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Stanford Report, March 29, 2000

Lowly squid's behavior may yield clues to human brain

BY MARK SHWARTZ

Squid.

The only time most of us think about this strange-looking sea creature is when it is served grilled, fried or basted in its own ink.

But the lowly squid is actually an intelligent invertebrate capable of learning complex behavior at a very young age.

A new study reveals that newborn squid actually learn through the process of trial and error, much like humans do, and that these early-life experiences can physically change a squid's nervous system in ways that may be permanent.


Photo: Hopkins researchers study the species Loligo opalescens, a common squid found in the Pacific Ocean off California. Adult squid like the one shown here are usually four to seven inches long. Courtesy: William Gilly.


These results also could provide new insight into how learning transforms the human brain, says William F. Gilly, a professor of cell and developmental biology at Stanford's Hopkins Marine Station.

Gilly and former postdoctoral fellow Thomas Preuss describe their latest findings on squid behavior in the January issue of The Journal of Experimental Biology.

"The squid is a mollusk -- an animal closely related to a clam," says Gilly, "but it has an amazingly rich behavioral repertoire. Its brain is probably as complicated as that of some mammals."

He points out that the squid is an ideal species for conducting neurological research, because its elaborate brain is connected to a set of giant axons -- the largest nerve cells in the animal kingdom (see illustration below).


When a newborn squid is frightened, its brain sends an electrical signal through the giant axons, causing the mantle muscles to automatically contract and discharge a jet of water. To gain voluntary control of its jet propulsion, the adult brain fires the small axon network first, bypassing the giant axons. Courtesy: William Gilly.


A giant axon can grow to be a millimeter wide, and its large size makes it much easier to measure electrical signals to and from the brain while the squid is carrying out various behaviors.

Startle-escape response

It is a well-known fact, write Gilly and Preuss, that a startled squid will release a powerful jet of water that propels its body forward or backward so it can escape predators.

This "startle-escape response" is similar to a reflex action and is triggered by the network of giant axons that connects the squid's brain to the muscles in its mantle -- the part of the body many of us like to eat.

When a squid is frightened, its brain sends an electrical signal through the giant axons in less than a tenth of a second -- an "all-or-nothing" impulse that causes the mantle muscles to involuntarily contract and discharge a jet of water.

Every squid is born with this startle-escape reflex, but to be successful in the wild, an animal must be able to voluntarily control and operate its jet propulsion system. That means preventing the giant axon network from automatically firing an all-or-nothing impulse.

And that's just what young squid start doing as soon as they are hatched.

According to Gilly and Preuss, the brain of a newborn squid quickly develops the ability to bypass the giant axons in favor of a parallel nerve network made up of small axons --- narrower neurons that control a different set of muscles in the mantle.

By the time it becomes an adult, a squid is able to regulate the force of its escape jet by simply activating the small axons first, then firing the giant axon network a fraction of a second later.

But is this ability to suppress the giant axon network genetically programmed in every squid, or is it a skill that each animal has to learn through experience?

To answer that question, Gilly and Preuss decided to focus on another important squid behavior that does depend on learning: the ability to hunt and capture prey.

Wild squid love to eat tiny crustaceans called copepods. But copepods are difficult to catch because they can detect and outswim a pursuing squid -- plus, copepods are covered with sharp, lobster-like spines (see drawing below).

Courtesy: William Gilly.

Through the process of trial-and-error, a young squid learns that the best way to capture a copepod is not to chase it but to remain still, spread its eight tentacles like a net, then quickly grab the crustacean and bite into it.

But Gilly observed that, when a juvenile squid grasps its first copepod, it often releases the spiny crustacean and jets backward in a classic startle-escape response.

Perhaps the copepod's needlelike exoskeleton irritates and startles the young squid, triggering an all-or-nothing signal through its giant axons and causing it to involuntarily spurt water.

With practice, novice squid eventually learn to hold onto copepods without automatically jetting in reverse -- an observation that led Gilly and Preuss to suspect that a squid's control of its escape reflex goes hand-in-hand with the development of its hunting skills.

Speedy and slow hunters

To find out, the researchers set up an experiment using newly hatched eggs from squid collected in Monterey Bay.

Newborn animals were divided into two groups. One received a diet that included speedy copepods. The other was fed only slow-moving brine shrimp larvae, which are much easier to catch.

When a newly hatched squid sees a potential meal, its first reaction is to lunge at the prey as quickly as possible -- a strategy that worked well for the group that was given brine shrimp.

In fact, two months into the experiment, the majority of shrimp-eaters were still pouncing on their slow-moving prey instead of developing more subtle hunting techniques.

But a different strategy developed among copepod-fed squid. Despite repeated attempts to pounce on their prey, these young squid were never fast enough to capture the swift crustaceans.

After several weeks of trial and error, they finally became adept copepod hunters. They stopped involuntarily jetting around and learned instead to approach copepods stealthily and then grab them -- a technique none of the shrimp-fed squid ever developed.

Clearly, the two experimental groups had learned different styles of hunting. To determine if the animals' escape reflex had also changed, Gilly and Preuss wired each squid's nervous system to miniature electrodes to compare how copepod-eaters and shrimp-eaters would respond to a very brief electrical shock.

Electrode analysis revealed that, after just two weeks, most copepod-fed squid were indeed firing their small axons first, enabling them to control their automatic escape response. Without this important skill, a wild squid would continue to unintentionally dart backward every time it tried to grab a meal, greatly reducing its ability to capture prey.

It was a different story for the shrimp-fed squid.

Electro-analysis showed that, after eight weeks, most shrimp-eaters were still firing their giant axons first, much like newly hatched squid. They had not learned to control the involuntary escape response and were probably using this infantile reflex to lunge at their prey.

"Furthermore," say the authors, "when switched to a copepod diet, these animals show no sign of developing the suppression of jetting that is necessary for captures" -- evidence that voluntary control of jet propulsion is indeed a behavior that must be learned at an early age.

"The inability of shrimp-fed squid to master copepod capture later in life implies that there is a short window of opportunity during the first weeks after birth in which benefit can be derived from trial-and-error experience," adds Gilly.

"If the squid does not learn to control its startle-escape reflex during that critical period, it seems to lose the ability to program its nervous system in a way that allows it to perform the sophisticated hunting skills that are necessary to survive in the wild."

Human research

This suggests that the process of learning by trial and error causes actual physical changes in the squid's neurons, says Gilly.

Similar findings have been made in vertebrates, including birds, cats and humans.

For example, research on newborn cats and monkeys has shown that sensory visual deprivation early in life leads to the loss of specific neurons in the brain that would normally respond to the visual images missing during development.

These experiments revealed that a critical time period exists when the effects of learned experience are beneficial.

But, Gilly notes, if the experience comes too late, it may do no good at all.

"This body of work also strongly supports the idea that a rich sensory environment is important for normal brain development in humans," Gilly points out.

He says that discovering exactly how a particular experience acts to modify specific neurons and guarantee their survival is one of the major challenges in neuroscience today.

And it's the unique anatomy of the squid that could allow a breakthrough in our understanding of how learning causes physical alterations in the brain.

"The simplicity of the squid's giant axon system will be advantageous in identifying the genes and chemicals involved in causing and maintaining these cellular changes -- even in people," Gilly predicts.

"In this way, the delectable calamari may actually help unlock the secret of how our own brain cells are modified by early childhood experiences and help explain why we are who we are." SR