Rapid, Hierarchical Modulation of Vocal Patterning by Steroid Hormones

Abstract

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.

Functional significance of the rapid regulation of brain estrogen action: Where do the estrogens come from?

“…The rapid behavioral activation observed in this experiment [64] thus potentially illustrates in males the synergistic interaction between rapid and slower genomic actions of estradiol as also demonstrated by recent work on female rats (see work of Kow and Pfaff and Vasudevan et al described above; [138,266]). In plain midshipman fish, an intramuscular injection of E 2 increases within 5 min the duration of fictive vocalizations stimulated by electrical stimuli in an in vitro preparation [208]. This effect persists for 15 to 30 min.…”

“…[218]. Remage-Healey and colleagues also recently demonstrated that 11-keto-testosterone (11kT, the main androgen in fishes) rapidly increases the duration of fictive vocalizations stimulated by electrical stimuli in an in vitro preparation ( [208], Remage-Healey and Bass, 2006, cited in [206]). Finally, Clifton and Andrew (1981, [61]) also suggested the existence of rapid effects of testosterone on aggressive behavior in chicks presented with foreign objects.…”

“…This is considerably shorter than the several days commonly required for genomic activation of behavioral responses (see below for further discussion of this issue). This rapidity of action is all the more striking that most of these effects were observed following systemic injections [33,64,69,208] so that the hormone had first to reach the target tissue and accumulate above a certain threshold before it could activate a cellular response and trigger the neuronal circuits involved in the expression of the behavior considered. Alternatively, most of the intra-tissue applications were performed via insertion of hormone in crystals [110,126,138].…”

Brain aromatase mRNA expression in two populations of the peacock blenny Salaria pavo with divergent mating systems

“…In the plainfin midshipman, a species that also presents male alternative reproductive phenotypes, injections of both 11KT and E 2 facilitated the duration of fictive vocalizations in courting males measured in a neurophysiological brain preparation (Remage-Healey and Bass, 2004). However, the fact that courting males presented much lower levels of aromatase in brain regions implicated in the control of vocal courtship displays when compared with parasitic males and females (Schlinger et al, 1999) suggests that T conversion into E 2 is not a main mechanism facilitating male vocal courtship behavior in this species.…”

“…Also, in the goldfish testosterone (T) and estradiol (E 2 ) injections in males stimulated approach behavior toward females within minutes, while fadrozole blocked the stimulatory effect of T (Lord et al, 2009). Finally, in the plainfin midshipman intramuscular injections of both 11KT and E 2 to courting males facilitated the duration of fictive vocalizations (similar to natural vocalizations produced in an agonistic and sexual context) measured in a neurophysiological brain preparation (Remage-Healey and Bass, 2004). These examples would suggest that, similarly to what has been found for birds and mammals, E 2 locally synthesized in the brain from testosterone (T) facilitates some aspects of male sexual behavior in fishes.…”