Program in Sensory Physiology and Behavior


A thin crescent of ice was still on Eel Pond when Pablo Correa came to the MBL last March to begin shooting a video. Correa’s visit was exploratory: He knew he wanted to make a short documentary about the MBL, but hadn’t defined a focus beyond the diverse animals maintained in the Marine Resources Center. Correa spent several days shadowing David Remsen, manager of the Marine Resources Department, and his staff, and he took an early-season sail with them on the MBL’s collecting boat, the Gemma. He also observed several MBL scientists who use marine animals as model organisms in their research.

The video Correa ended up making, “These Eyes Follow the Moon,” is not a typical documentary. It is nearly wordless and impressionistic. Yet it also captures an essential “feeling” about the MBL. It moves from the wide-open spaces of the MBL’s ocean setting to the quiet, focused concentration in labs where instruments are prepared for the microscopic imaging of cells. The video also reflects the rhythm of Marine Resources just as the collecting season starts up in early spring. (The MBL collects marine organisms for biological research from April through December, with August being the high season when squid and many other species are collected daily. “August is also the time of year when anything unusual starts to show up in the nets,” Remsen says.)

Correa is editor of the science section of El Espectador, a daily newspaper with national circulation based in Bogotá, Colombia; and a free-lancer for SciDev.net, a network that publishes science news from developing countries. He was a fellow in MIT’s Knight Science Journalism program in 2012-2013.

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Featured in this video are:

In the Marine Resources Center: Skate (Rajidae) at 0:06, 0:24 and 0:33; spider crabs (Libinia) at 3:30; scup (Stenotomus) at 3:40; spiny dogfish (Squalus ) at 4:10; seahorse (Hippocampus) at 4:16. At 4:30, Dave Remsen describes the eyes of the horseshoe crab (Limulus). At 5:30, cuttlefish (Sepiida) for the study of cephalopod camouflage in Roger Hanlon’s laboratory.

Movie of squid skin at 6:27 by Trevor Wardill and Paloma Gonzalez-Bellido: Confocal z-stack of squid skin, blue and green colors showing tissue auto fluorescence and Lucifer yellow forward filled neurons shifted to red using antibodies.

Gonzalez-Bellido PT and Wardill TJ (2012). Labeling and confocal imaging of neurons in thick invertebrate tissue samples. Cold Spring Harb Protoc: doi:10.1101/pdb.prot069625

Movie of dividing cells at 7:20 by James LaFountain and Rudolf Oldenbourg: The events of cell division during meiosis I in a living insect spermatocyte. Testes from the Crane fly Nephrotoma suturalis were observed with time-lapse liquid crystal polarized light microscopy (LC-PolScope, MBL, Woods Hole MA, and PerkinElmer, Hopkinton MA). Movie images display the naturally occurring birefringence of cell organelles and structures that are made up of aligned molecules, such as the meiotic spindle and mitochondria. Horizontal image width is 56 µm.

Some people prefer strong vertical lines in their clothing over horizontal ones, as they can appear slimming. As for cuttlefish? According to a new MBL study, when these marine creatures adaptively change their skin patterns for camouflage purposes, they respond to vertical visual cues in their environment more strongly than to horizontal cues.

A cuttlefish next to a checked wall pattern displays adaptive camouflage. Photo courtesy of Kim Ulmer, MBL

A cuttlefish next to a checked wall pattern displays adaptive camouflage.
Photo courtesy of Kim Ulmer, MBL

The study, led by Kimberly Ulmer and Roger Hanlon in the MBL’s Program in Sensory Physiology and Behavior, is published in the April issue of the Biological Bulletin.

Many prior experiments have shown the influence of two-dimensional (2D) substrates, such as sand and gravel habitats, on camouflage, yet many marine habitats have three-dimensional (3D) structures, such as rocks and coral, among which cuttlefish camouflage from predators. In this study, Ulmer and Hanlon tested the relative influence of horizontal versus vertical visual cues on cuttlefish camouflage. They found that visual stimuli in the vertical dimension (2D or 3D) have a stronger influence on changeable camouflage than do 2D stimuli presented horizontally. This effect is noteworthy because in many of the experiments, the vertical stimuli represented only a small proportion of the total visual surrounds, indicating that cuttlefish are selectively responding to vertical cues.

Such choices highlight the selective decision-making that occurs in cuttlefish as they determine their camouflage body patterns.

Citation:

Ulmer KM, KC Buresch, MM Kossodo, LM Mathger, LA Siemann and RT Hanlon (2013) Vertical visual features have a strong influence on cuttlefish camouflage. Biological Bulletin 224: 110-118.

Paloma T. Gonzalez-Bellido, who is now a postdoctoral scientist at the Marine Biological Laboratory (MBL), and colleagues from Howard Hughes Medical Institute, University of Minnesota, and Union College have been awarded a 2012 Cozzarelli Prize by the editorial board of Proceedings of the National Academy of Sciences (PNAS).

Gonzalez-Bellido and colleagues were honored for the “scientific excellence and originality” of their study of prey detection and interception in dragonflies.

The research was performed at Howard Hughes Medical Institute’s Janelia Farm Research Campus, where Gonzalez-Bellido was a postdoctoral scientist prior to joining the MBL’s Program in Sensory Physiology and Behavior in September 2011.

The study provides insight into basic visual-motor neural processing, and has implications for the development of “bioinspired” prosthetics for humans.

Green Darner Dragonfly Credit CC:Brian Robert Marshall

A green darner dragonfly, a member of the Aeshnidae family, in which Robert Olberg of Union College originally discovered the target-selective descending neurons (TSDNs). Credit: Brian Robert Marshall/Wikimedia

“I am honored to receive recognition for this work, for which we bridged the clinical and neuroethological fields, and developed new techniques,” says Gonzalez-Bellido. “This award has provided me with fuel to keep up the hard work and further my research plans.”

In order for a dragonfly to intercept its prey in midair (which dragonflies do with a 95% success rate), it needs to quickly track the prey and predict its future location. To understand how they undertake this complex task, Gonzalez-Bellido and her co-authors studied a small group of 16 motor neurons, called target-selective descending neurons (TSDNs), in the dragonfly Libellula luctuosa. These neurons, originally discovered by co-author Robert M. Olberg (Union College) in the green darner dragonfly, originate in the brain and extend to the thoracic ganglia, where the neural signal is interpreted and translated into wing muscle movements. Surprisingly, the scientists found that this small group of neurons can detect the direction of target prey with high accuracy and reliability across 360 degrees, and that this information is relayed from the brain to the wing motor centers in population vector form.

In 1988, co-author Apostolos Georgopoulos and his colleagues showed in monkeys that from the activity of neurons in the motor cortex, the population vector algorithm can predict the monkey’s upcoming arm movement. However, to achieve a more accurate prediction with this algorithm, upwards of 200 neurons were needed. Thus, the present discovery that a highly accurate neural code carrying information about target direction can be achieved with just 16 neurons is enlightening, and could have applications in the development of bioinspired robots. (Georgopolos is an MD-PhD at the University of Minnesota/Veterans Administration Medical Center who is interested in the development of prosthetics.)

Paloma-Gonzalez-Bellido Credit HHMI:Janelia Farm

Paloma Gonzalez-Bellido. Credit: HHMI/Janelia Farm

Randy Schekman, PhD, editor-in-chief of PNAS, describes the papers chosen for the Cozzarelli Prize as being “of exceptional interest… These papers are not merely technically superior but have had special impact and maybe novel techniques or novel applications of techniques, or very important discoveries.”

For this study, Gonzalez-Bellido and Trever Wardill (then at HHMI) developed a new protocol for labeling and confocal imaging of neurons in thick invertebrate tissue samples. In addition, her co-authors and former HHMI colleagues Hanchuan Peng and Jinzhu Yang developed a method for automatic 3D digital reconstruction (tracing) of neurons in microscopic images.

Gonzalez-Bellido sees the dragonfly as a promising model for understanding the evolution of neural systems. “It’s exciting that the same computation [the population vector algorithm] is used by monkeys and dragonflies for this task. Dragonflies belong to the most ancient groups of flying insects on earth, and they have changed little in 250 million years” she says.

The Cozzarelli Award was established in 2005 and named in 2007 to honor late PNAS editor-in-chief Nicholas R. Cozzarelli. Gonzalez-Bellido and the other awardees will be recognized at an awards ceremony during the National Academy of Sciences Annual Meeting on April 28, 2013, in Washington, D.C.

Out of more than 3,700 papers published in the journal last year, the editors selected Gonzalez-Bellido’s paper and five others for the Cozzarelli Prize.

Citation: 

Gonzalez-Bellido PT, Peng H, Yang J, Georgopoulos AP and Olberg RM (2012) Eight pairs of descending visual neurons in the dragonfly give wing motor centers accurate population vector of prey direction. PNAS 110: 696-701 /doi/10.1073/pnas.1210489109

A PNAS commentary on the paper is here.

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Among the animals that are appealing “cover models” for scientific journals, lancelets don’t spring readily to mind. Slender, limbless, primitive blobs that look pretty much the same end to end, lancelets “are extremely boring. I wouldn’t recommend them for a home aquarium,” says Enrico Nasi, adjunct senior scientist in the MBL’s Cellular Dynamics Program. Yet Nasi and his collaborators managed to land a lancelet on the cover of The Journal of Neuroscience last December. These simple chordates, they discovered, offer insight into our own biological clocks.

The head of the marine invertebrate amphioxus (Branchiostoma floridae), magnified 15 times. Amphioxus are the most ancient of the chordates (animals whose features include a nerve cord), according to molecular analysis. They are important to the study of the origin of vertebrates. Photo by Maria del Pilar Gomez. Click for larger version.

Nasi and his wife, MBL adjunct scientist Maria del Pilar Gomez, are interested in photo-transduction, the conversion of light by light-sensitive cells into electrical signals that are sent to the brain. The lancelet, also called amphioxus, doesn’t have eyes or a true brain. But what it does have in surprising abundance is melanopsin, a photopigment that is also produced by the third class of light-sensitive cells in the mammalian retina, besides the rods and cones. This third class of cells, called “intrinsically photosensitive retinal ganglion cells” (ipRGCs), were discovered in 2002 by Brown University’s David Berson and colleagues. Now sometimes called “circadian receptors,” they are involved in non-visual, light-dependent functions, such as adjustment of the animal’s circadian rhythms.

“It seemed like colossal overkill that amphioxus have melanopsin-producing cells,” Nasi says. “These animals do nothing. If you switch on a light, they dance and float to the top of the tank, and then they drop back down to the bottom. That’s it for the day.” But that mystery aside, Gomez and Nasi realized that studying amphioxus could help reveal the evolutionary history of the circadian receptors.

Amphioxus can grow as long as 2.5 inches and are typically found half-burrowed in sand. Photo by Hans Hillewaert.

As so it has. In 2009, Gomez and Nasi isolated the animal’s melanopsin-producing cells and described how they transduce light. In their recent paper, they tackled the puzzling question of why the light response of these amphioxus cells is several orders of magnitude higher than that of their more sophisticated, presumed descendents, the ipRGCs. (In mammals, the ipRGCs relay information on light and dark to the biological clock in the hypothalamus, where it is crucial for the regulation of circadian rhythms and associated control of hormonal secretion.)

By detailing how the large light response occurs in the amphioxus cells, Gomez and Nasi could relate their observations to the functional changes that may have occurred as the circadian receptors evolved and “eventually tailored their performance to the requirements of a reporter of day and night, rather than to a light sensor meant to mediate spatial vision.” The light-sensing cells of amphioxus, they discovered, may be the ”missing link“ between the visual cells of invertebrates and the circadian receptors in our own eyes.

Citations

Ferrer C., Melagón G., del Pilar Gomez M., and Nasi E. (2012) Dissecting the Determinants of Light Sensitivity in Amphioxus Microvillar Photoreceptors: Possible Evolutionary Implications for Melanopsin Signaling. J. Neurosci. 32: 17977-17987.

del Pilar Gomez M., Angueyra J.M, and Nasi E. (2009) Light-transduction in melanopsin-expressing photoreceptors of Amphioxus. PNAS 16: 9081-9086.

Enrico Nasi and Maria Gomez (second and third from left) with some of their students from the Universidad Nacional, de Colombia, where they hold faculty appointments. Nasi and Gomez regularly bring students to the MBL, where they are affiliated with the Program in Sensory Physiology and Behavior in addition to Cellular Dynamics.

What could a device like the Amazon Kindle possibly have in common with a cuttlefish?

Both depend on reflective surfaces to vividly communicate information.  For tablets and other e-devices, synthetic reflective e-paper is used to deliver the best available display technology for users.  For cuttlefish and their relatives, squid and octopus, (all of which belong to class of animals called cephalopods), their remarkable skin provides natural reflectivity with very efficient manipulation of available light. This enables their adaptive coloration for communication or camouflage with a speed and diversity unparalleled in the animal kingdom.

Credit: Lisa Ventre, University of Cincinnati

A new paper from MBL biologists Lydia Mäthger and Roger Hanlon and material scientists from the University of Cincinnati, the Air Force Research Laboratory and the Army Research Laboratory examines the parallels between e-Paper technology (the technology behind sunlight-readable devices like the Kindle) and the mechanisms of adaptive coloration in cephalopods.

The researchers note that while the basic approach for color change is similar in techie devices and in nature, humanity has never developed anything as complex or sophisticated as the biology and physics of cephalopod skin.

With their collaboration, the scientists propose three hopeful outcomes for the interdisciplinary community: that reflective display engineers may gain new insights from millions of years of natural selection and evolution; that biologists will benefit from understanding the types of mechanisms, characterization, and metrics used in synthetic reflective e-Paper; and that all scientists will gain a clearer picture of the long-term prospects for capabilities such as adaptive concealment and signaling.

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