Representational Drift In The Brain

Ever fascinating Ed Young on how little we know about the jelly inside our skulls: 

But other scientists have shown that the same phenomenon, called representational drift, occurs in a variety of brain regions besides the piriform cortex. Its existence is clear; everything else is a mystery. Schoonover and Fink told me that they don’t know why it happens, what it means, how the brain copes, or how much of the brain behaves in this way. How can animals possibly make any lasting sense of the world if their neural responses to that world are constantly in flux? If such flux is common, “there must be mechanisms in the brain that are undiscovered and even unimagined that allow it to keep up,” Schoonover said. “Scientists are meant to know what’s going on, but in this particular case, we are deeply confused. We expect it to take many years to iron out.”

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The team showed that if a neuron in the piriform cortex reacts to a specific smell, the odds that it will still do so after a month are just one in 15. At any one time, the same number of neurons fires in response to each odor, but the identity of those neurons changes. Daily sniffs can slow the speed of that drift, but they don’t eliminate it. Nor, bizarrely, does learning: If the mice associated a smell with a mild electric shock, the neurons representing that scent would still completely change even though the mice continued to avoid it. “The prevailing notion in the field has been that neuronal responses in sensory areas are stable over time,” says Yaniv Ziv, a neurobiologist at the Weizmann Institute of Science who was not involved in the new study. “This shows that’s not the case.”

“There have been hints of this for at least 15 years,” across many parts of the brain, Schoonover told me. The hippocampus, for example, helps animals navigate their surroundings. It contains place cells — neurons that selectively fire when their owner enters specific locations. Walk from your bed to your front door, and different place cells will fire. But these preferences aren’t fixed: Ziv and others have now shown that the locations to which these cells are tuned can also drift over time.

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It might be less common in other sensory hubs, such as the visual cortex, which processes information from the eyes. The neurons that respond to the smell of grass might change from month to month, but the ones that respond to the sight of grass seem to mostly stay the same. That might be because the visual cortex is highly organized. Adjacent groups of neurons tend to represent adjacent parts of the visual space in front of us, and this orderly mapping could constrain neural responses from drifting too far. But that might be true only for simple visual stimuli, such as lines or bars. Even in the visual cortex, Ziv found evidence of representational drift when mice watched the same movies over many days.

“We have a hunch that this should be the rule rather than the exception,” Schoonover said. “The onus now becomes finding the places where it doesn’t happen.” And in places where it does happen, “it’s the three F’s,” Fink added. “How fast does it go? How far does it get? And … how bad is it?”

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Schoonover and Fink compare the discovery of representational drift with the work of the astronomer Vera Rubin. In the 1970s, Rubin and her colleague Kent Ford noticed that some galaxies were spinning in unexpected ways that seemed to violate Newton’s laws of motion. Her analysis of that data provided the first direct evidence for dark matter, which makes up most of the matter in the universe, but has never been observed. Similarly, drift indicates “that there’s something else going on under the hood, and we don’t know what that is yet,” Schoonover said.

But the comparison between drift and Rubin’s spinning galaxies fails in one important way. Rubin knew that she was onto something odd because she could compare her data against Newtonian mechanics — a solid and thoroughly described theory of physics. No such theory exists in neuroscience. The field has a very clear idea of how individual neurons work, but it gets much fuzzier when it comes to neuronal networks, entire brains, or the behavior of whole animals.

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“There’s a real hunger in the field for new ideas,” Fink told me, which is why, he thinks, he and Schoonover haven’t yet faced the kind of vicious pushback that scientists with dogma-busting data tend to encounter. “People are really desperate for theories. The field is so immature conceptually that we’re still at the point of collecting factlets, and we’re not really in a position to rule anything out.” Neuroscience’s own representations of the brain still have plenty of room to drift.