Richard A. Satterlie

Muscle Organization of the Cubozoan Jellyfish Tripedalia cystophora Conant 1897

The musculature of the cubomedusa Tripedalia cystophora was investigated using immunohistochemical staining with an anti-actin antibody and histochemical staining with fluorescent phalloidin. The subumbrella is lined with a sheet of circular, striated muscle that is interrupted at the perradii, and by the nerve ring. The sheet is continuous with circular, striated muscle of the velarium, which turns radially on each face of the four velarial frenula. Perradial strips of smooth muscle run radially from just above the level of the rhopalia into the manubrium and lips. The strips give off perpendicular offshoots that run a short distance in parallel with the circular swim muscle. Musculature of the tentacles and pedalia is longitudinal and limited to the oral side of the pedalia. The pedalial muscle connects with bundles of smooth muscle that runs circularly from the tentacle base well into the subumbrella. The arrangement of striated muscle in the frenula suggests that these structures may function in directional nozzle formation of the velarium during turning. In addition, the perpendicular branching of the radial strips and the circular extensions of pedalial muscle may function in hinge formation to aid bending of the pedalia and tentacles into the subumbrella during feeding and protective responses.

The black box, the creature from the Black Lagoon, August Krogh, and the dominant animal

An organism is a complex chemical system that can respond to its environment, reproduce, grow, and develop in form and function, and maintain some measure of homeostasis. Nonetheless, it is a mistake to reduce the study of organisms to the level of chemistry, physics, or molecular biology. The system is highly integrated, and the properties of intact organisms are what determine their fitness in a changing environment, making the individual the primary unit of selection as well as the primary unit that interacts with the environment. Organismal biology seeks to describe and understand the responses of these complex biological systems to environmental challenges (both external and internal) as well as how they affect their environment. This approach works best when studies of model organisms are integrated into broader comparative investigations, over several levels of organization (populations, whole organisms, organs, tissues, cells, and genomes) and over time-frames from fractions of a second to millions of years. Organisms are the bridge between genomes and ecosystems, and between genetics and evolution. The impacts of environmental changes are reflected in the organism’s structure, function, development, growth, evolution, distribution, and diversity, all being dependent upon its ability, or inability, to adapt and survive. Conversely, the organism shapes the environment in both subtle and profound ways. In short, as organisms go, so go their genes and their populations—and our world. The development of modern molecular biology, genetics, and genomics (along with other ‘‘omics’’) has strengthened the interrelationships between field and laboratory in forming testable hypotheses for aspects of evolutionary change and responses to environmental change (Wake 2003). This two-way integration can, and does, arise at either end of a continuum extending from molecules to ecosystems in a highly hierarchical system. Integrative biology thus argues for a horizontal collaboration and cooperation in attacking important questions in biological research. This is more than a wave of the future; it is a valuable ongoing approach with incredible potential for the advancement of our base of knowledge in biology. Laying out ‘‘biology’’ in an overtly simplistic linear template based on structural and functional organization with molecules on one end and ecosystems on the other, we have a rather large middle ground. Organismal biology occupies this middle ground; hence any truly integrative study must pass through this region to construct large-scale concepts. When standing in this middle ground, one gets the sense that this region of organization is sometimes treated like a black box from which interesting jumps are made into molecules or populations, from laboratory or field perspectives. But returning to the organism is often

Changes in wingstroke kinematics associated with a change in swimming speed in a pteropod mollusk, Clione limacina

SUMMARY In pteropod mollusks, the gastropod foot has evolved into two broad, wing-like structures that are rhythmically waved through the water for propulsion. The flexibility of the wings lends a tremendous range of motion, an advantage that could be exploited when changing locomotory speed. Here, we investigated the kinematic changes that take place during an increase in swimming speed in the pteropod mollusk Clione limacina. Clione demonstrates two distinct swim speeds: a nearly constant slow swimming behavior and a fast swimming behavior used for escape and hunting. The neural control of Cliones swimming is well documented, as are the neuromuscular changes that bring about Cliones fast swimming. This study examined the kinematics of this swimming behavior at the two speeds. High speed filming was used to obtain 3D data from individuals during both slow and fast swimming. Cliones swimming operates at a low Reynolds number, typically under 200. Within a given swimming speed, we found that wing kinematics are highly consistent from wingbeat to wingbeat, but differ between speeds. The transition to fast swimming sees a significant increase in wing velocity and angle of attack, and range of motion increases as the wings bend more during fast swimming. Clione likely uses a combination of drag-based and unsteady mechanisms for force production at both speeds. The neuromuscular control of Cliones speed change points to a two-gaited swimming behavior, and we consider the kinematic evidence for Cliones swim speeds being discrete gaits.

Control of vortex rings for manoeuvrability

Manoeuvrability is critical to the success of many species. Selective forces acting over millions of years have resulted in a range of capabilities currently unmatched by machines. Thus, understanding animal control of fluids for manoeuvring has both biological and engineering applications. Within inertial fluid regimes, propulsion involves the formation and interaction of vortices to generate thrust. We use both volumetric and planar imaging techniques to quantify how jellyfish (Aurelia aurita) modulate vortex rings during turning behaviour. Our results show that these animals distort individual vortex rings during turns to alter the force balance across the animal, primarily through kinematic modulation of the bell margin. We find that only a portion of the vortex ring separates from the body during turns, which may increase torque. Using a fluorescent actin staining method, we demonstrate the presence of radial muscle fibres lining the bell along the margin. The presence of radial muscles provides a mechanistic explanation for the ability of scyphomedusae to alter their bell kinematics to generate non-symmetric thrust for manoeuvring. These results illustrate the advantage of combining imaging methods and provide new insights into the modulation and control of vorticity for low-speed animal manoeuvring.

The search for ancestral nervous systems: an integrative and comparative approach

Even the most basal multicellular nervous systems are capable of producing complex behavioral acts that involve the integration and combination of simple responses, and decision-making when presented with conflicting stimuli. This requires an understanding beyond that available from genomic investigations, and calls for a integrative and comparative approach, where the power of genomic/transcriptomic techniques is coupled with morphological, physiological and developmental experimentation to identify common and species-specific nervous system properties for the development and elaboration of phylogenomic reconstructions. With careful selection of genes and gene products, we can continue to make significant progress in our search for ancestral nervous system organizations.

Multiple Conducting Systems in the Cubomedusa Carybdea marsupialis

Acute responses to mechanical, electrical, and photic stimuli were used to describe neural conducting systems in the cubomedusan jellyfish Carybdea marsupialis underlying three behaviors: contractile responses of single tentacles, protective crumple responses, and alterations of swimming activity by the visual system. Responses of single tentacles consisted of tentacular shortening and inward pedalial bending, and were accompanied by bursts of extracellularly recorded spike activity that were restricted to the stimulated tentacle. With nociceptive stimuli delivered to the subumbrella or margin, all four tentacles produced similar responses in a crumple response. The spike bursts in all four tentacles showed coordinated firing as long as the nerve ring was intact. Crumples were still produced following cuts through the nerve ring, but the activity in individual tentacles was no longer coordinated. Responses to light-on stimulation of a rhopalium, as recorded from the pacemaker region, were weak and inconsistent, but when present, resulted in a stimulation of swimming activity. In comparison, light-off responses were robust and resulted in temporary inhibition of swimming activity. Light-off responses were conducted in the nerve ring to unstimulated rhopalia. In conclusion, three conducting systems have been described as components of the rhopalia-nerve ring centralized system in Carybdea: the swim motor system, the crumple coordination system, and the light-off response system.

A hyperpolarization-activated inward current alters swim frequency of the pteropod mollusk Clione limacina.

The pteropod mollusk, Clione limacina, exhibits behaviorally relevant swim speed changes that occur within the context of the animals ecology. Modulation of C. limacina swimming speed involves changes that occur at the network and cellular levels. Intracellular recordings from interneurons of the swim central pattern generator show the presence of a sag potential that is indicative of the hyperpolarization-activated inward current (I(h)). Here we provide evidence that I(h) in primary swim interneurons plays a role in C. limacina swimming speed control and may be a modulatory target. Recordings from central pattern generator swim interneurons show that hyperpolarizing current injection produces a sag potential that lasts for the duration of the hyperpolarization, a characteristic of cells possessing I(h). Following the hyperpolarizing current injection, swim interneurons also exhibit postinhibitory rebound (PIR). Serotonin enhances the sag potential of C. limacina swim interneurons while the I(h) blocker, ZD7288, reduces the sag potential. Furthermore, a negative correlation was found between the amplitude of the sag potential and latency to PIR. Because latency to PIR was previously shown to influence swimming speed, we hypothesize that I(h) has an effect on swimming speed. The I(h) blocker, ZD7288, suppresses swimming in C. limacina and inhibits serotonin-induced acceleration, evidence that supports our hypothesis.

Toward an Organismal Neurobiology: Integrative Neuroethology

Overt behavior is generated in response to a palette of external and internal stimuli and internal drives. Rarely are these variables introduced in isolation. This creates challenges for the organism to sort inputs that frequently favor conflicting behaviors. Under these conditions, the nervous system relies on established and flexible hierarchies to produce appropriate behavioral changes. The pteropod mollusc Clione limacina is used as an example to illustrate a variety of behavioral interactions that alter a baseline behavioral activity: slow swimming. The alterations include acceleration within the slow swimming mode, acceleration from the slow to fast swimming modes, whole body withdrawal (and inhibition of swimming), food acquisition behavior (with a feeding motivational state), and a startle locomotory response. These examples highlight different types of interaction between the baseline behavior and the new behaviors that involve external stimuli and two types of internal drives: a modular arousal system and a motivational state. The investigation of hierarchical interactions between behavioral modules is a central theme of integrative neuroethology that focuses on an organismal level of understanding of the neural control of behavior.

Recent developments in neurobiology: introduction to the symposium to honor Professor Douglas G. Stuart

This year’s symposiuim ‘‘Recent Developments in Neurobiology’’ honors Dr Douglas G. Stuart, Regents’ Professor Emeritus of Physiology at the University of Arizona for his long-time contribution to research in the field of neural control of movement, and for his service to the development of neuroscience research in the State of Arizona and beyond (Fig. 1). In addition to his long list of research accomplishments (summarized subsequently), Professor Stuart served as the Head of Physiology at the University of Arizona, and as Associate Dean of Research at the UA College of Medicine. He was a founding member of the College of Medicine (1967) and was awarded Regents’ Professor status in 1990. Professor Stuart has over 120 experimental papers in scientific journals, and over 80 chapters, reviews and symposium papers. In the recent years, he provided overviews on motor control and on the history of movement neuroscience.