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
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