Neuromuscular System of the Flexible Arm of the Octopus: Physiological Characterization

Abstract

The octopus arm is an outstanding example of an efficient boneless and highly flexible appendage. We have begun characterizing the neuromuscular system of the octopus arm in both innervated muscle preparations and dissociated muscle cells. Functionally antagonistic longitudinal and transverse muscle fibers showed no differences in membrane properties and mode of innervation. The muscle cells are excitable but have a broad range of linear membrane properties. They are electrotonically very compact so that localized synaptic inputs can control the membrane potential of the entire muscle cell. Three distinct excitatory neuronal inputs to each arm muscle cell were identified; their reversal potentials were extrapolated to be about -10 mV. These appear to be cholinergic as they are blocked by hexamethonium, D-tubocurarine, and atropine. Two inputs have low quantal amplitude (1-7 mV) and slow rise times (4-15 ms), whereas the third has a large size (5-25 mV) and fast rise time (2-4 ms). This large synaptic input is most likely due to exceptionally large quantal events. The probability of release is rather low, suggesting a stochastic activation of muscle cells. All inputs demonstrated a modest activity-dependent plasticity typical of fast neuromuscular systems. The pre- and postsynaptic properties suggest a rather direct relation between neuronal activity and muscle action. The lack of significant electrical coupling between muscle fibers and the indications for the small size of the motor units suggest that the neuromuscular system of the octopus arm has evolved to ensure a high level of precise localization in the neural control of arm function.

How Nervous Systems Evolve in Relation to Their Embodiment: What We Can Learn from Octopuses and Other Molluscs

“…The neuromuscular system of the octopus arm (and most likely of other molluscs) differs dramatically from those of skeletal animals, vertebrates, and arthropods [Matzner et al, 2000;Rokni and Hochner, 2002;Gutfreund et al, 2006;Feinstein et al, 2011]. The differences can be viewed as an adaptation of the 'mechanical system' ( fig.…”

“…Each muscle cell is innervated by three excitatory cholinergic motoneurons at a discrete synaptic junction near the center of each cell. This synaptic input can control the membrane potential of the entire cell, most likely due to its electrical compactness [Matzner et al, 2000;. Fast sodium spikes are thus unnecessary for spreading the electrical signal along the cell, as in vertebrate muscle cells.…”

Locomotion byAbdopus aculeatus(Cephalopoda: Octopodidae):walking the line between primary and secondary defenses

“…Although the nervous control of locomotion is poorly understood, these single-arm movements do not necessarily require complex control. Nervous control of reaching is decentralized and can proceed without involvement of the brain's motor control region [the peduncle lobe (Messenger, 1967;Williamson and Chrachri, 2004)], allowing for simple feed-forward movements capable of incorporating feedback (Gutfreund et al, 1996;Gutfreund et al, 1998;Matzner et al, 2000;Sumbre et al, 2001;Yekutieli et al, 2005a;Yekutieli et al, 2005b).…”

The biomechanical and neural control of hydrostatic limb movements in Manduca sexta

“…Others have examined the movements of myostatic tissues such as elephant trunks, vertebrate tongues and octopus arms (Gutfreund et al, 1998;Matzner et al, 2000;Wilson et al, 1991). There is also considerable interest in the hydrostatic components of spider leg joints (Sensenig and Shultz, 2003).…”