Behavioral Analysis of Cuttlefish Traveling Waves and Its Implications for Neural Control

SummaryTraveling waves (from action potential propagation to swimming body motions or intestinal peristalsis) are ubiquitous phenomena in biological systems and yet are diverse in form, function, and mechanism. An interesting such phenomenon occurs in cephalopod skin, in the form of moving pigmentation patterns called “passing clouds” [1]. These dynamic pigmentation patterns result from the coordinated activation of large chromatophore arrays [2]. Here, we introduce a new model system for the study of passing clouds, Metasepia tullbergi, in which wave displays are very frequent and thus amenable to laboratory investigations. The mantle of Metasepia contains four main regions of wave travel, each supporting a different propagation direction. The four regions are not always active simultaneously, but those that are show synchronized activity and maintain a constant wavelength and a period-independent duty cycle, despite a large range of possible periods (from 1.5 s to 10 s). The wave patterns can be superposed on a variety of other ongoing textural and chromatic patterns of the skin. Finally, a traveling wave can even disappear transiently and reappear in a different position (“blink”), revealing ongoing but invisible propagation. Our findings provide useful clues about classes of likely mechanisms for the generation and propagation of these traveling waves. They rule out wave propagation mechanisms based on delayed excitation from a pacemaker [3] but are consistent with two other alternatives, such as coupled arrays of central pattern generators [3] and dynamic attractors on a network with circular topology [4]

The underestimated giants: operant conditioning, visual discrimination and long-term memory in giant tortoises

Relatively little is known about cognition in turtles, and most studies have focused on aquatic animals. Almost nothing is known about the giant land tortoises. These are visual animals that travel large distances in the wild, interact with each other and with their environment, and live extremely long lives. Here, we show that Galapagos and Seychelle tortoises, housed in a zoo environment, readily underwent operant conditioning and we provide evidence that they learned faster when trained in the presence of a group rather than individually. The animals readily learned to distinguish colors in a two-choice discrimination task. However, since each animal was assigned its own individual colour for this task, the presence of the group had no obvious effect on the speed of learning. When tested 95 days after the initial training, all animals remembered the operant task. When tested in the discrimination task, most animals relearned the task up to three times faster than naive animals. Remarkably, animals that were tested 9 years after the initial training still retained the operant conditioning. As animals remembered the operant task, but needed to relearn the discrimination task constitutes the first evidence for a differentiation between implicit and explicit memory in tortoises. Our study is a first step towards a wider appreciation of the cognitive abilities of these unique animals

Squid adjust their body color according to substrate

Coleoid cephalopods camouflage on timescales of seconds to match their visual surroundings. To date, studies of cephalopod camouflage-to-substrate have been focused primarily on benthic cuttlefish and octopus, because they are readily found sitting on the substrate. In contrast to benthic cephalopods, oval squid (Sepioteuthis lessoniana species complex) are semi-pelagic animals that spend most of their time in the water column. In this study, we demonstrate that in captivity, S. lessoniana Sp.2 (Shiro-ika, white-squid) from the Okinawa archipelago, Japan, adapts the coloration of their skin using their chromatophores according to the background substrate. We show that if the animal moves between substrates of different reflectivity, the body patterning is changed to match. Chromatophore matching to substrate has not been reported in any loliginid cephalopod under laboratory conditions. Adaptation of the chromatophore system to the bottom substrate in the laboratory is a novel experimental finding that establishes oval squid as laboratory model animals for further research on camouflage

From the octopus to soft robots control: an octopus inspired behavior control architecture for soft robots

In recent years, breakthroughs have been made in both biology and robotics by the close cooperation between biologists and roboticists. Researchers in the fields of octopus biological study and soft robotics can also benefit from working together and inspiring each other. However, this collaboration is not easy because of the different research motivations and terminologies used. This paper starts from challenges for controlling soft robots, through biological inspirations from the octopus, to their engineering interpretation for creating a behavior control architecture for soft robots. Hypotheses related to the octopus biology from the engineering perspective are also proposed. This work serves as a case study in biologist-roboticist collaboration. It wishes to promote mutual understanding and cooperation between these two disciplines

Improving Keeping for Octopuses by Testing Different Escape-Proof Designs on Tanks for “Big Blue Octopus” (Octopus cyanea)

Octopus cyanea has a wide range of natural distribution and is interesting for scientific research. However, unlike Octopus vulgaris, the species is poorly studied, and few data exist on best practices for keeping them. One of the most common reasons for losing octopuses in human care is their ability to escape from holding tanks. Adult Octopus cyanea (n = 33) were locally collected in Okinawa throughout the year. All animals were housed at the laboratory facilities at the Marine Station of the Okinawa institute of Science and Technology. Animals were kept in a flow-through saltwater system in three different types of holding tanks ranging from 550 L to 600 L tanks or in 2000 L tanks, all with an environment enriched with clay pots or natural rocks as dens. They were fed a daily diet of dead fish or live or dead crustaceans ad libitum. To characterize the effectiveness of different keeping conditions, we compared escape attempts and non-natural deaths during the animals’ time under human care. We found that two types of tanks, the 600 L transparent acrylic glass tanks with weighted lids and the 2000 L tanks with synthetic grass lined walls, had significantly fewer escapes than the 550 L tanks

Recording electrical activity from the brain of behaving octopus

Octopuses, which are among the most intelligent invertebrates,1,2,3,4 have no skeleton and eight flexible arms whose sensory and motor activities are at once autonomous and coordinated by a complex central nervous system.5,6,7,8 The octopus brain contains a very large number of neurons, organized into numerous distinct lobes, the functions of which have been proposed based largely on the results of lesioning experiments.9,10,11,12,13 In other species, linking brain activity to behavior is done by implanting electrodes and directly correlating electrical activity with observed animal behavior. However, because the octopus lacks any hard structure to which recording equipment can be anchored, and because it uses its eight flexible arms to remove any foreign object attached to the outside of its body, in vivo recording of electrical activity from untethered, behaving octopuses has thus far not been possible. Here, we describe a novel technique for inserting a portable data logger into the octopus and implanting electrodes into the vertical lobe system, such that brain activity can be recorded for up to 12 h from unanesthetized, untethered octopuses and can be synchronized with simultaneous video recordings of behavior. In the brain activity, we identified several distinct patterns that appeared consistently in all animals. While some resemble activity patterns in mammalian neural tissue, others, such as episodes of 2 Hz, large amplitude oscillations, have not been reported. By providing an experimental platform for recording brain activity in behaving octopuses, our study is a critical step toward understanding how the brain controls behavior in these remarkable animals

Recording electrical activity from the brain of behaving octopus

Octopuses, which are among the most intelligent invertebrates,1,2,3,4 have no skeleton and eight flexible arms whose sensory and motor activities are at once autonomous and coordinated by a complex central nervous system.5,6,7,8 The octopus brain contains a very large number of neurons, organized into numerous distinct lobes, the functions of which have been proposed based largely on the results of lesioning experiments.9,10,11,12,13 In other species, linking brain activity to behavior is done by implanting electrodes and directly correlating electrical activity with observed animal behavior. However, because the octopus lacks any hard structure to which recording equipment can be anchored, and because it uses its eight flexible arms to remove any foreign object attached to the outside of its body, in vivo recording of electrical activity from untethered, behaving octopuses has thus far not been possible. Here, we describe a novel technique for inserting a portable data logger into the octopus and implanting electrodes into the vertical lobe system, such that brain activity can be recorded for up to 12 h from unanesthetized, untethered octopuses and can be synchronized with simultaneous video recordings of behavior. In the brain activity, we identified several distinct patterns that appeared consistently in all animals. While some resemble activity patterns in mammalian neural tissue, others, such as episodes of 2 Hz, large amplitude oscillations, have not been reported. By providing an experimental platform for recording brain activity in behaving octopuses, our study is a critical step toward understanding how the brain controls behavior in these remarkable animals