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Connecting Neurons and Behavior
Invertebrate experiments show
peripheral nervous system critical in sensing stimuli
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Think of it as a large company with a centrally located headquarters and manufacturing facility, supplemented with many sales offices scattered about the country. Though they are interdependent, which office connects with customers and produces revenue? It is the sales office out in the periphery.
photo
by Stanley Leary
Physiological and
behavioral experiments conducted in the Georgia Tech School of Biology
artificially reproduced sexually distinct behaviors in male marsh
fiddler crabs by transplanting them with the limbs of female fiddler
crabs.
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The analogy fits for the findings from a series of novel experiments
conducted by researchers at the Georgia Institute of Technology. They
found that properties of sensory neurons in invertebrate animal limbs,
rather than an organism's central nervous system, seem to be critical in
determining what types of information are received and what behaviors
result.
Researchers base their conclusion on physiological and behavioral
experiments that artificially reproduced sexually distinct behaviors in
male marsh fiddler crabs by transplanting them with the limbs of female
fiddler crabs. Ongoing experiments are investigating whether the same
phenomena occurs when male limbs are transplanted onto females.
"Experimental work that can manipulate sensory systems in this way
are extraordinarily rare, and this ability results in an unprecedented
opportunity to explore how behaviors are produced and how sensory
systems are assembled," says Dr. Marc Weissburg, an assistant professor
in the Georgia Tech School of Biology.
Though Weissburg's work addresses questions regarding the
organization of sex-specific nervous systems and the generation of
sex-specific behavior, it has implications beyond gender differences. If
he can determine how invertebrates regenerate neural tissue that
functions successfully, Weissburg believes other researchers may some
day be able to apply those findings to stimulate regeneration in
vertebrates, including humans, he says. Invertebrates and vertebrates
have the same type of nervous system building blocks, and thus
implications — not firm conclusions — can be drawn for humans,
Weissburg explains.
"Because human neural tissue does not normally regrow, examining this
basic process in cases where transplantation is viable may shed light on
how to develop treatments for injuries involving spinal cord damage, or
which result in sensory damage," Weissburg says.
For his experiments, Weissburg chose marsh fiddler crabs (Uca
pugilator) as a sample species because they are quite common in the
eastern United States, and the males and females are strikingly
different in anatomy and behavior. Females have two feeding claws, which
are more sensitive than the male feeding claw. Males have one feeding
claw and a larger claw that is used for defense and for signaling mating
cues. Weissburg and his research team transplanted a developing female
feeding claw onto males in place of their defense claw with a 20 percent
success rate, which was surprisingly high, he says. This resulted in a
sample size of more than 80 animals to date.
Physiological experiments that recorded the electrical activity of
the transplanted claw show it contained chemical sensors that respond to
stimuli, as would any feeding claw. Behavioral studies stimulated the
transplanted claw with various agents. The experiments showed
definitively that neurons from the transplanted claw established
connections in a part of the central nervous system that normally does
not process chemical stimuli. Thus, these connections with the brain
allowed novel input — that is, chemical information — to be acted
upon by the transplanted claw, Weissburg says. Males fed when their
transplanted limb was stimulated (though they most often did so with
their own feeding claw rather than the transplant, indicating a lack of
motor skill in the transplant). Also, males were able to distinguish
among stimuli of different intensities.
"The results are surprising, showing that a brain region normally
wired to process touch, vibration and pressure, and thus insensitive to
chemical stimuli, can process this information," Weissburg says. "Also,
sensory neurons are able to regrow into unfamiliar neural territory,
making it possible for the brain to respond to novel sensory cues."
The question that remains to be answered by future experiments is how
much of the results stem from the brain's ability to adapt and encode
any type of sensory information and how much stems from specific
modifications that occur in the sensory neurons themselves, Weissburg
explains.
The experiment results have secondary implications in explaining
sex-specific behavior. Behaviors expressed in only one sex can largely
stem from the nature of the sensory equipment, Weissburg says. The
physiological experiments indicated that the transplanted female limb
remained physiologically female. Males with transplanted female limbs
became more sensitive to chemical cues applied to the transplanted claw
than to their own feeding claw. Thus males mimicked female behavior when
the transplanted limb was stimulated.
"This is another observation to add to the longstanding debate: What
makes us different, nature or nurture?" Weissburg says. "If it is our
nature, where precisely do those differences reside? Clearly, the
equipment one is dealt has a large effect. Brain differences, while
relevant, may be less important than previously supposed given the
nature of the peripheral nervous system to strongly influence behavior."
Weissburg's experiments are uncommon. Only a few other researchers
have manipulated sensory systems in this fashion, some in invertebrates
and others with vertebrates. Weissburg knows of only one other study,
one with ferrets (a vertebrate), that has resulted in rewiring normal
sensory connections in what Weissburg calls a "cross-modal
reorganization." In the case of ferrets, neurons that sensed visual
stimuli connected to a brain region that normally processed auditory
information. But researchers were only able to produce a limited number
of specimens in this study because it involved a complicated procedure
that created a brain lesion on pre-natal ferrets.
Weissburg's study, however, produced a greater number of specimen
animals because of the relatively easier task of transplanting, he says.
A greater number of specimens yields more definitive results.
"Dr. Weissburg's approach is a good one because of the ease of
transplanting claws on this animal," says Dr. Chuck Derby, a professor
of biology at Georgia State University in Atlanta. "These experiments
can only work because the fiddler crab has this modular chemosensory
structure — its claw. This would be very difficult to do in
vertebrates.
"And these experiments are also powerful because of the greater
possibility of doing a number of different experiments," says Derby, one
of Weissburg's mentors. These include exchanging female for male claws
and vice versa, as well as replacing a male defense claw with a male
feeding claw.
Georgia Tech undergraduate students James Moffett, Omar Johnson and
Brian McAlvin are members of Weissburg's research team and will be
involved in future experiments.
For the full text news release,
see
www.gtri.gatech.edu/res-news/CRAB.html.
For more information, contact Dr. Marc Weissburg, School of
Biology, Georgia Institute of Technology, Atlanta, GA 30332-0230.
(Telephone: 404/894-8433);
(E-mail:
marc.weissburg@biology.gatech.edu)
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