skip to main content
Explore Scholarly Publications and Datasets in the NSF-PAR

  • NSF Public Access
  • Search Results
  • Accepted Manuscript: Social Communication across Reproductive Boundaries: Hormones and the Auditory Periphery of Songbirds and Frogs
Title: Social Communication across Reproductive Boundaries: Hormones and the Auditory Periphery of Songbirds and Frogs
Synopsis Most animals experience reproductive transitions in their lives; for example, reaching reproductive maturity or cycling in and out of breeding condition. Some reproductive transitions are abrupt, while others are more gradual. In most cases, changes in communication between the sexes follow the time course of these reproductive transitions and are typically thought to be coordinated by steroid hormones. We know a great deal about hormonal control of communication behaviors in birds and frogs, as well as the central neural control of these behaviors. There has also been significant interest in the effects of steroid hormones on central nervous system structures that control both the production and reception of communication signals associated with reproductive behaviors. However, peripheral sensory structures have typically received less attention, although there has been growing interest in recent years. It is becoming clear that peripheral sensory systems play an important role in reproductive communication, are plastic across reproductive conditions, and, in some cases, this plasticity may be mediated by steroid hormones. In this article, we discuss recent evidence for the role of peripheral auditory structures in reproductive communication in birds and frogs, the plasticity of the peripheral auditory system, and the role of steroid hormones in more » mediating the effects of the peripheral auditory system on reproductive communication. We focus on both seasonal and acute reproductive transitions, introduce new data on the role of hormones in modulating seasonal patterns, and make recommendations for future work. « less
Authors:
; ; ;
Award ID(s):
2035226
Publication Date:
NSF-PAR ID:
10312599
Journal Name:
Integrative and Comparative Biology
Volume:
61
Issue:
1
ISSN:
1540-7063
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; ; ; ; ; ; ( , Integrative and Comparative Biology)
    Abstract In seasonally breeding vertebrates, hormones coordinate changes in nervous system structure and function to facilitate reproductive readiness and success. Steroid hormones often exert their effects indirectly via regulation of neuromodulators, which in turn can coordinate the modulation of sensory input with appropriate motor output. Female plainfin midshipman fish (Porichthys notatus) undergo increased peripheral auditory sensitivity in time for the summer breeding season, improving their ability to detect mates, which is regulated by steroid hormones. Reproductive females also show differences in catecholaminergic innervation of auditory circuitry compared with winter, non-reproductive females as measured by tyrosine hydroxylase (TH), the rate-limiting enzymemore »in catecholaminergic synthesis. Importantly, catecholaminergic input to the inner ear from a dopaminergic-specific forebrain nucleus is decreased in the summer and dopamine inhibits the sensitivity of the inner ear, suggesting that gonadal steroids may alter auditory sensitivity by regulating dopamine innervation. In this study, we gonadectomized non-reproductive females, implanted them with estradiol (E2) or testosterone (T), and measured TH immunoreactive (TH-ir) fibers in auditory nuclei where catecholaminergic innervation was previously shown to be seasonally plastic. We found that treatment with T, but not E2, reduced TH-ir innervation in the auditory hindbrain. T-treatment also reduced TH-ir fibers in the forebrain dopaminergic cell group that projects to the inner ear, and likely to the auditory hindbrain. Higher T plasma in the treatment group was correlated with reduced-ir TH terminals in the inner ear. These T-treatment induced changes in TH-ir fibers mimic the seasonal downregulation of dopamine in the midshipman inner ear and provide evidence that steroid hormone regulation of peripheral auditory sensitivity is mediated, in part, by dopamine.« less
  2. ; ( , Integrative and Comparative Biology)
    Synopsis Intra- and inter-sexual communications are vital to the survival and reproductive success of animals. In species that cycle in and out of breeding or other physiological condition, sensory function can be modulated to optimize communication at crucial times. Little is known, however, about how widespread this sensory plasticity is across taxa, whether it occurs in multiple senses or both sexes within a species, and what potential modulatory substances and substrates are involved. Thus, studying modulation of sensory communication in a single species can provide valuable insights for understanding how sensory abilities can be altered to optimize detection of salientmore »signals in different sensory channels and social contexts. The African cichlid fish Astatotilapia burtoni uses multimodal communication in social contexts such as courtship, territoriality, and parental care and shows plasticity in sensory abilities. In this review, we synthesize what is known about how visual, acoustic, and chemosensory communication is used in A. burtoni in inter- and intra-specific social contexts, how sensory funtion is modulated by an individual’s reproductive, metabolic, and social state, and discuss evidence for plasticity in potential modulators that may contribute to changes in sensory abilities and behaviors. Sensory plasticity in females is primarily associated with the natural reproductive cycle and functions to improve detection of courtship signals (visual, auditory, chemosensory, and likely mechanosensory) from high-quality males for reproduction. Plasticity in male sensory abilities seems to function in altering their ability to detect the status of other males in the service of territory ownership and future reproductive opportunities. Changes in different classes of potential modulators or their receptors (steroids, neuropeptides, and biogenic amines) occur at both peripheral sensory organs (eye, inner ear, and olfactory epithelium) and central visual, olfactory, and auditory processing regions, suggesting complex mechanisms contributing to plasticity of sensory function. This type of sensory plasticity revealed in males and females of A. burtoni is likely more widespread among diverse animals than currently realized, and future studies should take an integrative and comparative approach to better understand the proximate and ultimate mechanisms modulating communication abilities across taxa.« less
  3. ; ; ( , Integrative and Comparative Biology)
    Synopsis Across the animal kingdom, the ability to produce communication signals appropriate to social encounters is essential, but how these behaviors are selected and adjusted in a context-dependent manner are poorly understood. This question can be addressed on many levels, including sensory processing by peripheral organs and the central nervous system, sensorimotor integration in decision-making brain regions, and motor circuit activation and modulation. Because neuromodulator systems act at each of these levels, they are a useful lens through which to explore the mechanisms underlying complex patterns of communication. It has been clear for decades that understanding the logic of input–outputmore »decision making by the nervous system requires far more than simply identifying the connections linking sensory organs to motor circuits; this is due in part to the fact that neuromodulators can promote distinct and temporally dynamic responses to similar signals. We focus on the vocal circuit dynamics of Xenopus frogs, and describe complementary examples from diverse vertebrate communication systems. While much remains to be discovered about how neuromodulators direct flexibility in communication behaviors, these examples illustrate that several neuromodulators can act upon the same circuit at multiple levels of control, and that the functional consequence of neuromodulation can depend on species-specific factors as well as dynamic organismal characteristics like internal state.« less
  4. ; ; ; ; ; ; ( , Integrative and Comparative Biology)
    Abstract Although mate searching behavior in female túngara frogs (Physalaemus pustulosus) is nocturnal and largely mediated by acoustic cues, male signaling includes visual cues produced by the vocal sac. To compensate for these low light conditions, visual sensitivity in females is modulated when they are in a reproductive state, as retinal thresholds are decreased. This study tested whether estradiol (E2) plays a role in this modulation. Female túngara frogs were injected with either human chorionic gonadotropin (hCG) or a combination of hCG and fadrozole. hCG induces a reproductive state and increases retinal sensitivity, while fadrozole is an aromatase inhibitor thatmore »blocks hCG-induced E2 synthesis. In an analysis of scotopic electroretinograms (ERGs), hCG treatment lowered the threshold for eliciting a b-wave response, whereas the addition of fadrozole abolished this effect, matching thresholds in non-reproductive saline-injected controls. This suggests that blocking E2 synthesis blocked the hCG-mediated reproductive modulation of retinal sensitivity. By implicating E2 in control of retinal sensitivity, our data add to growing evidence that the targets of gonadal steroid feedback loops include sensory receptor organs, where stimulus sensitivity may be modulated, rather than more central brain nuclei, where modulation may affect mechanisms involved in motivation.« less
  5. ; ; ; ( , Brain, Behavior and Evolution)
    As species change through evolutionary time, the neurological and morphological structures that underlie behavioral systems typically remain coordinated. This is especially important for communication systems, in which these structures must remain coordinated both within and between senders and receivers for successful information transfer. The acoustic communication of anurans (“frogs”) offers an excellent system to ask when and how such coordination is maintained, and to allow researchers to dissociate allometric effects from independent correlated evolution. Anurans constitute one of the most speciose groups of vocalizing vertebrates, and females typically rely on vocalizations to localize males for reproduction. Here, we compile andmore »compare data on various aspects of auditory morphology, hearing sensitivity, and call-dominant frequency across 81 species of anurans. We find robust, phylogenetically independent scaling effects of body size for all features measured. Furthermore, after accounting for body size, we find preliminary evidence that morphological evolution beyond allometry can correlate with hearing sensitivity and dominant frequency. These data provide foundational results regarding constraints imposed by body size on communication systems and motivate further data collection and analysis using comparative approaches across the numerous anuran species.« less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email