The ability to conjure up possible futures or alternative realities is the flip side of memory.

Both faculties
cohabit in the brain region called the hippocampus

Henry Molaison, known for years as “H.M.,” was famously unable to form new memories. If
someone he had met left the room only to return several minutes later, he would greet that
person again as if for the first time. Because of surgery to treat intractable epilepsy, H M.
lacked a sea-horse-shaped brain structure called the hippocampus and had amnesia. His case
helped establish the hippocampus as an engine of memory.

In recent years scientists have discovered another essential deficit that burdens people with
hippocampal amnesia: they can’t envision the range of possibilities that must be considered
to make future plans. When researchers asked a group of people with hippocampal damage to
describe themselves in a fictitious scene—say, lying on a white sandy beach—they came up
largely blank, producing only fragmented images. Brain scans of healthy people, by contrast,
showed that their hippocampus was engaged even more when they imagined the future than
when they summoned the past.

Studies of neural activity in rats have since come along to support the idea that the
hippocampus plays a central role in imagination. “It’s still responsible for creating memories
of what is happening right now,” says Loren Frank, a systems neuroscientist at the Howard
Hughes Medical Institute and the University of California, San Francisco. “And now it seems
it is also responsible for rolling out possibilities.” Frank and his colleagues make their case in
a paper entitled “Imagination as a Fundamental Function of the Hippocampus,” which was
published in the Philosophical Transactions of the Royal Society B.

That dual role makes sense, experts say, in part because imagination depends largely, if not
exclusively, on memory. “Why do we talk about imagination separately from memory? From
the public point of view [talking about them together] is a crazy idea. But you can put it in a
simple way: there is absolutely no way you can imagine anything without the past,” says
György Buzsáki, a systems neuroscientist at New York University, who was not involved with
the paper.

In addition, both skills involve essentially the same process: combining bits and pieces of
experience with emotions, inner commentary and things people have read or heard about,
says Donna Rose Addis, a cognitive neuroscientist at the Rotman Research Institute in
Toronto and the University of Toronto, who was also not involved with the recent review.
This process can even distort memories by mixing them with imaginary material. “Memory is
a form of imagination,” Addis says.

From Frank’s point of view, imagination gives memory a purpose: helping us make decisions
based on what we’ve learned—for instance, deciding to avoid a food that once made us sick.
“From an evolutionary perspective, we are reasonably sure that the purpose of memories is
actually in the future,” Frank says. “Memories allow you to take experiences that you have
and retrieve them to make predictions about what will happen next.” This chain of neural
events even loops back on itself. We also need to form memories of our simulations of the
future so that when we have an experience, we have something to draw on. “We have found
that the encoding of an imagined simulation also involves the hippocampus,” Addis says.
Much of the recent evidence for imagination’s roots in the brain draws on a Nobel Prize–
winning discovery in the 1970s of “place cells” in the hippocampus. When a rat runs a maze,
the activity of these cells changes in a predictable way based on the animal’s position in the
maze. These hippocampal cells tell an animal where it is in the world. This function seemed
distinct from imagination until Frank and his colleagues showed that the activity of these
cells does not always represent an animal’s actual location.

The firing patterns of place cells repeat about eight times per second in rats, forming what is
called the theta rhythm. And within each cycle, the researchers found, the patterns
progressively change to represent three different locations for the animal that are separated
in time: the place it just was, its current position and, late in the cycle, a possible upcoming
location. “The neural activity has this unmistakable structure where, at certain time points, it
looks like what the animal is experiencing in the present. At these other time points, it looks
like an imaginary experience,” says Kenneth Kay, a postdoctoral researcher at the Mortimer
B. Zuckerman Mind Brain Behavior Institute at Columbia University and a co-author of the
paper. (The paper’s first author is Frank’s graduate student, Alison Comrie.)

What a rat seems to be imagining in any given cycle varies. When the rat is approaching a
T-junction in a maze, the late theta activity alternates between two possible immediate
futures: a turn to the left in one cycle and a turn to the right in the next. It’s as if the animal is
planning its next move, akin to a soccer player who is running toward a ball and flipping
through various scenarios before deciding on a play.

In other instances, that late theta activity denotes a more distant place in the maze, as if the
animals’ mind wandered to some other scene or scenario, perhaps some place it would rather
be. The researchers also found instances in which this imagination portion of the cycle
reflected a hypothetical direction of travel that differed from the animal’s actual directional
heading. “They are representing things that can roughly be thought of as possibilities or
hypotheticals, things that could be but aren’t necessarily the case in terms of a possible future
or just an alternative reality,” Frank says.

The mere existence of spontaneous activity within the hippocampus that is not necessarily
tied to a specific place, some experts say, hints at an internal thought process that is
separated from reality. “That rhythmicity [of the theta wave] is not coming from the
environment,” Kay says. “That’s highly reminiscent of the notion that our imaginings are
coming from ourselves, and they are not from this external reality.”

Another form of imagination seems to occur when an animal isn’t traveling through space but
is eating, grooming or zoning out. At these times, scientists have detected bursts of activity in
the hippocampus called “sharp wave ripples,” which also occur during sleep, that seem to
represent mental replays of past events. The replays occur about 10 times faster than the
original event, a reenactment that is reminiscent of human experience. “One huge advantage
of using our minds to think about things sometimes is: we can quickly play through things,
we can quickly simulate them,” Kay says.

While these mental replays are a form of recollection, they can also represent events the
animal has not experienced, Frank says. Some sharp wave ripples appear to connect two
trajectories that an animal had experienced separately but not together, he says. The ripple
activity may, in essence, build a mental map so that the animal can mentally traverse new
paths, such as shortcuts and detours. In this context, the hippocampus seems to be acting to
combine past events in new ways, something that “is more like imagination than it is just
replaying the past or predicting the future,” says Lynn Nadel, an emeritus professor of
cognitive science and psychology at the University of Arizona, who did not contribute to the
recent paper.

The experiments of neuronal activity in rodents are important, experts say, because they
place the idea of imagination into a physical reality: that of the brain itself. “This gives us an
opportunity to take a fuzzy cognitive concept like imagination” and link it to brain activity,
says Daphna Shohamy, a cognitive neuroscientist at Columbia University, and director and
CEO of Columbia's Zuckerman Institute, who was not involved in those studies or the review
paper.

Humans’ internal worlds are rich, however, and the studies of place cells in rats may not
represent all types of human imagination. The animal results connect most directly with
imagination that is based in experience and action, as in planning out a strategy for moving
through the world, Nadel says. But other experts believe the hippocampus has a much
broader repertoire: it may also forge ties between ideas and information. “I don’t think the
hippocampus cares, really, about what you’re connecting,” Addis says.

Some of Shohamy’s work supports the idea that the hippocampus might be important for
mental simulations that are not rooted in time or place. She has found that people with
damage to the hippocampus are much slower than those without brain damage to choose
between food items—say, a Kit Kat versus M&Ms—that they like about equally well. The
problem seems to be that they have trouble imagining what the options are like. “It looks as if
they are spending more time trying to conjure up the evidence,” Shohamy says. In the end,
they make a choice at random.

Although the hippocampus may play a central role in imagination, it is by no means

performing a solo act. It needs the cooperation of other brain areas. Frank likens the
hippocampus to an orchestra conductor that cues up neurons in other regions that represent
the sights, sounds and smells that either are part of a recollection or “fit together in some
imagined thing.”
One mystery is how people separate a real symphony from music playing in their head. “It’s
amazing that we’re not all psychotic all the time, that we’re not all delusional, because our
brains are clearly making stuff up a lot of the time about things that could be,” Frank says.
New data from Frank’s group suggest the brain may use sensory input—say, the feeling of a
foot hitting the ground while walking—to flag what is real versus what is just in the mind’s
eye and so ground this hive of neural activity in the physical world. The brain, he says,
separates fact from fiction by reconciling the information it receives from the outside world
with its own internal models.

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