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Elastic arteries in invertebrates: mechanics of the octopus aorta.

The aorta of the octopus, Octopus dofleini, is a highly distensible, elastic tube. The circumferential elastic modulus increases with inflation in the physiological range from abut 10(4) to 10(5) newtons per square meter. Rubber-like fibers have been isolated, apparently for the first time, from the aorta of an invertebrate. These fibers have an elastic modulus, like elastin, of about 4 x 10(5) newtons per square meter and are present in sufficient quantity to account for the elastic properties of the intact vessel under physiological conditions. Thus the circulatory system of an invertebrate animal provides an "elastic reservoir" (much like that of the vertebrate system), which increases the efficiency of the circulation.

Animals↗

Ionic currents underlying fast action potentials in the obliquely striated muscle cells of the octopus arm.

The octopus arm provides a unique model for neuromuscular systems of flexible appendages. We previously reported the electrical compactness of the arm muscle cells and their rich excitable properties ranging from fast oscillations to overshooting action potentials. Here we characterize the voltage-activated ionic currents in the muscle cell membrane. We found three depolarization-activated ionic currents: 1) a high-voltage-activated L-type Ca(2+) current, which began activating at approximately -35 mV, was eliminated when Ca(2+) was substituted by Mg(2+), was blocked by nifedipine, and showed Ca(2+)-dependent inactivation. This current had very rapid activation kinetics (peaked within milliseconds) and slow inactivation kinetics (tau in the order of 50 ms). 2) A delayed rectifier K(+) current that was totally blocked by 10 mM TEA and partially blocked by 10 mM 4-aminopyridine (4AP). This current exhibited relatively slow activation kinetics (tau in the order of 15 ms) and inactivated only partially with a time constant of ~150 ms. And 3) a transient A-type K(+) current that was totally blocked by 10 mM 4AP and was partially blocked by 10 mM TEA. This current exhibited very fast activation kinetics (peaked within milliseconds) and inactivated with a time constant in the order of 60 ms. Inactivation of the A-type current was almost complete at -40 mV. No voltage-dependent Na(+) current was found in these cells. The octopus arm muscle cells generate fast (~3 ms) overshooting spikes in physiological conditions that are carried by a slowly inactivating L-type Ca(2+) current.

Action Potentials↗

A learning and memory area in the octopus brain manifests a vertebrate-like long-term potentiation.

Cellular mechanisms underlying learning and memory were investigated in the octopus using a brain slice preparation of the vertical lobe, an area of the octopus brain involved in learning and memory. Field potential recordings revealed long-term potentiation (LTP) of glutamatergic synaptic field potentials similar to that in vertebrates. These findings suggest that convergent evolution has led to the selection of similar activity-dependent synaptic processes that mediate complex forms of learning and memory in vertebrates and invertebrates.

Animals↗

Dynamic model of the octopus arm. I. Biomechanics of the octopus reaching movement.

The octopus arm requires special motor control schemes because it consists almost entirely of muscles and lacks a rigid skeletal support. Here we present a 2D dynamic model of the octopus arm to explore possible strategies of movement control in this muscular hydrostat. The arm is modeled as a multisegment structure, each segment containing longitudinal and transverse muscles and maintaining a constant volume, a prominent feature of muscular hydrostats. The input to the model is the degree of activation of each of its muscles. The model includes the external forces of gravity, buoyancy, and water drag forces (experimentally estimated here). It also includes the internal forces generated by the arm muscles and the forces responsible for maintaining a constant volume. Using this dynamic model to investigate the octopus reaching movement and to explore the mechanisms of bend propagation that characterize this movement, we found the following. 1) A simple command producing a wave of muscle activation moving at a constant velocity is sufficient to replicate the natural reaching movements with similar kinematic features. 2) The biomechanical mechanism that produces the reaching movement is a stiffening wave of muscle contraction that pushes a bend forward along the arm. 3) The perpendicular drag coefficient for an octopus arm is nearly 50 times larger than the tangential drag coefficient. During a reaching movement, only a small portion of the arm is oriented perpendicular to the direction of movement, thus minimizing the drag force.

Animals↗

Dynamic model of the octopus arm. II. Control of reaching movements.

The dynamic model of the octopus arm described in the first paper of this 2-part series was used here to investigate the neural strategies used for controlling the reaching movements of the octopus arm. These are stereotypical extension movements used to reach toward an object. In the dynamic model, sending a simple propagating neural activation signal to contract all muscles along the arm produced an arm extension with kinematic properties similar to those of natural movements. Control of only 2 parameters fully specified the extension movement: the amplitude of the activation signal (leading to the generation of muscle force) and the activation traveling time (the time the activation wave takes to travel along the arm). We found that the same kinematics could be achieved by applying activation signals with different activation amplitudes all exceeding some minimal level. This suggests that the octopus arm could use minimal amplitudes of activation to generate the minimal muscle forces required for the production of the desired kinematics. Larger-amplitude signals would generate larger forces that increase the arm's stability against perturbations without changing the kinematic characteristics. The robustness of this phenomenon was demonstrated by examining activation signals with either a constant or a bell-shaped velocity profile. Our modeling suggests that the octopus arm biomechanics may allow independent control of kinematics and resistance to perturbation during arm extension movements.

Animals↗

Sinusoidal analysis of electroretinogram of squid and octopus.

1. An isolated eye or eye plus optic lobe preparation (in oxygenated chilled seawater) from Loligo opalescens, Octopus bimaculata, and O. bimaculoides was used to study the electroretinogram (ERG) for small signal intensity-modulated stationary spots of light. 2. If light intensity was modulated sinusoidally (modulation depth 0-50%) the ERG response is sinusoidal with less than 2% of the power present in the next five harmonics compared to the fundamental. Bode plots, amplitude and phase shift plotted against frequency, were constructed from these sinusoidal input-output experiments. 3. Linearity and time invariance were tested: a) an increase in amplitude of sinusoidal modulation by a constant factor caused an increase in response amplitude by the same factor but caused no change in shape of the Bode plot gain or phase curves; b) the transfer function represented by the Bode plot could be used to predict waveshape of the response to a brief flash (Green's or impulse-response function); c) the Fourier transformed square-wave response could be used to obtain a Bode plot which coincided with that obtained by sinusoidal input-output experiments. 4. The Bode plot can be fit by the transfer function of 5-12 (depending on conditions and on the preparations) series cascaded low-pass filters whose corner frequences are distributed between 0.2 and 40 Hz. Alternatively, 3-7 filters plus a delay of 25-130 ms fits the Bode plots equally well. The series filter model is compatible with a simply physical model consisting of cascaded chemical reactions whose forward rate constants are reciprocals of the filter time constants, whose reverse rate constants are negligible, and in which the concentration of an intermediate product controls membrane current. 5. As mean intensity is increased, the gain decreases. This effect is more pronounced at low frequencies than at high frequencies. Thus, the system is nonlinear for large intensity changes. The process of adaptation involves not only a change in gain, but a change in shape of the Bode plot, i.e., change in filter corner frequencies. In terms of the reaction chain model, this means that some rate constants change as the state of adaptation is changed.

Animals↗

Voltage-dependent conductances in cephalopod primary sensory hair cells.

Cephalopods, such as sepia, squid, and octopus, show a well-developed and sophisticated control of balance particularly during prey capture and escape behaviors. There are two separate areas of sensory epithelium in cephalopod statocysts, a macula/statolith system, which detects linear accelerations (gravity), and a crista/cupula system, which detects rotational movements. The aim of this study is to characterize the ionic conductances in the basolateral membrane of primary sensory hair cells. These were studied using a whole cell patch-clamp technique, which allowed us to identify five ionic conductances in the isolated primary hair cells; an inward sodium current, an inward calcium current, and three potassium outward currents. These outward currents were distinguishable on the basis of their voltage-dependence and pharmacological sensitivities. First, a transient outward current (IA) was elicited by depolarizing voltage steps from a holding potential of -60 mV, was inactivated by holding the cell at -40 mV, and was blocked by 4-aminopyridine. A second, voltage-sensitive, outward current with a sustained time course was identified. This current was not blocked by 4-aminopyridine nor inactivated at a holding potential of -40 mV and hence could be separated from IA using these protocols. A third outward current that depended on Ca2+ entry for its activation was detected, this current was identified by its sensitivity to Ca2+ channel blockers such as Co2+ and Cd2+ and by the N-shaped profile of its current-voltage curve. Inward currents were studied using cesium aspartate solution in the pipette to block the outward currents. Two inward currents were observed in the primary sensory hair cells. A fast transient inward current, which is presumably responsible for spike generation. This inward current appeared as a rapidly activating inward current; this was strongly voltage dependent. Three lines of evidence suggest that this fast transient inward current is a Na+ current (INa). First, it was blocked by tetrodotoxin (TTX); second, it also was blocked by Na+-free saline; and third, it was inactivated when primary hair cells were held at a potential more than -40 mV. The sustained inward current was not affected by TTX and was increased in amplitude 5 min after equimolar Ba2+ replaced Ca2+ as a charge carrier. This inward current also was blocked after external application of 2 mmol/l Co2+ or Cd2+. Furthermore, this current was reduced significantly in a dose-dependent manner by nifedipine, suggesting that it is an L-type Ca2+ current (ICa).

Animals↗

Neuromuscular system of the flexible arm of the octopus: physiological characterization.

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.

Animals↗

Octopus senescence: the beginning of the end.

Senescence is a normal stage of an octopus's life cycle that often occurs before death. Some of the following symptoms typify it: lack of feeding, retraction of skin around the eyes, uncoordinated movement, increased undirected activity, and white unhealing lesions on the body. There is inter- and intraspecific variability. Senescence is not a disease or a result of disease, although diseases can also be a symptom of it. Both males and females go through a senescent stage before dying-the males after mating, the females while brooding eggs and after the eggs hatch. There are many aspects of octopus senescence that have not yet been studied. This study discusses the ecological implications of senescence.

Aging↗

Interspecific evaluation of octopus escape behavior.

The well-known ability of octopuses to escape enclosures is a behavior that can be fatal and, therefore, is an animal welfare issue. This study obtained survey data from 38 participants-primarily scientists and public aquarists who work with octopuses-on 25 described species of octopus. The study demonstrates that the likeliness to escape is species specific (p =.001). The study gives husbandry techniques to keep captive octopuses contained. This first interspecific study of octopus escape behavior allows readers to make informed species-specific husbandry choices.

Animal Husbandry↗

The Octopus vulgaris estrogen receptor is a constitutive transcriptional activator: evolutionary and functional implications.

Steroid hormones such as estrogens and androgens are important regulators of reproduction, physiology, and development in a variety of animal taxa, including vertebrates and mollusks. Steroid hormone receptors, which mediate the classic cellular responses to these hormones, were thought to be vertebrate specific, which left the molecular mechanisms of steroid action in invertebrates unresolved. Recently an estrogen receptor (ER) ortholog was isolated from the sea hare Aplysia californica, but the functional significance of the receptor was unclear because estrogens and other steroids are not known to be important in that species. Furthermore, the Aplysia ER was found to be a constitutive transcriptional activator, but it was unclear whether the estrogen independence of the ER was an Aplysia-specific novelty or a more ancient character general to the mollusks. Here we report on the isolation and functional characterization of the first ER ortholog from an invertebrate in which estrogens are produced and play an apparent role, the cephalopod Octopus vulgaris. We show that the Octopus ER is a strong constitutive transcriptional activator from canonical estrogen response elements. The receptor does not bind estradiol and is unresponsive to estrogens and other vertebrate steroid hormones. These characteristics are similar to those observed with the Aplysia ER and support the hypothesis that the evolving ER gained constitutive activity deep in the mollusk lineage. The apparent reproductive role of estrogens in Octopus and other mollusks is unlikely to be mediated by the ER and may take place through an ancient, non-ER-mediated pathway.

Amino Acid Sequence↗