Our previous studies led us to propose that a regulatory gene, fruitless (fru), functions as part of the Drosophila melanogaster sex determination regulatory gene hierarchy and encodes male-specific proteins (FruM) that build the potential for male sexual behaviors into the central nervous system during development. Recent work by our lab and others has provided strong support for this proposal by demonstrating that the FruM proteins are both necessary and sufficient to specify the potential for male courtship behavior.
The FruM proteins are expressed exclusively in a subset of the CNS neurons and in subsets of the primary sensory neurons of all sensory systems implicated in courtship (vision, hearing, taste, smell, touch). About 2,000 CNS neurons (~2 percent of neurons) express FruM proteins and are found in small groups throughout the brain and ventral nerve cord. Strikingly, these neurons are dedicated to sexual behaviors, as inactivating them has no discernible effects other than on sexual behaviors. The findings that FruM proteins are expressed in only a small portion of the nervous system that is dedicated to sexual behavior and that they are necessary and sufficient for nearly all aspects of sexual behavior are provocative. They suggest FruM provides a handle for dissecting the developmental, genetic, molecular, and neuronal bases of male courtship behavior.
We believe the key to understanding (1) how the potential for a complex behavior is built into the nervous system and (2) how the neurons subserving male courtship behavior function together to ensure the ordered manifestation of the events comprising this behavior is to focus on the groups of neurons in which the FruM proteins are expressed. On the one hand, we can address how the FruM transcription factors shape the anatomical and molecular characteristics of particular groups of neurons. On the other hand, we can address the roles of individual groups of these neurons in the complex set of behaviors that comprise male courtship. Thus we focus on the roles that these neurons play in adult male sexual behavior and on the fru-dependent characteristics that distinguish them.
To elucidate the structure of the Fru-specified courtship circuitry and how it functions, we are using fru-based genetic tools that permit the manipulation of FruM-expressing neurons, without affecting other neurons. This allows us to visualize the nuclei of FruM-expressing neurons and their projections, silence these neurons, change the sex of these cells from male to female or from female to male, and suppress FruM synthesis in targeted neurons. Thus we can functionally manipulate a discrete group of FruM neurons and behaviorally assess the effects of this on the execution of male courtship. We can also use these tools to identify the neuroanatomical and molecular characteristics of neurons that are specified by FruM.
Our findings suggest we (1) have identified with cellular level resolution the cells governing male courtship behavior and (2) in the FruM proteins have transcription factors expressed exclusively within those cells and whose functions are to build those cells into the courtship circuitry. This means that we can now use the powerful somatic cell genetic, molecular, neurobiological, and behavioral tools available in D. melanogaster to answer fundamental neurobiological questions: (1) How are cells allocated during development to become part of the circuitry responsible for a complex innate behavior? How is the pattern of FruM-expressing neurons in the nervous system generated? (2) How is the circuitry responsible for a complex innate behavior built? At both the neuroanatomical and molecular levels, what aspects of neuronal development and differentiation are regulated by FruM expression in the many cell types that comprise this circuit? (3) How does the circuitry responsible for a complex innate behavior function? What roles do individual/groups of FruM-expressing neurons play in courtship behavior? Neuroanatomically, do the FruM neurons comprise a circuit, as strongly predicted by our findings to date, and if so, what is the detailed structure of that circuit?
We hope that these studies will provide a model for how the circuits underlying other innate behaviors are built and function.
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As of February 11, 2009
