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The Journal of Neuroscience, December 17, 2003, 23(37):11568-11576

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Behavioral/Systems/Cognitive
Functional Specialization of Male and Female Vocal Motoneurons

Ayako Yamaguchi,^1,2 Leonard K. Kaczmarek,² and Darcy B. Kelley¹

¹Department of Biological Sciences, Columbia University, New York, New York 10027, and ²Department of Pharmacology, Yale University School of Medicine, New Haven, Connecticut 06520

Vocal behaviors of African clawed frogs (Xenopus laevis) are produced by a single pair of muscles. This simplification, relative to other vertebrates, allows us to more easily determine how CNS motor pathways function to produce sex-specific songs. We describe here certain sexually differentiated properties of vocal motoneurons that are matched to male and female vocal demands. Both active and passive membrane properties differ between the sexes. Male motoneurons have lower input resistances and larger membrane capacitances than female motoneurons. Two distinct firing patterns are found, in different proportions, in males and females. The strongly adapting neurons that predominate in males initiate spikes at short, reliable latencies, whereas the weakly adapting motoneurons characteristic of females translate graded levels of depolarization into different firing rates. Low-threshold potassium currents (I_KL) predominate in males. Hyperpolarization-activated cationic currents (I_H) are found almost exclusively in males. Modeling results indicate that sex-typical active and passive properties can account for the occurrence of strongly and weakly adapting spike trains in the sexes. In particular, I_KL seem to play an important role in determining the firing patterns of neurons. We suggest that these physiological differences facilitate transformation of synaptic inputs into male- and female-specific outputs that generate sexually distinct songs in vivo.

Key words: sex differences; vocal communication; firing properties; motoneurons; ion currents; intrinsic membrane properties; Xenopus laevis

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Received July 22, 2003; revised October 23, 2003; accepted October 24, 2003.

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