skip to main content

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 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.  more » « less
Award ID(s):
Author(s) / Creator(s):
; ; ;
Date Published:
Journal Name:
Integrative and Comparative Biology
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. 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 enzyme 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. 
    more » « less
  2. 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 salient 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. 
    more » « less
  3. Abstract

    Individuals of virtually all vertebrate species are exposed to annual fluctuations in the deterioration and renewal of their environments. As such, organisms have evolved to restrict energetically expensive processes and activities to a specific time of the year. Thus, the precise timing of physiology and behavior is critical for individual reproductive success and subsequent fitness. Although the majority of research on seasonality has focused on seasonal reproduction, pronounced fluctuations in other non‐reproductive social behaviors, including agonistic behaviors (e.g., aggression), also occur. To date, most studies that have investigated the neuroendocrine mechanisms underlying seasonal aggression have focused on the role of photoperiod (i.e., day length); prior findings have demonstrated that some seasonally breeding species housed in short “winter‐like” photoperiods display increased aggression compared with those housed in long “summer‐like” photoperiods, despite inhibited reproduction and low gonadal steroid levels. While fewer studies have examined how the hormonal correlates of environmental cues regulate seasonal aggression, our previous work suggests that the pineal hormone melatonin acts to increase non‐breeding aggression in Siberian hamsters (Phodopus sungorus) by altering steroid hormone secretion. This review addresses the physiological and cellular mechanisms underlying seasonal plasticity in aggressive and non‐aggressive social behaviors, including a key role for melatonin in facilitating a “neuroendocrine switch” to alternative physiological mechanisms of aggression across the annual cycle. Collectively, these studies highlight novel and important mechanisms by which melatonin regulates aggressive behavior in vertebrates and provide a more comprehensive understanding of the neuroendocrine bases of seasonal social behaviors broadly.

    more » « less
  4. 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–output 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. 
    more » « less
  5. This review highlights the principal effects of steroid hormones at central and peripheral levels in the neuroendocrine axis. The data discussed highlight the principal role of oestrogens and testosterone in hormonal programming in relation to sexual orientation, reproductive and metabolic programming, and the neuroendocrine mechanism involved in the development of polycystic ovary syndrome phenotype. Moreover, consistent with the wide range of processes in which steroid hormones take part, we discuss the protective effects of progesterone on neurodegenerative disease and the signalling mechanism involved in the genesis of oestrogen‐induced pituitary prolactinomas.

    more » « less