechanisms that are important for mediation of complex behaviors and learning and memory. The octopus is an ideal animal for such a study, as it is a unique invertebrate mollusc with learning abilities similar to those of vertebrates.
Despite decades of behavioral research, almost nothing is known about the cellular mechanisms mediating learning and memory in their advanced, centralized brain. We have developed an in vitro slice preparation of an area in their brain (vertical lobe, VL) which is involved in learning and memory and provides the first opportunity for such a cellular analysis. Intracellular recording from the neurons in the VL and extracellular recording of its field potentials revealed a synaptic input to the VL which undergoes a robust activity-dependent long-term potentiation (LTP). This glutamatergic LTP clearly resembles aspects of vertebrate LTP, indicating that similar cellular mechanisms and network organizations have been selected during the evolution of animals with complex forms of learning. Further cellular studies, combined with behavioral research done in collaboration with Drs. G. Fiorito and ER. Brown at the Stazione Zoologica di Napoli, will help to find the similar and different mechanisms that evolved in animals with sophisticated behaviors, and thus, may shed light on mechanisms important for the cognitive functions of the brain.


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