Sex-Specific Behavior Controlled By Peripheral Nervous System

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," said Dr. Marc Weissburg, an assistant professor in the Georgia Tech School of Biology. He will present his research, funded by the National Institutes of Health, on Nov. 10 at the Society for Neuroscience annual meeting in Los Angeles.

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 said. Invertebrates and vertebrates have the same type of nervous system building blocks, and thus implications -- not firm conclusions -- can be drawn for humans, Weissburg explained.

"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 said.

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 said. 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 said. 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 said. "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 explained.

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 said. 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 said. "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 said. 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," said 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," said 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.