Monkeys also believe in winning streaks, study shows

Humans have a well-documented tendency to see winning and losing streaks in situations that, in fact, are random. But scientists disagree about whether the “hot-hand bias” is a cultural artifact picked up in childhood or a predisposition deeply ingrained in the structure of our cognitive architecture.

Now in the first study in non-human primates of this systematic error in decision making, researchers find that monkeys also share our unfounded belief in winning and losing streaks. The results suggests that the penchant to see patterns that actually don’t exist may be inherited — an evolutionary adaptation that may have provided our ancestors a selective advantage when foraging for food in the wild, according to lead author Tommy Blanchard, a doctoral candidate in brain and cognitive sciences at the University of Rochester.

The cognitive bias may be difficult to override even in situations that are truly random. This inborn tendency to feel that we are on a roll or in a slump may help explain why gambling can be so alluring and why the stock market is so prone to wild swings, said coauthor Benjamin Hayden, assistant professor brain and cognitive sciences at the University of Rochester.

Hayden, Blanchard, and Andreas Wilke, an assistant professor of psychology at Clarkson University, reported their findings in the July issue of the Journal of Experimental Psychology: Animal Learning and Cognition.

To measure whether monkeys actually believe in winning streaks, the researchers had to create a computerized game that was so captivating monkeys would want to play for hours. “Luckily, monkeys love to gamble,” said Blanchard. So the team devised a fast-paced task in which each monkey could choose right or left and receive a reward when they guessed correctly.

The researchers created three types of play, two with clear patterns (the correct answer tended to repeat on one side or to alternate from side to side) and a third in which the lucky pick was completely random. Where clear patterns existed, the three rhesus monkeys in the study quickly guessed the correct sequence. But in the random scenarios, the monkeys continued to make choices as if they expected a “streak.” In other words, even when rewards were random, the monkeys favored one side.

The monkeys showed the hot-hand bias consistently over weeks of play and an average of 1,244 trials per condition. “They had lots and lots of opportunities to get over this bias, to learn and change, and yet they continued to show the same tendency,” said Blanchard.

So why do monkeys and humans share this false belief in a run of luck even when faced over and over with evidence that the results are random? The authors speculate that the distribution of food in the wild, which is not random, may be the culprit. “If you find a nice juicy beetle on the underside of a log, this is pretty good evidence that there might be a beetle in a similar location nearby, because beetles, like most food sources, tend to live near each other,” explained Hayden.

Evolution has also primed our brains to look for patterns, added Hayden. “We have this incredible drive to see patterns in the world, and we also have this incredible drive to learn. I think it’s very related to why we like music, and why we like to do crossword puzzles, Sudoku, and things like that. If there’s a pattern there, we’re on top of it. And if there may or may not be a pattern there, that’s even more interesting.”

Understanding the hot-hand bias could inform treatment for gambling addiction and provide insights for investors, said Hayden. “If a belief in winning streaks is hardwired, then we may want to look for more rigorous retaining for individuals who cannot control their gambling. And investors should keep in mind that humans have an inherited bias to believe that if a stock goes up one day, it will continue to go up.”

The results also could provide nuance to our understanding of free will, said Blanchard, who was drawn to the study of decision making during prior graduate training in philosophy. “Biases in our decision-making mechanisms, like this bias towards belief in winning and losing streaks, say something really deep about what sorts of creatures we are. We often like to think we make decisions based only on the information we’re conscious of. But we’re not always aware of why we make certain decisions or believe certain things.

“We’re a complex mix of biases and heuristics and statistical reasoning. When you put it all together, that’s how you get sophisticated behavior. We don’t know where a lot of these biases come from, but this study — and others like it — suggest many of them are due to cognitive mechanisms we share with our primate relatives,” said Blanchard.

This research was supported by grants from the National Science Foundation and the Brain and Behavior Research Foundation to Hayden.

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Rhesus proteins transport ions, not gas

Do they carry the gas ammonia or the ammonium ion in their luggage? And is transport active or passive? Biochemists have long speculate on the mechanistic details of the ammonium transport family of proteins (Amt), which include the Rhesus protein factors, known as the mammalian blood group system. What was previously known is that Amt proteins extend across cellular membranes where they specifically transport the nitrogen into bacteria and plant cells, essential nutrient for their growth and survival. In mammals, Rhesus proteins regulate acid and ion balance in kidney and liver cells. A team of scientists led by Prof. Dr. Susana Andrade from the Institute of Biochemistry of the University of Freiburg and the Cluster of Excellence BIOSS Centre for Biological Signalling Studies has now determined the transport properties of Amt proteins with great precision on the basis of electrophysiology tests on artificial lipid systems.

The scientists cloned the membrane proteins from an archaea, a microorganisms that lives under extreme temperature conditions and isolate them. In 2005, the Freiburg researchers already threw light on the crystalline three-dimensional structure of a protein of this kind. Now they have added the protein to a layer of lipid molecules, enabling them to measure the ion currents directly. The team discovered that a positive charge travels through the membrane: The membrane proteins do not transport the gas ammonia NH3 but rather the ammonium ion NH4+. The researchers published their findings in the journal Proceedings of the National Academy of Sciences of the USA.

“The results can, in a large part, be transferred to the Rhesus proteins from mammals,” says Andrade as Amt proteins bear a close resemblance to the Rhesus proteins found in humans. They are produced in the blood, in the kidney, and in the liver, where they regulate the intake of ammonium and thus the body’s pH. The researchers tested three Amt proteins that are present in the bacteria and also determined the speed with which they allow ammonium to pass through the membrane. “In the future, we want to modify individual components of the transporter to improve our understanding of the exact molecular details involved” explains Andrade.

The scientific debate on Amt/Rh proteins stems from the difficulty of distinguishing between ammonia and ammonium in measurements, as the two molecules are transformed into each other in a continuous state of balance with protons. “Our in vitro method gives us a level of precision that finally allows us to draw valid conclusions concerning the transport process,” stresses the researcher.

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Chimps like listening to music with a different beat

While preferring silence to music from the West, chimpanzees apparently like to listen to the different rhythms of music from Africa and India, according to new research published by the American Psychological Association.

“Our objective was not to find a preference for different cultures’ music. We used cultural music from Africa, India and Japan to pinpoint specific acoustic properties,” said study coauthor Frans de Waal, PhD, of Emory University. “Past research has focused only on Western music and has not addressed the very different acoustic features of non-Western music. While nonhuman primates have previously indicated a preference among music choices, they have consistently chosen silence over the types of music previously tested.”

Previous research has found that some nonhuman primates prefer slower tempos, but the current findings may be the first to show that they display a preference for particular rhythmic patterns, according to the study. “Although Western music, such as pop, blues and classical, sound different to the casual listener, they all follow the same musical and acoustic patterns. Therefore, by testing only different Western music, previous research has essentially replicated itself,” the authors wrote. The study was published in APA’s Journal of Experimental Psychology: Animal Learning and Cognition.

When African and Indian music was played near their large outdoor enclosures, the chimps spent significantly more time in areas where they could best hear the music. When Japanese music was played, they were more likely to be found in spots where it was more difficult or impossible to hear the music. The African and Indian music in the experiment had extreme ratios of strong to weak beats, whereas the Japanese music had regular strong beats, which is also typical of Western music.

“Chimpanzees may perceive the strong, predictable rhythmic patterns as threatening, as chimpanzee dominance displays commonly incorporate repeated rhythmic sounds such as stomping, clapping and banging objects,” said de Waal.

Sixteen adult chimps in two groups participated in the experiment at the Yerkes National Primate Research Center at Emory University. Over 12 consecutive days for 40 minutes each morning, the groups were given the opportunity to listen to African, Indian or Japanese music playing on a portable stereo near their outdoor enclosure. Another portable stereo not playing any music was located at a different spot near the enclosure to rule out behavior that might be associated with an object rather than the music. The different types of music were at the same volume but played in random order. Each day, researchers observed the chimps and recorded their location every two minutes with handwritten notes. They also videotaped the activity in the enclosure. The chimps’ behavior when the music was played was compared to their behavior with no music.

“Chimpanzees displaying a preference for music over silence is compelling evidence that our shared evolutionary histories may include favoring sounds outside of both humans’ and chimpanzees’ immediate survival cues,” said lead author Morgan Mingle, BA, of Emory and Southwestern University in Austin. “Our study highlights the importance of sampling across the gamut of human music to potentially identify features that could have a shared evolutionary root.”

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To avoid interbreeding, monkeys have undergone evolution in facial appearance

Old World monkeys have undergone a remarkable evolution in facial appearance as a way of avoiding interbreeding with closely related and geographically proximate species, researchers from New York University and the University of Exeter have found. Their research provides the best evidence to date for the role of visual cues as a barrier to breeding across species.

“Evolution produces adaptations that help animals thrive in a particular environment, and over time these adaptations lead to the evolution of new species,” explains James Higham, an assistant professor in NYU’s Department of Anthropology and the senior author of the study, which appears in the journal Nature Communications. “A key question is what mechanisms keep closely related species that overlap geographically from inter-breeding, so that they are maintained as separate species.

“Our findings offer evidence for the use of visual signals to help ensure species recognition: species may evolve to look distinct specifically from the other species they are at risk of inter-breeding with. In other words, how you end up looking is a function of how those around you look. With the primates we studied, this has a purpose: to strengthen reproductive isolation between populations.”

The study’s lead author was William Allen, who undertook the work while a post-doctoral researcher in NYU’s Department of Anthropology. The researchers studied guenons — a group of more than two dozen species of monkeys indigenous to the forests of Central and West Africa. Many different species of guenons are often sympatric — they live in close proximity to each other, with multiple species often traveling, feeding, and sleeping side-by-side. Therefore interbreeding, which could result in afflicted infertile offspring, remains an unwelcome possibility.

In the 1980s, Oxford zoologist Jonathan Kingdon tried to explain the diversity in facial appearance of guenons, which show markings such as differently colored eyebrow patches, ear tufts, nose spots, and mouth patches. He hypothesized that sympatric guenon species had undergone facial changes that visually reinforced differences among their species in order to avoid the risks of hybridizing.

However, Kingdon’s ideas were primarily based on observations with the naked eye, and he failed to find evidence for his hypotheses. The NYU and University of Exeter scientists sought to test Kingdon’s conclusions quantitatively using sophisticated methods — facial recognition algorithms that can identify and quantify detailed features in faces.

To do this, they photographed nearly two dozen species of guenons in various settings, over an 18-month period: in zoos in the United States and the United Kingdom and in a wildlife sanctuary in Nigeria. Armed with more than 1,400 standardized photographs, the researchers employed what is known as the eigenface technique, which has been used in the field of computer vision for machine recognition of faces, in order to distinguish primate features and then to determine whether the appearance of each guenon species was related to the appearance of other species.

Their results showed that, as predicted, the face patterns of guenon species have evolved to become more visually distinctive — specifically from those guenon species they overlap with geographically — and hence those that they are risk of hybridizing with.

“These results strongly suggest that the extraordinary appearance of these monkeys has been due to selection for visual signals that discourage hybridization,” observes lead author Allen, now at the University of Hull. “This is perhaps the strongest evidence to date for a role for visual signals in the key evolutionary processes by which species are formed and maintained, and it is particularly exciting that we have found it in part of our own lineage.”

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Facial Features of Old World Monkeys Evolved to Prevent Interbreeding

Old World monkeys have undergone a remarkable evolution in facial appearance as a way of avoiding interbreeding with closely related and geographically proximate species, researchers from New York University and the University of Exeter have found. Their research provides the best evidence to date for the role of visual cues as a barrier to breeding across species.

“Evolution produces adaptations that help animals thrive in a particular environment, and over time these adaptations lead to the evolution of new species,” explains James Higham, an assistant professor in NYU’s Department of Anthropology and the senior author of the study, which appears in the journal Nature Communications. “A key question is what mechanisms keep closely related species that overlap geographically from inter-breeding, so that they are maintained as separate species.

“Our findings offer evidence for the use of visual signals to help ensure species recognition: species may evolve to look distinct specifically from the other species they are at risk of inter-breeding with. In other words, how you end up looking is a function of how those around you look. With the primates we studied, this has a purpose: to strengthen reproductive isolation between populations.”

Full story here .

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Chimpanzees Observed Making A Fashion Statement — Sticking Blades Of Grass In Their Ears

“Our observation is quite unique in the sense that nothing seems to be communicated by it,” says study author Edwin van Leeuwen, a primate expert at the Max Planck Institute in The Netherlands.

To figure out if this was really a tradition, and not just chimpanzees sticking grass in their ears at random, van Leeuwen and his colleagues spent a year observing four chimp groups in Chimfunshi Wildlife Orphanage Trust, a sanctuary in Zambia. Only one troop performed the grass-in-ear behavior, although all of the chimps lived in the same grassy territory. There’s no genetic or ecological factors, the scientists believe, that would account for this behavior — only culture.

Lydia Luncz, a primatologist at the Max Planck Institute in Leipzig, Germany, who was not involved with the research, agrees. This study shows how the chimpanzees who learned to put grass in their ears did so through the “natural transmission” of new behavior, she says.

The cultural quirk first popped up in 2010 when a chimpanzee, named Julie, was spotted sporting a long-stemmed piece of grass.

Full story here .

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That’s So Random: Why We Persist in Seeing Streaks

Animal testing methods for some chemicals should change, experts urge

Challenging risk assessment methods used for decades by toxicologists, a new review of the literature led by environmental health scientist Laura Vandenberg at the University of Massachusetts Amherst suggests that oral gavage, the most widely accepted method of dosing lab animals to test chemical toxicity, does not accurately mimic how humans are exposed to chemicals in everyday life.

Oral gavage refers to the way researchers give chemicals to animals by putting a tube down their throats to deliver substances directly to the stomach. It has been used for decades and is at present the dosing scheme preferred for assessing potential toxicity of endocrine disrupting chemicals (EDC) by regulatory agencies.

Vandenberg, with colleagues at the University of Missouri-Columbia and Université de Toulouse, France, writes, “We conclude that gavage may be preferred over other routes for some environmental chemicals in some circumstances, but it does not appropriately model human dietary exposures for many chemicals. Because it avoids exposure pathways, is stressful and thus interferes with endocrine responses, gavage should be abandoned as the default route of administration for hazard assessments of EDCs.”

Though gavage does offer precise dose and timing control, the authors say it is not appropriate for assessing EDCs, using Bisphenol A (BPA) as a primary example. Its drawbacks include the fact that gavage bypasses the mouth, which means animals experience “dramatic differences in absorption, bioavailability and metabolism” than humans experience when eating food, which is thought to be the way most people are exposed to BPA. Further, gavage carries well-known risks including perforation of the esophagus that diminish its value.

Finally, the authors point out that the gavage protocol itself can induce stress responses in the endocrine system, which may confound EDC assessment. “We propose the exploration of alternatives to mimic human exposures when there are multiple exposure routes/sources and when exposures are chronic,” they urge. Their work appears in the current issue of Environmental Health.

Vandenberg and colleagues say they chose BPA because exposure is widespread in humans, low doses have been linked to adverse effects in laboratory animals, exposure is linked to a wide range of human diseases, and unanswered questions remain about how best to model exposure routes and sources. The lack of detailed understanding of all potential routes of exposure applies to many chemicals used in a wide range of products, they add.

The researchers reviewed more than 60 papers and reports, pointing out that “for hypothesis testing, route of exposure may not be of central importance, but for hazard assessment, risk assessors typically require that studies use a route of exposure that is deemed ‘relevant’ to humans.”

They point to recent studies in dogs and monkeys where scientists could study different BPA absorption when it was administered both by mouth and by traditional gavage. Given to dogs under the tongue, BPA entered into circulation largely in an unconjugated form, that is, without having been converted to an inactive form by the liver in so-called first-pass metabolism. By comparison, over 99 percent of the BPA was metabolized rapidly in the dogs with gavage. Similarly, less than 1 percent of administered BPA was bioavailable in blood in a gavage experiment with monkeys, while BPA fed in a piece of fruit resulted in over 7 percent of administered BPA being bioavailable in blood.

The authors point out that while “all dosing methods have pros and cons that must be considered in the design of a study,” recent studies suggest that gavage may interfere with the study of EDCs and viable alternatives do exist. EDCs and drugs can be administered by milling a compound into feed, dissolving it in drinking water, feeding animals from a pipette or adding a compound to a wafer or other food. Also, implanted devices and osmotic pumps “are of particular interest in BPA studies because they can provide constant exposures to low doses that produce serum concentrations that approximate those found in humans. These routes of exposure may be relevant also because there are important and significant non-oral sources of BPA exposure,” Vandenberg and colleagues state.

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Herpes Infected ‘Since Before We Were Human’

Humans and monkeys of one mind when it comes to changing it

Covert changes of mind can be discovered by tracking neural activity when subjects make decisions, researchers from New York University and Stanford University have found. Their results, which appear in the journal Current Biology, offer new insights into how we make decisions and point to innovative ways to study this process in the future.

“The methods used in this study allowed us to see the idiosyncratic nature of decision making that was inaccessible before,” explains Roozbeh Kiani, an assistant professor in NYU’s Center for Neural Science and the study’s lead author.

The study’s other authors included Christopher Cueva and John Reppas of Stanford’s Department of Neurobiology and William Newsome, who holds appointments at the university’s Department of Neurobiology and at the Howard Hughes Medical Institute at Stanford’s School of Medicine.

Previous work on the decision-making process — a plan of action based on evidence, prior knowledge, and payoff — has been methodologically limited. In earlier studies, scientists analyzed one neuron at a time, then averaged these results across neurons to develop an understanding of this activity. However, such a measurement offers only snapshots of neurological behavior and misses the fine-scale dynamics that lead up to a decision.

In the Current Biology study, the researchers examined many neurons at once, giving them a more detailed understanding of decision making.

“Now we can look at the nuances of this dynamic and track changes over a specified period,” explains Kiani. “Looking at one neuron at a time is ‘noisy’: results vary from trial to trial so you cannot get a clear picture of this complex activity. By recording multiple neurons at the same time, you can take out this noise and get a more robust picture of the underlying dynamics.”

The researchers studied macaque monkeys, running them through a series of tasks while monitoring the animals’ neuronal workings.

In the experiment, the monkeys viewed a patch of randomly moving dots on a computer screen. Following the stimulus, monkeys received a “Go” signal to report the motion direction by making an eye movement. The scientists sought to predict the monkeys’ choices purely based on the recorded neural responses before the Go signal. Their model achieved highly accurate predictions.

The same model was then used to study potential dynamics of the monkeys’ decision at different times before the Go signal. The scientists confirmed these predictions by stopping the decision-making process at arbitrary times and comparing the model predictions with the monkeys’ actual choices.

Surprisingly, the monkeys’ decisions were not always stable. Occasionally, they vacillated from one choice to another, indicating covert changes of mind during decision-making. These changes of mind closely matched the properties of human changes of mind, which were uncovered in a 2009 study. They were more frequent in uncertain conditions, more likely to correct an initial mistake, and more likely to happen earlier during a decision.

The research was supported by the Howard Hughes Medical Institute, the Air Force Research Laboratory (FA9550-07-1-0537), a Berry Postdoctoral Fellowship, and a Sloan Research Fellowship.

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Thieving chimps changing the way African farmers feed their families

Light-fingered chimpanzees are changing the way subsistence farmers make a living in Africa by causing them to grow different crops and spend more time guarding their goods. This is according to work performed by researchers from Trinity College Dublin’s School of Geography, who say that communities near the edge of tropical forests are experiencing a lack of ‘dietary diversity’ and an increased exposure to disease-carrying insects as a result.

Through crop raiding, a form of human-wildlife conflict, hundreds of thousands of marginalized farmers are losing edible crops to damage from these troublesome animals each year. Farmers are reducing their cultivation of maize, beans and other staples, which are highly prized by raiding species. In addition, by guarding their existing crops during the night, farmers are increasingly exposed to malaria carried by mosquitos and soil-based worms which cause elephantiasis.

Despite the positive actions taken by affected farmers working around the Gishwati Forest fragment in western Rwanda, the shifts in farming practice are having a cumulative, negative effect on their communities. The damage might be minor on each occasion, but the losses soon add up, and an increased risk of disease is a major problem.

“Unsurprisingly, non-human primates are quite fond of the food crops we grow! The chimps are basically imposing a ‘natural tax’ on farmers growing crops near the nutrient-rich soils of the forest,” said Shane McGuinness, lead author on the research and PhD student in Geography at Trinity, who conducted the interview-based study with the help of the Great Apes Trust and local conservation workers.

Although their numbers are small in this forest, chimpanzees are an internationally protected species and have the potential to generate substantial amounts of tourism-driven revenue. Sylvain Nyandwi of the Great Apes Trust of Iowa (the organisation currently charged with conserving the forest), said that 19 chimps had been identified but there were likely to be more elusive thieves out there that had yet to be accounted for.

Actions to reduce the impact of the chimps must be carefully measured to balance the conservation of the important habitat in which they live, while protecting the lives and livelihoods of local people. Farmers changed the crops they were growing to reduce the risk of crop raiding without needing to be prompted by conservation organisations.

McGuinness added: “This is a great, positive step towards proper, community-led conservation. Using local knowledge and appropriate scientific know-how to solve these human-wildlife conflicts is imperative to implementing lasting and robust conflict mitigation.”

Work is now being finalized on a much larger project around the Volcanoes National Park in northern Rwanda, made famousby the film Gorillas in the Mist, where McGuinness is assessing the impacts of mountain gorilla, buffalo and golden monkey on the conservation of this park and the development of surrounding human communities.

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New monkey model for AIDS offers promise for medical research

HIV-1, the virus responsible for most cases of AIDS, is a very selective virus. It does not readily infect species other than its usual hosts — humans and chimpanzees. While this would qualify as good news for most mammals, for humans this fact has made the search for effective treatments and vaccines for AIDS that much more difficult; without an accurate animal model of the disease, researchers have had few options for clinical studies of the virus.

New work from Paul Bieniasz’s Laboratory of Retrovirology at The Rockefeller University and the Aaron Diamond AIDS Research Center and Theodora Hatziioannou’s laboratory, also at Aaron Diamond, may help fill this gap. In research described in Science, they announce that they have coaxed a slightly modified form of the HIV-1 virus to not only infect pigtailed macaques, a species of monkey, but to cause full blown AIDS in the primates, a first.

As part of the disease, human AIDS patients lose immune cells known as CD4+ T-cells. To develop a new animal model to study the disease, scientists induced AIDS from HIV-1 infection in otherwise resistant monkeys. Before infection (top), monkey CD4+ T-cells (brown) appear at normal levels. After 20 weeks of infection (bottom), these cells are almost completely absent.

“HIV-1 only causes AIDS in humans and chimpanzees, but the latter are not a practical model and are no longer used for HIV/AIDS research. Our goal has been to figure out how HIV-1 could cause disease in a new host,” Bieniasz says. “By accomplishing this with macaques, we have taken a step toward establishing a new model for AIDS that can be used universally in prevention and treatment research.”

Although pigtailed macaques have fewer defenses against HIV-1 than most other primates — they lack an antiviral protein that fights off the virus — the researchers still had to alter both the virus and the macaque immune system in order to induce AIDS.

They bolstered the virus with a defense-disabling protein made by Simian Immunodeficiency Virus (SIV), a relative of HIV-1. Then they encouraged the modified HIV strain to adapt to its new host by passing it from one monkey to another, resulting in six generations of infected monkeys and an adapted virus. Even so, the monkeys’ immune systems were still able to control the HIV-1 infection. So, the researchers temporarily weakened their immune systems by depleting a type of white blood cell, known as a CD8 T-cell, that destroys virus-infected cells.

“When we depleted their CD8 cells, the infected monkeys developed disease closely mirroring that of human patients. For example they contracted AIDS-defining conditions including pneumocystis pneumonia, a textbook example of an opportunistic infection in AIDS,” says Hatziioannou. “Because it replicates what happens when HIV-1 compromises a human patient’s immune system, our approach could potentially be used in the development of therapies and preventative measures for human patients.”

In fact, if fully developed, the macaque model will offer a substantial improvement for research. Often, HIV therapy and prevention research relies on SIV, a viral relative of HIV-1, since SIV can cause AIDS-like disease in nonhuman primates. However, SIV doesn’t always behave the same way HIV-1 does. “We still have one major hurdle to overcome: If we could get HIV-1 to cause AIDS without depleting the CD8 cells, we could replace models that make use of SIV for this research.”

This work and previous research in the lab has also illuminated the process by which HIV-1 and other members of the lentivirus family can colonize a new host like the macaques. It turns out that evading or fighting off the antiviral proteins produced by the new host’s cells is key.

“This new model for HIV-1 infection is the result of years spent exploring scientific questions about how the virus interacts with a host’s antiviral defenses. These kinds of basic insights will enable us to continue to improve this model,” Hatziioannou says.

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Animals conceal sickness symptoms in certain social situations

Animals have the ability to conceal their sickness in certain social situations. According to a new review, when given the opportunity to mate or in the presence of their young, sick animals will behave as though they were healthy. The research has implications for our understanding of the spread of infectious diseases.

The review’s sole author, Dr. Patricia Lopes from the Institute of Evolutionary Biology and Environmental Studies at the University of Zurich, says that animals from a number of different species will eat and drink less, reduce their activity and sleep more when they are sick in order to conserve energy for their recovery. However, this can all change depending on the social situation.

In a paper published this week in the journal Proceedings of the Royal Society B, Lopes reviewed a range of different social situations that affected the behavior of sick animals, including the presence of offspring, intruders or potential mates. Animals ranging from birds to monkeys have all been demonstrated to conceal their sickness behavior when other animals are present. For instance, Lopes’ previous research has demonstrated that sick zebra finches will behave as though they are healthy in the presence of other zebra finches, particularly when there is the opportunity to mate.

Ability to use unique opportunities

According to Lopes, “The idea is that behaving sick helps animals recover from the disease and so this should be the default way to behave when sick. However, if being sick coincides with, for example, a unique opportunity to mate, then animals may adjust their priorities and behave as though they are not sick.” Lopes goes on to suggest that such a change may have tradeoffs for an animal with limited energy to invest in recovering from illness versus mating or caring for young.

The review also considers the implications in the context of infectious disease. “Recognizing when animals are concealing their sickness is critical to how we both detect and control the spread of infectious diseases,” says Lopes. Ultimately, improving our understanding of how the social situation affects a sick animal’s behavior can improve our models of disease detection and transmission. This extends to the spread of disease in humans living in an increasingly crowded and connected world. According to the U.S. Center for Disease Control, over 60% of communicable diseases in humans originate from animals.

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Bacteria evade human immune system with a burst of mutations during initial infection

Bacteria that cause ulcers in humans undergo accelerated evolution during the initial stages of infection, allowing them to evade the immune system, according to new research by an international team of researchers including Penn State scientists. The study shows, for the first time, and in real-time, the interplay between the human immune system and invading bacteria that allows the bacteria to counter the immune response by quickly evolving. A paper describing the research is published in the 13 June 2014 issue of the journal Nature Communications.

“Our next-generation sequencing approach enabled, for the first time, the tracing of Helicobacter pylori infections in human patients,” said Stephan Schuster, professor of biochemistry and molecular biology at Penn State.

The scientists compared the genome sequence of the stomach bacterium Helicobacter pylori just prior to infection and at several time points after infection. “We were blown away by the very high mutation rate that we found during the initial phase of infection,” said Bodo Linz, research associate at Penn State and lead author of the paper. Patients infected with H. pylori, experience an initial, acute phase of infection during which symptoms are most severe and the immune response is strongest. “We found that the bacteria accumulated mutations at a rate 30 to 50 times faster during this acute phase than during the later, chronic phase of infection when an equilibrium was reached between the bacteria and the immune response,” Linz said.

Although the rate at which mutations accumulate in the genome of H. pylori during the chronic phase of infection had been determined previously, no one yet had looked at the initial, acute phase because it is so difficult to capture and sequence the bacteria at the time of initial infection.

To determine the mutation rate during this early phase, the research team took two approaches. First, the researchers isolated the bacteria from two previously-infected human volunteers and determined its genome sequence. After eradicating the bacteria from the volunteers through treatment with antibiotics, they then re-infected the now-cured patients with their own strain of H. pylori. At 20 days after infection in one case and at 44 days after infection in the other, the scientists again isolated the bacteria from the volunteers and sequenced its genome. The patients then received another antibiotic treatment to eliminate the bacteria. “By comparing the genome sequence of the bacteria before and after re-infection, we were able to determine the rate at which the bacterial genome changes during this early, acute phase of infection in a human host,” said Linz.

In a parallel experiment, the team infected a rhesus monkey with H. pylori and collected samples of the bacteria from the monkey for genome sequencing at one week, one month, two months, and six months after initial infection. In the monkey, the scientists were able to directly compare the rate of DNA changes in the bacterial genome between the acute and chronic stages. Although mutations continued to accumulate in the bacterial genome during the chronic phase, the rate of substitutions dropped considerably after the initial four-week period.

An infection with H. pylori triggers an immune response that involves the release of reactive oxygen and nitrogen molecules that are known to induce mutations in the DNA sequence and to cause chromosomes to break apart and recombine. Previous studies had shown that the H. pylori genome is forgiving of this kind of abuse. “Strains of the bacterium isolated from different human hosts vary immensely, both in DNA sequence and in gene content” Schuster said. “There are about 1,100 core genes that individual strains of H. pylori share, but another four-to-five-hundred genes vary between strains. The high mutation and recombination rates that produce this variation allow the bacteria to be exquisitely adapted to its host and to evade eradication by the host’s immune system.”

Of particular importance in the battle between the immune system and invading bacteria are the proteins that protrude through the outer cell membrane of the bacteria. Because these outer-membrane proteins are on the outside of the bacterial cell, they are visible to the human immune system and therefore are targeted by antibodies. “Antibodies are so tuned to recognize the three-dimensional structure of outer-membrane proteins that they can attach to them with lock-and-key specificity, thereby labeling the foreign bacteria cell for elimination,” said Linz. Mutations in the genes that code for outer-membrane proteins can produce changes in the protein’s structure and, if the key then no longer fits the lock, the genetic mutations allow the bacterium to evade recognition by antibodies. “The intense selective pressure on the bacteria to survive the immune response, coupled with increased mutation rates, produces the incredibly fast rate of genomic change that we discovered in this study,” Linz said. “Mutations occur randomly throughout the genome, but because they help the bacteria avoid elimination by the immune system, changes in outer-membrane proteins appear much more often than would be expected by chance in the surviving bacteria.”

This initial burst of mutations during the acute phase of infection allows the bacteria to survive the host’s immune response and to establish a chronic infection. Whether bacteria other than H. pylori undergo a similar burst of accelerated evolution immediately after infection is not yet known, but the team plans to investigate other common human pathogens in future research.

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Study: Human Ancestors Got Herpes From Chimps

Adults today are more likely to have herpes — oral or genital — than not. But where did this widespread disease come from?

To answer that question, you’ll have to go back millions of years, to a time before we were human.

New genomic analysis has found that oral herpes may have been around since before our split with chimpanzees happened about 6 million years ago. The virus then branched out and followed the evolution of hominids to become oral herpes, or herpes simplex virus 1 (HSV-1).

“The ancestor of all monkeys and apes had the herpes virus,” said study author and virologist Joel Wertheim of the University of California at San Diego. “When the host species lineage started to split, the viruses also formed new lineages.”

The virus responsible for genital herpes hit our ancestors later, likely jumping from proto-chimps to a now-extinct hominid — either Homo habilis or Homo erectus — about 1.6 million years ago. The ancient virus eventually gave rise to what is now known as herpes simplex virus 2 (HSV-2) in humans, commonly spread through sexual contact.

Because the chimpanzee herpes simplex virus found its way back into our lineage, we are the only primate species known to be infected with two distinct herpes simplex viruses. But how the transmission occurred from primate-to-hominid all those years ago remains a mystery.

“We can’t say whether the interaction that led to cross-transmission was physical aggression or sexual contact,” Wertheim said. “We just don’t know, but both are possible.”

Alternate means could have been through hominids hunting and eating the meat of proto-chimps or living with them in close quarters, said virologist Alberto Severini of the University of Manitoba, who was not involved in the research.

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Human language’s deep origins appear to have come directly from birds, primates

On the island of Java, in Indonesia, the silvery gibbon, an endangered primate, lives in the rainforests. In a behavior that’s unusual for a primate, the silvery gibbon sings: It can vocalize long, complicated songs, using 14 different note types, that signal territory and send messages to potential mates and family.

Far from being a mere curiosity, the silvery gibbon may hold clues to the development of language in humans. In a newly published paper, two MIT professors assert that by re-examining contemporary human language, we can see indications of how human communication could have evolved from the systems underlying the older communication modes of birds and other primates.

From birds, the researchers say, we derived the melodic part of our language, and from other primates, the pragmatic, content-carrying parts of speech. Sometime within the last 100,000 years, those capacities fused into roughly the form of human language that we know today.

But how? Other animals, it appears, have finite sets of things they can express; human language is unique in allowing for an infinite set of new meanings. What allowed unbounded human language to evolve from bounded language systems?

“How did human language arise? It’s far enough in the past that we can’t just go back and figure it out directly,” says linguist Shigeru Miyagawa, the Kochi-Manjiro Professor of Japanese Language and Culture at MIT. “The best we can do is come up with a theory that is broadly compatible with what we know about human language and other similar systems in nature.”

Specifically, Miyagawa and his co-authors think that some apparently infinite qualities of modern human language, when reanalyzed, actually display the finite qualities of languages of other animals — meaning that human communication is more similar to that of other animals than we generally realized.

“Yes, human language is unique, but if you take it apart in the right way, the two parts we identify are in fact of a finite state,” Miyagawa says. “Those two components have antecedents in the animal world. According to our hypothesis, they came together uniquely in human language.”

Introducing the ‘integration hypothesis’

The current paper, “The Integration Hypothesis of Human Language Evolution and the Nature of Contemporary Languages,” is published this week in Frontiers in Psychology. The authors are Miyagawa; Robert Berwick, a professor of computational linguistics and computer science and engineering in MIT’s Laboratory for Information and Decision Systems; and Shiro Ojima and Kazuo Okanoya, scholars at the University of Tokyo.

The paper’s conclusions build on past work by Miyagawa, which holds that human language consists of two distinct layers: the expressive layer, which relates to the mutable structure of sentences, and the lexical layer, where the core content of a sentence resides. That idea, in turn, is based on previous work by linguistics scholars including Noam Chomsky, Kenneth Hale, and Samuel Jay Keyser.

The expressive layer and lexical layer have antecedents, the researchers believe, in the languages of birds and other mammals, respectively. For instance, in another paper published last year, Miyagawa, Berwick, and Okanoya presented a broader case for the connection between the expressive layer of human language and birdsong, including similarities in melody and range of beat patterns.

Birds, however, have a limited number of melodies they can sing or recombine, and nonhuman primates have a limited number of sounds they make with particular meanings. That would seem to present a challenge to the idea that human language could have derived from those modes of communication, given the seemingly infinite expression possibilities of humans.

But the researchers think certain parts of human language actually reveal finite-state operations that may be linked to our ancestral past. Consider a linguistic phenomenon known as “discontiguous word formation,” which involve sequences formed using the prefix “anti,” such as “antimissile missile,” or “anti-antimissile missile missile,” and so on. Some linguists have argued that this kind of construction reveals the infinite nature of human language, since the term “antimissile” can continually be embedded in the middle of the phrase.

However, as the researchers state in the new paper, “This is not the correct analysis.” The word “antimissile” is actually a modifier, meaning that as the phrase grows larger, “each successive expansion forms via strict adjacency.” That means the construction consists of discrete units of language. In this case and others, Miyagawa says, humans use “finite-state” components to build out their communications.

The complexity of such language formations, Berwick observes, “doesn’t occur in birdsong, and doesn’t occur anywhere else, as far as we can tell, in the rest of the animal kingdom.” Indeed, he adds, “As we find more evidence that other animals don’t seem to posses this kind of system, it bolsters our case for saying these two elements were brought together in humans.”

An inherent capacity

To be sure, the researchers acknowledge, their hypothesis is a work in progress. After all, Charles Darwin and others have explored the connection between birdsong and human language. Now, Miyagawa says, the researchers think that “the relationship is between birdsong and the expression system,” with the lexical component of language having come from primates. Indeed, as the paper notes, the most recent common ancestor between birds and humans appears to have existed about 300 million years ago, so there would almost have to be an indirect connection via older primates — even possibly the silvery gibbon.

As Berwick notes, researchers are still exploring how these two modes could have merged in humans, but the general concept of new functions developing from existing building blocks is a familiar one in evolution.

“You have these two pieces,” Berwick says. “You put them together and something novel emerges. We can’t go back with a time machine and see what happened, but we think that’s the basic story we’re seeing with language.”

Miyagawa acknowledges that research and discussion in the field will continue, but says he hopes colleagues will engage with the integration hypothesis.

“It’s worthy of being considered, and then potentially challenged,” Miyagawa says.

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Herpes infected humans before they were human

Researchers at the University of California, San Diego School of Medicine have identified the evolutionary origins of human herpes simplex virus (HSV) -1 and -2, reporting that the former infected hominids before their evolutionary split from chimpanzees 6 million years ago while the latter jumped from ancient chimpanzees to ancestors of modern humans — Homo erectus — approximately 1.6 million years ago.

The findings are published in the June 10 online issue of Molecular Biology and Evolution.

“The results help us to better understand how these viruses evolved and found their way into humans,” said Joel O. Wertheim, PhD, assistant research scientist at the UC San Diego AntiViral Research Center and lead author of the study. “Animal disease reservoirs are extremely important for global public health. Understanding where our viruses come from will help guide us in preventing future viruses from making the jump into humans.”

Approximately two-thirds of the human population is infected with at least one herpes simplex virus. The viruses are most commonly presented as cold sores on the mouth or lips or blisters on the genitals.

“Humans are the only primates we know of that have two herpes simplex viruses,” said Wertheim. “We wanted to determine why.”

The researchers compared the HSV-1 and HSV-2 gene sequences to the family tree of simplex viruses from eight monkey and ape host species. Using advanced models of molecular evolution, the scientists were able to more accurately estimate ancient viral divergence times. This approach allowed them to determine when HSV-1 and HSV-2 were introduced into humans with far more precision than standard models that do not account for natural selection over the course of viral evolution.

The genetics of human and primate herpes viruses were examined to assess their similarity. It became clear that HSV-1 has been present in humans far longer than HSV-2, prompting the researchers to further investigate the origins of HSV-2 in humans.

The viral family tree showed that HSV-2 was far more genetically similar to the herpes virus found in chimpanzees. This level of divergence indicated that humans must have acquired HSV-2 from an ancestor of modern chimpanzees about 1.6 million years ago, prior to the rise of modern humans roughly 200,000 years ago.

“Comparing virus gene sequences gives us insight into viral pathogens that have been infecting us since before we were humans,” said Wertheim.

Co-authors include Martin D. Smith and Sergei L. Kosakovsky Pond, UC San Diego; Davey M. Smith, UC San Diego and Veterans Affairs San Diego Healthcare System; Konrad Scheffler, UC San Diego and Stellenbosch University, South Africa.

Funding for this research came from the University of California Laboratory Fees Research Program (grant 12-LR-236617), the National Institutes of Health (grants DA034978 and GM093939), the Bioinformatics and Information Technologies Core of the UC San Diego Center for AIDS Research (P30 AI036214), and the Department of Veterans Affairs.

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Chimps Outsmart Humans At Simple Strategy Game

Researchers at the California Institute of Technology have found that chimpanzees at the Kyoto University Primate Research Institute are consistently better at humans when playing simple competitive games.

In one game, called the Inspection Game, chimps and humans played a variation on hide-and-seek. In pairs of their own species (humans and chimps did not directly compete with each other for the study), the players sit back-to-back, each with a computer screen in front of them. After pushing a circle on the screen, they have to choose one of two boxes, right or left. They are then shown their opponent’s selection.

Each player has a different role. The “mismatchers” have to choose the opposite of their opponent’s selection, while the “matchers” have to choose the same as their opponent’s selection. Each game lasted 200 rounds, and players that “won” a round were given a reward. In order to consistently win, players had to be able to anticipate their opponent’s choices.

In game theory, there is a concept known as the Nash equilibrium. This means the balance that can be achieved when each player knows their opponent’s strategies, but has nothing to gain by changing their own strategy. The 16 Japanese students participating in the study performed as expected: slow to learn their opponents’ strategies, and not reaching the Nash equilibrium.

The six chimpanzees, however, learned the game and their opponents’ moves rapidly, very nearly reaching the Nash equilibrium, even when the researchers swapped the chimps’ roles and introduced higher rewards for specific choices. As the game changed, the chimps changed their strategies accordingly.

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‘Healthy’ component of red wine, resveratrol, causes pancreatic abnormalities in fetuses

Here’s more evidence that pregnant women should be careful about what they eat and drink: A new research report appearing in the June 2014 issue of The FASEB Journal shows that when taken during pregnancy, resveratrol supplements led to developmental abnormalities in the fetal pancreas. This study has direct relevance to human health–Resveratrol is widely used for its recognized health benefits, and is readily available over the counter.

“The important message in this study is that women should be very careful about what they consume while pregnant, and they should not take supplements, like Resveratrol, without consulting with their doctors,” said Kevin L. Grove, Ph.D., a researcher involved in the work from the Division of Diabetes, Obesity and Metabolism and the Division of Reproductive and Development Science at Oregon Health and Science University in Portland, Oregon. “What might be good for the mother may not be good for the baby.”

To make this discovery, Grove and colleagues administered Resveratrol supplements every day throughout pregnancy to obese female macaque monkeys consuming a Western diet. A second group of obese monkeys were not given the supplement, and all comparisons were made against lean monkeys fed a healthy low fat diet. The animals were closely monitored for health complications and blood flow through the placenta was determined by ultra sound. The fetuses were analyzed for developmental abnormalities, and findings showed definitive evidence of pancreatic abnormalities.

“We’ve known for a long time that resveratrol is pharmacologically active, and we’re just now really beginning to understand the pros and cons of consuming high concentrations of this substance,” said Gerald Weissmann, M.D., Editor-in-Chief of The FASEB Journal. “As we begin to establish a safety profile for resveratrol and other dietary supplements, findings like this should come as no surprise. There are always negative side effects when you eat, drink, take or do too much of anything.”

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Auditing Ape School

Genome sequences show how lemurs fight infection

The young lemur named Eugenius started to get sick. Very sick. He was lethargic, losing weight and suffering from diarrhea. Duke Lemur Center veterinarians soon pinpointed the cause of his illness: Eugenius tested positive for Cryptosporidium, a microscopic intestinal parasite known to affect people, pets, livestock and wildlife worldwide.

In humans, thousands of cases of Cryptosporidium are reported in the United States each year, spread primarily through contaminated water.

Since Eugenius was the first animal diagnosed in 1999, the parasite has caused periodic diarrhea outbreaks at the Duke Lemur Center. All of the infected animals are sifakas — the only lemur species out of 17 at the center known to fall prey to the parasite — and most of them were under age five when they got sick.

Despite various efforts to stop the infection, such as quarantining infected lemurs and decontaminating their enclosures, more than half of the sifakas living at the center have tested positive for crypto at some point. While most animals recover, the pattern has veterinarians puzzled over why the outbreaks persist.

Now, thanks to advances in next-generation sequencing technology, researchers are getting closer to understanding how these endangered animals fight the infection and detecting the illness early enough to minimize its spread.

In a study published in the May 29, 2014, edition of Molecular Ecology Resources, Duke researchers Peter Larsen, Ryan Campbell and Anne Yoder used high-throughput sequencing on sifaka blood samples to generate sequence data for more than 150,000 different sifaka antibodies — protective molecules that latch on to bacteria, viruses and other foreign invaders in the body and fight them off before they cause infection.

Traditional sequencing methods can capture only a fraction of the millions of antibodies circulating in the bloodstream at a given time. But faster next-generation sequencing technology lets researchers sequence a much larger portion of the antibody arsenal. The end result is a high-resolution ‘snapshot’ of antibody diversity that could shed light on how the immune system responds to stress and infection.

The research is part of a growing field called ecoimmunology, which aims to push the study of immunology beyond lab animals like fruit flies and mice and understand how immune systems function in real-world settings outside the lab.

The next step will be to compare blood samples from healthy and sick lemurs, to see if researchers can identify the specific antibodies that play a role in binding to Cryptosporidium and neutralizing the infection — information that could be key to developing vaccines.

This research will likely lead to new methods of disease detection and treatment for lemurs in captivity, especially infected animals that show no outward signs of being sick. But it also may lead to monitoring the health status of lemurs and other primates living in the wild simply by screening blood samples for antibody patterns indicating exposure to specific parasites.

That’s good news for lemurs in their native home of Madagascar, where lemurs live on the brink of extinction, and where human population growth makes contact with people and inter-species exchange of infectious disease increasingly likely.

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Skin grafts from genetically modified pigs may offer alternative for burn treatment

A specially-bred strain of miniature swine lacking the molecule responsible for the rapid rejection of pig-to-primate organ transplants may provide a new source of skin grafts to treat seriously burned patients. A team of investigators from Massachusetts General Hospital (MGH) report that skin grafts from pigs lacking the Gal sugar molecule were as effective in covering burn-like injuries on the backs of baboons as skin taken from other baboons, a finding that could double the length of time burns can be protected while healing. The report in the journal Transplantation has been published online.

“This exciting work suggests that these GalT-knockout porcine skin grafts would be a useful addition to the burn-management armamentarium,” says Curtis Cetrulo, MD, of the MGH Transplantation Biology Research Center (TBRC) and the Division of Plastic and Reconstructive Surgery, corresponding author of the Transplantation paper. “We are actively exploring options for establishing clinical-grade production of these grafts and hope to begin a clinical trial in due course.”

A key component in the treatment of major burns, particularly those involving more than 30 percent of the body surface, is removing the damaged skin and covering the injury, preferably with a graft of a patient’s own tissue. When insufficient undamaged skin is available for grafting, tissue from deceased donors is used as a temporary covering. But deceased-donor skin grafts are in short supply and expensive — disadvantages also applying to artificial skin grafts — must be carefully tested for pathogens and are eventually rejected by a patient’s immune system. Once a deceased-donor graft has been rejected, a patient’s immune system will reject any subsequent deceased-donor grafts almost immediately.

The current study was designed to investigate whether a resource already available at the MGH might help expand options for protecting burned areas following removal of damaged skin. For more than 30 years David H. Sachs, MD, founder and scientific director of the TBRC, has been investigating ways to allow the human body to accept organ and tissue transplants from animals. Sachs and his team developed a strain of inbred miniature swine with organs that are close in size to those of adult humans. Since pig organs implanted into primates are rapidly rejected due to the presence of the Gal (alpha-1,3-galactose) molecule, Sachs and his collaborators used the strain that he developed to generate miniature swine in which both copies of the gene encoding GalT (galactosyltransferase), the enzyme responsible for placing the Gal molecule on the cell surface, were knocked out.

When Cetrulo’s team used skin from these Gal-free pigs to provide grafts covering burn-like injuries on the backs of baboons — injuries made while the animals were under anesthesia — the grafts adhered and developed a vascular system within 4 days of implantation. Signs of rejection began to appear on day 10, and rejection was complete by day 12 — a time frame similar to what is seen with deceased-donor grafts and identical to that observed when the team used skin grafts from other baboons. As with the use of second deceased-donor grafts to treat burned patients, a second pig-to-baboon graft was rapidly rejected. But if a pit-to baboon was followed by a graft using baboon skin, the second graft adhered to the wound and remained in place for around 12 days before rejection. The researchers also showed that acceptance of a second graft was similar no matter whether a pig xenograft or a baboon skin graft was used first.

“These results raise the possibility not only of providing an alternative to deceased-donor skin for many patients but also that, in patients whose burns are particularly extensive and require prolonged coverage, sequential use of GalT-knockout and deceased-donor skin could provide extended, high-quality wound coverage,” says co-author David Leonard, MBChB, of the TBRC and Division of Plastic and Reconstructive Surgery. “A high-quality alternative to deceased-donor skin that could be produced from a specially maintained, pathogen-free herd of GalT-knockout miniature swine would be an important resource for burn management in both civilian and military settings.”

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Researchers Control Monkey’s Choice by Activating a Brain Region

According to researchers from Massachusetts General Hospital (MGH), activating a particular region of the brain affects the decision-making progress. The team was able to change monkeys’ choices between two images by artificially stimulating the ventral tegmental area (VTA), which consists of a group of neurons located at the base of the midbrain.

“Previous studies had correlated increased activity in the primate VTA with positive events experienced by the animal but could not prove that VTA activity actually caused behavioral changes,” stated study author, Wim Vanduffel, PhD, of the Martinos Center for Biomedical Imaging at MGH and head of the Laboratory for Neuro- and Psychophysiology at the University of Leuven. “Studies in rodents have shown that artificially manipulating VTA activity strongly influences behavior, and our work has bridged the gap between rodent and primate.”

In this study, the team placed microelectrodes in the VTAs of macaque monkeys using high-resolution magnetic resonance imaging as a guide. In the beginning of the experiment, the monkeys were showed two images. The researchers recorded which image the monkeys preferred by observing their eye movements. The monkeys had been trained to look initially at a white square and then at either picture. The picture that the monkeys looked at most frequently was considered the favored one.

After knowing which image the monkeys preferred, the researchers showed the monkeys the picture pairs once again. This time when the monkeys looked at the less favored picture, the team administered mild stimulation to the VTA. The researchers noted that the stimulation caused the monkeys to change their preference. The stimulation was then applied when the monkeys glanced at their preferred image. The monkeys’ preference changed back to normal.

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