Editor | On 14, Nov 2018

Darrell Mann

Every September arctic ground squirrels in Alaska, Canada and Siberia retreat into burrows more than a meter beneath the tundra, curl up in nests built from grass, lichen and caribou hair, and begin to hibernate. As their lungs and hearts slow, the rivers of blood flowing through their bodies dwindle and their core body temperatures plummet, dipping below the freezing point of water. Electrical signals zipping along crisscrossing neural highways vanish in many areas of the brain. Seven months later the squirrels wake up and return to the surface—famished, eager to mate and perfectly healthy.

How hibernating mammals survive for so long at such low temperatures without any food or water beyond what they have stored in their own fat fascinates scientists for many reasons. Hibernation is an amazing biological feat and an opportunity to learn new ways of pushing the human body beyond its ostensible limits, as well as healing it when it breaks down. The arctic ground squirrel’s brain, in particular, seems to be incredibly resilient. When ground squirrels hibernate their neurons shrink and many connections between neurons shrivel. But their brains periodically compensate for this loss with massive growth spurts, multiplying neural links beyond what existed before hibernation. Learning how the ground squirrel’s brain recuperates could not only help scientists understand the brain’s plasticity, but also suggest new ways to reverse or prevent cellular damage in neuro-degenerative diseases. In particular, recent research on hibernating brains is changing the way some scientists think about misshapen tau proteins, which are a hallmark of Alzheimer’s disease.

Brain freeze

Most small hibernating mammals—hamsters, hedgehogs, bats—turn down their body’s thermostat during hibernation, relinquishing one of the defining features of all mammals: warm blood. Arctic ground squirrels are the most extreme example. In August 1987 Brian Barnes of the University of Alaska Fairbanks (U.A.F.) captured 12 arctic ground squirrels and implanted tiny temperature-sensitive radio transmitters in the animals’ abdomens. He transported the squirrels to outdoor enclosures in Fairbanks—wire cages with borders reaching more than 1.2 meters belowground. By September the ground squirrels had dug burrows within the enclosures and begun to hibernate. Their body temperatures dropped to –2.9 degrees Celsius, almost three degrees below the freezing point of freshwater and probably the lowest core body temperature ever recorded in a living mammal. Despite this, ground squirrel blood remains liquid, most likely through a phenomenon known as supercooling.

In laboratory experiments, Barnes also measured the temperature of various body parts as the squirrels hibernated in a chamber kept at –4.3 degrees C. Although their colons, feet and bellies dropped below zero C, their necks never grew colder than 0.7 degree C, suggesting that the brain remains a little warmer than the rest of the body. Most mammals would die within hours if their brains were cooled so low, yet ground squirrel brains survived near freezing temperatures for weeks at a time. Every two to three weeks the squirrels shivered themselves back to their typical body temperature of 36.4 degrees C, which they maintained for 12 to 15 hours before becoming frozen pop-squirrels once more. Later, scientists would confirm that these intermittent periods of arousal are crucial to the ground squirrels’ survival—without them their brains would wither long before spring’s arrival.

Doom and bloom

Hibernation devastates the ground squirrel brain, wilting thousands if not millions of vital connections between brain cells, known as synapses. But its brain has evolved impressive resilience, repeatedly renewing itself at astonishing speeds, like a forest erupting through the scorched earth in a matter of days. Victor Popov of the Institute of Cell Biophysics in Russia discovered some of the earliest evidence of this plasticity. In the early 1990s Popov and his colleagues captured wild Siberian ground squirrels and kept them in temperature-controlled enclosures as they hibernated. The researchers sacrificed different animals at three distinct stages—during hibernation; two hours after one of the intermittent arousal periods; or one day after emerging from hibernation—and removed their brains to stain and examine the neurons within the hippocampus, an area crucial for memory. Neurons from squirrels that were in the middle of hibernation were shrunken and had far fewer dendrites—branches that receive signals from other neurons—compared with brain cells from fully awake and aroused squirrels. The dendrites in hibernating brains also had fewer dendritic spines, which jut out from the main branch like thorns on a rose stem and increase the number of possible synapses with nearby cells.

Whereas neurons in hibernating brains looked like barren tree limbs in the dead of winter, brain cells from squirrels that had just emerged from hibernation into a period of arousal sported dense crowns of overlapping dendrites. In only two hours the squirrels’ brains had not only compensated for all the synapses lost during hibernation—their brain cells now boasted many more links than those of an active squirrel in the spring or summertime. One day later, however, their brains had pruned many of these ties, probably recognizing them as superfluous, much the way the developing mammalian brain shears its blooming neural forest.

Since Popov’s study other researchers have observed similar loss and recovery of synapses in the brains of hibernating hamsters and hedgehogs. In a 2006 study Craig Heller of Stanford University discovered that the hibernating brain is incredibly plastic overall, not just in the hippocampus. Heller thinks that squirrels and similar hibernators lose dendrites during hibernation because their metabolism is too slow and their brains too cold and idle to keep those living wires in working condition.

Perhaps it’s more efficient to let them shrivel, like a houseplant withering from neglect, and quickly nurse them back to life during those intermittent bouts of arousal. That way the mammals save as much energy as possible yet still preserve vital neural connections. Even so, researchers have estimated that many small hibernating mammals devote between 80 and 90 percent of all energy used during hibernation to keeping their brains alive.

Here’s what the ground squirrel’s brain re-building feat looks like as a conflict resolution strategy:

Principle 34, Discarding & Recovering – or should that be ‘doom and bloom’? – looks like as good a match as we’ll ever get between problem and solution. If only life always worked out that way.