Rapid, hierarchical modulation of vocal patterning by steroid hormones

Vocal control systems have been identified in all major groups of jawed vertebrates. Although steroid hormones are instrumental in the long-term development and maintenance of neural structures underlying vocalization, it is unknown whether steroids rapidly modulate the neural activity of vocal motor systems. The midshipman fish generates advertisement and agonistic calls that mainly differ in duration. A descending midbrain pathway activates a hindbrain-spinal vocal circuit that directly establishes the discharge frequency and duration of the rhythmic vocal motor volley. This vocal motor output, which can be monitored from occipital nerve roots, directly determines the rate and duration of contraction of a pair of sonic muscles and, in turn, the fundamental frequency and duration of vocalizations. Here, we demonstrate that the duration of the vocal motor volley, or fictive vocalization, is rapidly responsive to steroid hormones, including androgens, estrogens, and glucocorticoids. These responses are consistent, in part, with a nongenomic mechanism and are steroid specific at the receptor level, suggesting the possibility of multiple membrane-bound receptor populations. We also show, using intact and semi-intact preparations, that steroids hierarchically modulate fictive vocalizations; whereas the hindbrain-spinal region is both necessary and sufficient for rapid (within 5 min) effects on duration, descending midbrain input is necessary for maintenance (up to 120 min) of these effects. The conserved nature of vertebrate vocal motor systems suggests that the neuroendocrine principles outlined in this study may be a fundamental feature of all vocal vertebrates.