Show Summary Details

Page of

PRINTED FROM the OXFORD RESEARCH ENCYCLOPEDIA, NEUROSCIENCE ( (c) Oxford University Press USA, 2020. All Rights Reserved. Personal use only; commercial use is strictly prohibited (for details see Privacy Policy and Legal Notice).

date: 20 January 2020

Hormones and Animal Communication

Summary and Keywords

Animals produce communication signals to attract mates and deter rivals during their breeding season. The coincidence in timing results from the modulation of signaling behavior and neural activity by sex steroid hormones associated with reproduction. Adrenal steroids can influence signaling for aggressive interactions outside the breeding season. Androgenic and estrogenic hormones act on brain circuits that regulate the motivation to produce and respond to signals, the motor production of signals, and the sensory perception of signals. Signal perception, in turn, can stimulate gonadal development.

Keywords: animal communication, hormones, steroid, acoustic, vocal, bird, song, testosterone, estrogen, neuromodulation


Many animals produce communication signals in different sensory modalities to attract mates, to coordinate gonadal development within mated pairs, and to deter rivals of the same sex. These signals are produced most often, or only, during the period of active breeding, and the coincidence in timing is a result of the modulation of signaling behavior and physiology by sex steroid hormones associated with reproduction. Circulating levels of androgenic and/or estrogenic hormones, and local estrogen synthesis in the brain, increase at the onset of breeding and stimulate different regions of the brain to increase signaling behavior. Steroids modulate signaling by acting on different brain circuits that regulate (a) the motivation to produce and respond behaviorally to signals; (b) the motor production of the signal; and (c) the sensory perception of the signal. The steroid sensitivity of these brain pathways provides a mechanism for coordinating communication behavior with reproduction. Signaling can be costly for the sender in several ways, including the energetic demands of neural and muscular activity required for signal production, decreased time for other behaviors such as foraging, and increased risk of exposure to predators and parasites. These costs are amplified because individuals may signal hundreds to thousands of times per day early in the breeding season. Steroid regulation of communication decreases these costs by restricting signaling to times of the year when it is required for breeding. Another benefit of steroid regulation is to provide a mechanism for sexually dimorphic development of brain regions required for signal production and endocrine responses to signals. In some taxa (fish, frogs), breeding signals are produced only by males, but females also signal in some reptilian taxa (e.g., Sceloporus lizards; Martins, 1991, 1993), some primate species (Geissmann & Orgeldinger, 2000; Pradhan, Engelhardt, van Schaik, & Maestripieri, 2006), and many species of birds (Odom, Hall, Riebel, Omland, & Langmore, 2014).

The relationship between signaling and steroid hormones has been studied most extensively for acoustic communication systems in ray-finned fish (Actinopterygii), frogs (anuran amphibians), and songbirds (oscine Passeriformes). Hormone modulation of electrocommunication in weakly electric fish (Mormyridae and Gymnotiformes) has also been studied in detail and shows many parallels to acoustic systems (Smith, 2013; Zakon, 1998, 2003). Steroid hormone modulation of visual displays has been shown in lizards (e.g., Sceloporus graciosus; Ruiz, French, Demas, & Martins, 2010), birds (e.g., golden-collared manakins, Manacus vitellinus; Fuxjager, Miles, & Schlinger, 2018), and perhaps also fish (Oliveira & Goncalves, 2008). Sex steroids and their metabolites excreted or secreted serve as chemical signals in many fish, amphibian, and mammalian taxa (Doyle & Meeks, 2018). Peptide hormones released by cells in the preoptic area of the brain (in fish and frogs) or anterior hypothalamus (in birds and mammals) may also modulate communication (Arch & Narins, 2009; Dunham & Wilczynski, 2014; Goodson & Bass, 2001; Grozhik et al., 2013). Neuromodulatory peptides include vasoactive intestinal polypeptide (VIP), arginine-vasopressin (AVP, mammals), arginine-vasotocin (AVT, fish, frogs, birds), oxytocin (OT, mammals), and isotocin (IT; the non-mammalian homolog of oxytocin). Given space constraints, only acoustic systems in vertebrates will be discussed in detail.

Steroid Modulation of Signal Production

Hormones act at multiple levels of the brain and periphery to modulate signaling behavior (Arnold, 1990; Ball, Riters, & Balthazart, 2002; Forlano, Schlinger, & Bass, 2006). Sex steroids act both on brain regions that control the motivation to signal (preoptic area, anterior hypothalamus), and on brain regions and muscles involved in the motor production of signals. This discussion of hormonal modulation of signal production will focus on birdsong as it is well studied and a learned behavior, unlike acoustic signals in most other vertebrates. It should be understood, however, that there are many similarities in the hormonal modulation of acoustic signal behavior and its underlying neuromuscular substrates in fish, frogs, and birds (reviewed in Forlano, Maruska, Sisneros, & Bass, 2016; Leary, 2009).

Sex Steroids Activate Song Behavior in Adult Birds

Song is produced at the highest rate during periods of intense reproductive activity when circulating blood concentrations of gonadal sex steroids, especially testosterone (T), are elevated. In males, T levels generally rise at the onset of the breeding season, fluctuate with different reproductive activities (e.g., courtship, nest building, incubating eggs, feeding young), and then decline to basal levels as breeding ends (Wingfield & Moore, 1987). Castration of males decreases or eliminates singing, and T treatment of castrated or intact males can increase song production (reviewed in Schlinger & Brenowitz, 2017). In some species (e.g., Island Canaries, Serinus canarius) adult females can be stimulated to sing by treatments with T. Other sex steroids, including 5α‎-dihyrdrotestosterone (DHT), 17β‎-estradiol (E2), and progesterone, are also elevated in the blood and/or brain of breeding male birds, and may contribute to song activation (Wingfield, Whaling, & Marler, 1994). In some species, song is also produced outside the breeding season, when circulating hormone levels are basal. Song may be used by nonbreeding birds to defend territories (e.g., Song Sparrow, Melospiza melodia; Smith, Brenowitz, Beecher, & Wingfield, 1997) or to maintain social cohesion in flocks and roosts (e.g., Red-winged Blackbird, Agelaius phoeniceus; Brenowitz, 1981). When produced outside the breeding season, song is given much less often, and with less stereotyped structure, than in breeding birds (Smith et al., 1997; Smith, Brenowitz, Wingfield, & Baptista, 1995). Activation of song in an aggressive context in nonbreeding birds appears to be regulated by the secretion of dehydroepiandrosterone (DHEA) from the adrenal glands, which is converted locally in the brain to T and E2 (Soma, Wissman, Brenowitz, & Wingfield, 2002). DHEA is an inert steroid precursor that does not stimulate hypertrophy of the reproductive system, with the associated energetic costs, in nonbreeding birds (Jalabert, Munley, Demas, & Soma, 2018).

Steroids Act on Neural Circuits That Regulate Signaling Behavior

The motivation to sing, the motor production of song, and song learning in birds are regulated by discrete neural circuits (Figure 1). Neurons at all levels of these circuits have receptors for androgen receptors (AR) and/or estrogen receptors (ER), and respond to steroid binding with changes in electrical activity and/or patterns of gene expression. The pronounced effect of sex steroids on these circuits is consistent with the close relationship between song behavior and reproduction.

Hormones and Animal Communication

Figure 1. A schematic sagittal drawing of the songbird brain showing projections of major nuclei involved in vocal signaling, and the distribution of steroid receptors. The descending motor pathway (green arrows) controls the production of song. The blue arrows indicate the anterior forebrain pathway that is essential for song learning and adult song plasticity. The red arrows indicate the neural circuit that regulates the motivation to sing. Abbreviations: CG/ICo, central grey-intercollicular complex; DLM, medial portion of the dorsolateral nucleus of the medial thalamus; LMAN, lateral portion of the magnocellular nucleus of the anterior nidopallium; nXIIts, tracheosyringeal part of the hypoglossal nucleus; POM, medial preoptic area; RA, robust nucleus of the arcopallium; V, lateral ventricle; X, Area X of the medial striatum.

Bass, Gilland, and Baker (2008) have noted that there is a striking evolutionary conservation of the overall organization of the vocal neural circuitry at the level of the caudal hindbrain and rostral spinal cord in acoustically signaling fish, amphibians, and birds. They suggest that the similarities in this circuitry across taxa arise from an ancestral, shared developmental origin in rhombomere 8. All of these vertebrate taxa have steroid receptors in neurons of midbrain and hindbrain structures involved in signaling. Unique among vertebrates, however, songbirds elaborated upon this ancestral circuitry by evolving a network of steroid-sensitive nonlimbic forebrain nuclei that have descending input to the hindbrain vocal circuit, and this may have been the definitive event in the evolutionary origin of the songbird (i.e., Oscine) lineage of Passerines (Brenowitz, 1997). Mammals evolved descending input from the motor cortex to the hindbrain vocal circuit (Jürgens, 2009), but differ from songbirds in lacking pronounced hormone sensitivity in the forebrain vocal regions.

Steroid Action on Neural Circuit for Motivation to Signal

The motivation to sing is mediated in reproductive birds by steroid activation of the medial preoptic area (POM) and midbrain central grey-intercollicular complex (CG/ICo) (Ball et al., 2002). CG/ICo projects to the sensorimotor song nucleus HVC (see Figure 1). Neurons in POM contain AR, and both AR and ER are present in CG/ICo neurons. T implanted in the POM of castrated male canaries increased the motivation to sing (Alward, Cornil, Balthazart, & Ball, 2018). Lesions of POM disrupted song production in male European Starlings (Riters & Ball, 1999), and electrical stimulation of CG/ICo evokes vocalization in several species (reviewed in Kingsbury, Kelly, Schrock, & Goodson, 2011).

Steroid Action on Neural Circuit and Muscles for Signal Production

The motor pathway controls the production of song. This circuit consists of projections from the thalamic nucleus Uva and the nidopallial nucleus NIf to HVC (not shown in Figure 1). HVC projects to the robust nucleus of the arcopallium (RA), and RA projects to the dorsomedial part of CG/ICo, the tracheosyringeal part of the hypoglossal motor nucleus in the brainstem (nXIIts) (Figure 1), and to respiratory control nuclei in the brainstem (not shown). Motor neurons in nXIIts send their axons to the muscles of the sound-producing organ, the syrinx. When these motorneurons are stimulated, the syringeal muscles contract and move two labial membranes into the expiratory air stream, which sets them into vibration to produce sound. Contraction of the syringeal muscles also changes the shape and/or length of the vocal tract, which influences the frequency composition of sounds produced by the labia (Suthers & Zollinger, 2004). The projection from RA onto the motor neurons in nXIIts is myotopically organized (Vicario, 1991). Neuronal activity in the premotor nuclei HVC and RA is synchronized with the production of sound by the syrinx (Fee, Kozhevnikov, & Hahnloser, 2004). If nuclei in the motor pathway are inactivated, a bird may adopt appropriate posture and beak movements, but does not produce sound (Nottebohm, Stokes, & Leonard, 1976).

AR are expressed at high levels in HVC, RA, NIf, ICo, nXIIts, and the syringeal muscles (Figure 1). HVC and ICo neurons also express ER. The RA-projecting neurons in HVC express only AR (Johnson & Bottjer, 1993; Sohrabji, Nordeen, & Nordeen, 1989).

Steroid binding by neurons in motor pathway can alter their electrical excitability and/or patterns of gene expression. The neurotransmitters norepinephrine (NE) and dopamine (DA), and tyrosine hdroxylase, the rate-limiting enzyme in catecholamine (CA) synthesis, are all present in HVC and RA, as well as area X and LMAN in the song learning circuit (see Steroid Action on Neural Circuit for Song Learning and Plasticity, and also Barclay & Harding, 1988). Castration of male Zebra Finches (Taenopygia guttatus) decreased NE and DA levels and turnover in RA, and E2 restored CA function (Barclay & Harding, 1990). Seasonal changes in circulating T levels alter the expression of genes in HVC and RA that are functionally related to neuronal birth and death, neuronal plasticity, neuronal excitability, angiogenesis, endocrinology, metabolism, and growth factors (Thompson et al., 2012).

Androgen has trophic effects on muscles involved in sound production. Muscle mass, cross-sectional fiber area, motor neuron endplate size, and/or twitch duration and speed increase in response to androgens in muscles involved in sound production in frogs (Girgenrath & Marsh, 2003), fish (Connaughton & Taylor, 1995), and birds (Bleisch, Luine, & Nottebohm, 1984). (Androgens also have trophic effects on muscles involved in visual signaling in frogs (Mangiamele & Fuxjager, 2018), lizards (Johnson, Kircher, & Castro, 2018), and birds (Fuxjager et al., 2018).)

Sex Steroids Influence Song Learning

Song in the oscine Passeriformes is distinctive because it is a learned behavior. In most, but not all, songbird species studied, if a young bird is raised in isolation from other birds, or deafened, it will never produce a normal song as an adult (Konishi, 1965; Marler, 1970; Thorpe, 1958). In many species a bird must hear song during a sensitive period in the first year of life to learn it (e.g., Zebra Finch). In other species, the sensitive period for learning opens again seasonally in adult birds (e.g., European Starling, Sturnus vulgaris; Beecher & Brenowitz, 2005; Brenowitz & Beecher, 2005). During the initial, sensory, phase of juvenile song learning, birds form a sensory memory or template of song that they hear conspecific adults produce. In the subsequent motor phase of learning, birds start to translate this sensory template into a motor program. Initially, a young bird emits sounds that bear only a slight resemblance to the memorized adult song. This first phase of subsong is marked by the production of crude sounds that are highly variable in structure. The young bird gradually improves its vocal performance during the next few months. By comparing auditory feedback of its own vocalizations to the memorized template, a bird comes to produce more polished sounds that increasingly resemble the template. This period of plastic song is characterized by variability in the order in which song syllables are combined. The bird continues to improve its performance so that when it becomes sexually mature at the onset of its first breeding season, it produces a crystallized song that has a well-defined stereotyped structure.

Sex steroids are important for song learning, signaling the onset and termination of sensitive periods for learning. Estrogens and androgens may have opposing functions that may open (estrogen), and close (androgen) sensitive periods of plasticity for new song learning (Bottjer & Johnson, 1997). E2 circulates at high levels in the blood of juvenile Song Sparrows and Swamp Sparrows (Melospiza georgiana; Marler, Peters, Ball, Dufty, & Wingfield, 1988; Marler, Peters, & Wingfield, 1987), when males are acquiring new song memories. E2 levels subsequently decrease when the birds begin to vocalize as young adults. Blood levels of E2 correlate with the degree of song learned by individual Swamp Sparrows (Marler et al., 1987).

Androgens are responsible for terminating the period of song plasticity so that the young adult bird produces a stereotyped version of conspecific song in its first breeding season. Birds castrated or treated with androgen antagonists at different stages of song learning are able to memorize a sensory template of adult song, and proceed through the early motor phases of song learning. On the one hand, without T, birds are unable to develop a stereotyped, complete version of conspecific song (Arnold, 1975; Bottjer & Hewer, 1992; Kroodsma, 1986; Marler et al., 1988). Implanting young birds with exogenous T, on the other hand, produces rapid crystallization, even of incompletely developed song (Korsia & Bottjer, 1991; Whaling, Nelson, & Marler, 1995). These studies show that exposure to high plasma levels of T at puberty is necessary for the production of a stereotyped version of conspecific song.

Steroid Action on Neural Circuit for Song Learning and Plasticity

The anterior forebrain circuit is essential for song learning and adult song plasticity, as well as playing a role in song perception. This pathway consists of projections from HVC to area X in the striatum, from X to the dorsolateral division of the medial thalamus (DLM), from DLM to the lateral portion of the magnocellular nucleus of the anterior nidopallium (LMAN), and finally to RA (Figure 1). Area X is homologous to the mammalian basal ganglia (Luo, Ding, & Perkel, 2001). LMAN neurons that project to RA send collaterals to area X, providing the potential for feedback within this pathway. The projections within this circuit are topographically organized (Foster, Mehta, & Bottjer, 1997). Inactivation of LMAN, DLM, or area X in juveniles prevents the development of normal song, but does not disrupt previously crystallized song in adults (Bottjer, Miesner, & Arnold, 1984; Halsema & Bottjer, 1992; Scharff & Nottebohm, 1991; Sohrabji, Nordeen, & Nordeen, 1990). Juvenile males with lesions of area X persist in producing songs that are variable in structure, as though they are unable to crystallize. In contrast, if LMAN is lesioned in juvenile males, they produce songs with aberrant but stable structure.

Androgen receptors are expressed at high levels in LMAN and DLM neurons, as well as in HVC and RA. AR mRNA was reported to be expressed at low levels in area X in one study (Bernard, Bentley, Balthazart, Turek, & Ball, 1999). The area X-projecting neurons in HVC contain either AR or ER (Johnson & Bottjer, 1993, 1995; Sohrabji et al., 1989), but individual X-projecting neurons express only one of these receptor types (Frankl-Vilches & Gahr, 2018; Gahr, 1990).

Sex Steroids Modulate Signal Perception and Behavioral Responses

Increases in sex steroid levels in the blood and/or locally synthesized E2 in the brain during the breeding season can modulate the activity of neural circuits involved in signal perception, in motivation to respond to signals with aggressive or sexual behaviors, and in reproductive priming. In frogs, fishes, and birds, peripheral and central auditory processing systems exhibit seasonal changes in activity that are associated with changes in reproductive state (reviewed in Caras & Remage-Healey, 2016; Forlano et al., 2016; Wilczynski & Burmeister, 2016). Steroid modulation of auditory activity ensures that receivers will be responsive to the acoustic mating signals produced by senders at the optimal time for reproduction.

Steroids Alter Behavioral Responses to Signals

It is widely observed across vertebrate taxa that males in reproductive condition respond aggressively when they detect the advertisement signals of other males of the same species. Aggressive responses to signals are typically modulated by circulating androgen levels, though the relationship between aggression and T levels can change with season, stage of breeding, parenting status, and social familiarity among individuals (Oliveira, 2004; Wingfield et al., 1994). Castrated males, and males treated with androgen antagonists, generally are less aggressive in response to other males’ signals, and less successful at defending territories against other males during the breeding season (Jalabert et al., 2018; Wingfield, 1994).

Female birds of numerous species perform copulation solicitation displays in response to conspecific, but not heterospecific, songs when in reproductive condition (reviewed in Catchpole & Slater, 2008). Outside the breeding season, female birds do not perform sexual displays to male song. Female canaries in breeding condition built nests more rapidly when exposed to playback of conspecific rather than heterospecific song, and when exposed to more complex canary song than simpler song (Kroodsma, 1976). The response of female Tungara frogs (Physalaemus pustulosus) to conspecific male calls changed with hormonal condition (Lynch, Crews, Ryan, & Wilczynski, 2006). Female frogs showed their strongest phonotaxic approach to playbacks of male calls when circulating levels of estrogen and progesterone peaked (Lynch & Wilczynski, 2005).

The behavioral response of males and females to signals may change with their hormonal levels. During the breeding season, territorial male Red-winged Blackbirds and White-crowned Sparrows (Zonotrichia leucophrys) respond aggressively to the songs of other males (reviewed in Catchpole & Slater, 2008). Female blackbirds and sparrows in reproductive condition respond to conspecific male song by soliciting copulations (Searcy & Brenowitz, 1988; Searcy & Marler, 1984). Outside the breeding season, however, when redwings and sparrows forage and roost in large groups, male song becomes an attractive signal and individuals of both sexes approach singing males (Brenowitz, 1981).

Steroids Act on Neural Circuits for Signal Perception

Hormones act on receptors in auditory end organs and central auditory neurons to modulate their sensitivity and activity in response to acoustic signals across vertebrates. Similar effects of sex steroids on sensory receptors and neurons are seen in weakly electric fish (Smith, 2013; Zakon, 1998).

ER are present in hair cells of auditory end organs in fish (sacculus), birds, and mammals (cochlea), ER are present in the auditory nerve spiral ganglion cell bodies of fish and mammals, and AR are found in the spiral ganglion of birds (Forlano et al., 2016; Noirot et al., 2009; Stenberg, Wang, Sahlin, & Hultcrantz, 1999). Neurons in auditory nucei in the brainstem and midbrain express ER or, to a lesser degree, AR in different vertebrates. Steroid receptors may be sparse or absent in thalamic and primary telencephalic auditory regions, including nucleus ovoidalis and Field L in birds (Caras, 2013; Forlano et al., 2016; Voigt, Ball, & Balthazart, 2009). Telencephalic secondary auditory regions may express ER (e.g., medial caudal nidopallium, NCM, in birds) or AR (e.g., dorsal medial telencephalon in fish; Caras, 2013; Forlano et al., 2016).

Sex steroids act on auditory neurons to modulate their sensitivity to stimulation by, and/or level of activity in response to, conspecific signals. Female midshipman fish (Poricthys notatus) become more sensitive to harmonic frequencies contained in male advertisement calls as their blood levels of E2 and T rise at the onset of the breeding season (Forlano et al., 2016). Female African cichlid fish (Astatotilapia burtoni) in reproductive condition are more sensitive to sound frequencies present in male courtship signals, and there is a correlation between circulating levels of E2 and hearing thresholds (Maruska, Ung, & Fernald, 2012). Hearing conspecific song increases local E2 synthesis in NCM of Zebra Finches, which then increases sound-evoked neuronal activity and auditory response strength (Remage-Healey, Coleman, Oyama, & Schlinger, 2010). E2 treatment of female White-crowned Sparrows increases conspecific song-evoked activity in neurons in Field L, and expands the range of sound intensities over which song stimuli elicit responses (Caras, O’Brien, Brenowitz, & Rubel, 2012). This effect of E2 on activity in Field L neurons is particularly interesting because these cells do not express steroid receptors; hormone modulation may result from steroid effects on auditory nuclei upstream in the sensory circuit, and/or by dopaminergic projections from the central grey (CG), substantia nigra (SN), and ventral tegmental area (VTA) to auditory regions of the brainstem, thalamus, and telencephalon (Appeltants, Absil, Balthazart, & Ball, 2000; Matragrano et al., 2012). Neurons in the CG, SN, and VTA are sensitive to sex steroids (Purves-Tyson et al., 2012; Sipos & Nyby, 1996).

Steroids Act on Neural Circuits that Mediate Aggressive Responses to Signals

The neural circuit that mediates aggressive behavior is conserved across vertebrates, and includes the medial amygdala (nucleus taeniae in birds), the bed nucleus of the stria terminalis (BNST), the lateral septum (LS), the POM, the anterior hypothalamus (AH), the ventromedial hypothalamus (VMH), and CG/ICo (Jalabert et al., 2018). Neurons in each of these brain regions express AR and/or ER. It has been shown in frogs, lizards, and birds that POM and different hypothalamic regions receive auditory input from midbrain and thalamic auditory nuclei (Bruce & Neary, 1995; Hoke, Ryan, & Wilczynski, 2005; Wild, 2017). The extensive connectivity between sub-regions confers auditory sensitivity throughout the hypothalamus. Auditory information is conveyed from the AH and VMH to other nuclei in the circuit for aggression. The auditory sensitivity of neurons throughout this circuit to conspecific signals is modulated by binding of sex steroids, and this provides a neural basis for the observed hormone sensitivity of aggressive responses shown by animals when they detect the signals of other conspecifics.

Signal Perception Can Prime the Reproductive System

Acting through the hypothalamic–pituitary–gonadal axis (HPGA) and the release of gonadotrophin-releasing hormone (GnRH), detection of auditory signals can stimulate testicular and ovarian development (Oliveira, 2004; Wingfield et al., 1994). Perception of conspecific, but not heterospecific, calls stimulates testicular development in males of different frog species (reviewed in Leary, 2009). The rate of seasonal testis growth, and circulating T levels, in male birds of several species have been shown to increase in the presence of females in reproductive condition (reviewed in Wingfield et al., 1994). Detection of conspecific male calls has been shown to stimulate ovarian development, sexual receptivity, and/or circulating E2 levels in female frogs (reviewed in Leary, 2009). In female birds of several species, exposure to a live male producing courtship signals, or to playback of conspecific, but not heterospecific, vocalizations stimulates growth of the ovaries and oviduct in females (reviewed in Wingfield et al., 1994). Auditory sensitivity of hypothalamic neurons thus provides a substrate for interactions between signal perception, hormones, behavioral motivation, and reproductive priming (Hoke et al., 2005).


  • Auditory end organ:

    an anatomical structure that contains the primary sensory receptors (hair cells in vertebrates) that transduce acoustic energy to neural activity.

  • Crystallization:

    the third stage in the motor phase of song learning, when birds produce a well-structured, stereotyped version of the conspecific song model to which they were exposed during the earlier memory acquisition phase.

  • Modulation:

    alteration of ongoing behavior or neural activity

  • Motivation:

    the physiological drive that initiates behavior in response to an internal or external stimulus

  • Oscine:

    a suborder of birds in the order Passeriformes, also referred to as “songbirds”

  • Perception:

    the processing and identification of sensory input.

  • Plastic song:

    the second stage in the motor phase of song learning. Plastic song is louder and better structured than subsong, but still variable in form.

  • Rhombomere:

    in vertebrate embryos, a transient constricted swelling of the neural tube that gives rise to the hindbrain

  • Memory phase:

    the first major phase of song learning, which occurs when a bird listens to and memorizes songs produced by adult conspecific birds.

  • Motor phase:

    the second major phase of song learning, which involves ongoing comparison between a sensory model of song acquired during an earlier memorization phase and auditory feedback from a bird’s own production of song.

  • Subsong:

    the first stage in the motor phase of song learning. Subsong is quiet, poorly structured, and very variable in form.

  • Template:

    a sensory model of song acquired during the initial memory phase of song learning. A bird compares auditory feedback from its own singing with this sensory model to gradually improve song quality to eventually match the template.


Alward, B. A., Cornil, C. A., Balthazart, J., & Ball, G. F. (2018). The regulation of birdsong by testosterone: Multiple time-scales and multiple sites of action. Hormones and Behavior, 104, 32–40.Find this resource:

Appeltants, D., Absil, P., Balthazart, J., & Ball, G. F. (2000). Identification of the origin of catecholaminergic inputs to HVc in canaries by retrograde tract tracing combined with tyrosine hydroxylase immunocytochemistry. Journal of Chemical Neuroanatomy, 18(3), 117–133.Find this resource:

Arch, V. S., & Narins, P. M. (2009). Sexual hearing: The influence of sex hormones on acoustic communication in frogs. Hearing Research, 252(1–2), 15–20.Find this resource:

Arnold, A. P. (1975). The effects of castration and androgen replacement on song, courtship, and aggression in zebra finches (Poephila guttata). Journal of Experimental Zoology, 191(3), 309–326.Find this resource:

Arnold, A. P. (1990). The passerine bird song system as a model in neuroendocrine research. Journal of Experimental Zoology Supplement, 4, 22–30.Find this resource:

Ball, G. F., Riters, L. V., & Balthazart, J. (2002). Neuroendocrinology of song behavior and avian brain plasticity: multiple sites of action of sex steroid hormones. Frontiers in Neuroendocrinology, 23(2), 137–178.Find this resource:

Barclay, S. R., & Harding, C. F. (1988). Androstenedione modulation of monoamine levels and turnover in hypothalamic and vocal control nuclei in the male zebra finch: steroid effects on brain monoamines. Brain Research, 459(2), 333–343.Find this resource:

Barclay, S. R., & Harding, C. F. (1990). Differential modulation of monoamine levels and turnover rates by estrogen and/or androgen in hypothalamic and vocal control nuclei of male zebra finches. Brain Research, 523(2), 251–262.Find this resource:

Bass, A. H., Gilland, E. H., & Baker, R. (2008). Evolutionary origins for social vocalization in a vertebrate hindbrain–spinal compartment. Science, 321(5887), 417–421.Find this resource:

Beecher, M. D., & Brenowitz, E. A. (2005). Functional aspects of song learning in songbirds. Trends in Ecology & Evolution, 20(3), 143–149.Find this resource:

Bernard, D. J., Bentley, G. E., Balthazart, J., Turek, F. W., & Ball, G. F. (1999). Androgen receptor, estrogen receptor alpha, and estrogen receptor beta show distinct patterns of expression in forebrain song control nuclei of European starlings. Endocrinology, 140(10), 4633–4643.Find this resource:

Bleisch, W., Luine, V. N., & Nottebohm, F. (1984). Modification of synapses in androgen-sensitive muscle. I. Hormonal regulation of acetylcholine receptor number in the songbird syrinx. The Journal of Neuroscience, 4(3), 786–792.Find this resource:

Bottjer, S. W., & Hewer, S. J. (1992). Castration and antisteroid treatment impair vocal learning in male zebra finches. Journal of Neurobiology, 23(4), 337–353.Find this resource:

Bottjer, S. W., & Johnson, F. (1997). Circuits, hormones, and learning: Vocal behavior in songbirds. Journal of Neurobiology, 33(5), 602–618.Find this resource:

Bottjer, S. W., Miesner, E. A., & Arnold, A. P. (1984). Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science, 224(4651), 901–903.Find this resource:

Brenowitz, E. A. (1981). Territorial song as a flocking signal in red winged blackbirds (Agelaius phoeniceus). Animal Behaviour, 29(2), 641–642.Find this resource:

Brenowitz, E. A. (1997). Comparative approaches to the avian song system. Journal of Neurobiology, 33(5), 517–531.Find this resource:

Brenowitz, E. A., & Beecher, M. D. (2005). Song learning in birds: Diversity and plasticity, opportunities and challenges. Trends in Neuroscience, 28(3), 127–132.Find this resource:

Bruce, L. L., & Neary, T. J. (1995). Afferent projections to the ventromedial hypothalamic nucleus in a lizard, Gekko gecko. Brain Behavior and Evolution, 46(1), 14–29.Find this resource:

Caras, M. L. (2013). Estrogenic modulation of auditory processing: A vertebrate comparison. Frontiers in Neuroendocrinology, 34(4), 285–299.Find this resource:

Caras, M. L., O’Brien, M., Brenowitz, E. A., & Rubel, E. W. (2012). Estradiol selectively enhances auditory function in avian forebrain neurons. The Journal of Neuroscience, 32(49), 17597–17611.Find this resource:

Caras, M. L., & Remage-Healey, L. (2016). Modulation of peripheral and central auditory processing by estrogens in birds. In A. H. Bass, J. A. Sisneros, A. N. Popper, & R. R. Fay (Eds.), Hearing and hormones (pp. 77–99). Cham, Switzerland: Springer International.Find this resource:

Catchpole, C. K., & Slater, P. J. B. (2008). Bird song: Biological themes and variations (2nd ed.). Cambridge, England: Cambridge University Press.Find this resource:

Connaughton, M. A., & Taylor, M. H. (1995). Effects of exogenous testosterone on sonic muscle mass in the weakfish, Cynoscion regalis. General and Comparative Endocrinology, 100(2), 238–245.Find this resource:

Doyle, W. I., & Meeks, J. P. (2018). Excreted steroids in vertebrate social communication. The Journal of Neuroscience, 38(14), 3377–3387.Find this resource:

Dunham, L. A., & Wilczynski, W. (2014). Arginine vasotocin, steroid hormones and social behavior in the green anole lizard (Anolis carolinensis). The Journal of Experimental Biology, 217(20), 3670–3676.Find this resource:

Fee, M. S., Kozhevnikov, A. A., & Hahnloser, R. H. (2004). Neural mechanisms of vocal sequence generation in the songbird. Annals of the New York Academy of Science, 1016, 153–170.Find this resource:

Forlano, P. M., Maruska, K. P., Sisneros, J. A., & Bass, A. H. (2016). Hormone-dependent plasticity of auditory systems in fishes. In A. H. Bass, J. A. Sisneros, A. N. Popper, & R. R. Fay (Eds.), Hearing and hormones (pp. 15–51). Cham, Switzerland: Springer International.Find this resource:

Forlano, P. M., Schlinger, B. A., & Bass, A. H. (2006). Brain aromatase: New lessons from non-mammalian model systems. Frontiers in Neuroendocrinology, 27(3), 247–274.Find this resource:

Foster, E. F., Mehta, R. P., & Bottjer, S. W. (1997). Axonal connections of the medial magnocellular nucleus of the anterior neostriatum in zebra finches. The Journal of comparative neurology, 382(3), 364–381.Find this resource:

Frankl-Vilches, C., & Gahr, M. (2018). Androgen and estrogen sensitivity of bird song: A comparative view on gene regulatory levels. Journal of Comparative Physiology A, 204(1), 113–126.Find this resource:

Fuxjager, M. J., Miles, M. C., & Schlinger, B. A. (2018). Evolution of the androgen-induced male phenotype. Journal of Comparative Physiology A, 204(1), 81–92.Find this resource:

Gahr, M. (1990). Localization of androgen receptors and estrogen receptors in the same cells of the songbird brain. Proceedings of the National Academy of Science U S A, 87(23), 9445–9448.Find this resource:

Geissmann, T., & Orgeldinger, M. (2000). The relationship between duet songs and pair bonds in siamangs, Hylobates syndactylus. Animal Behaviour, 60(6), 805–809.Find this resource:

Girgenrath, M., & Marsh, R. L. (2003). Season and testosterone affect contractile properties of fast calling muscles in the gray tree frog Hyla chrysoscelis. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 284(6), R1513–R1520.Find this resource:

Goodson, J. L., & Bass, A. H. (2001). Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Research Reviews, 35(3), 246–265.Find this resource:

Grozhik, A. V., Horoszko, C. P., Horton, B. M., Hu, Y., Voisin, D. A., & Maney, D. L. (2013). Hormonal regulation of vasotocin receptor mRNA in a seasonally breeding songbird. Hormones and Behavior.Find this resource:

Halsema, K., & Bottjer, S. (1992). Chemical lesions of a thalamic nucleus disrupt song development in male zebra finches. Society for Neuroscience, 18, 1052.Find this resource:

Hoke, K. L., Ryan, M. J., & Wilczynski, W. (2005). Social cues shift functional connectivity in the hypothalamus. Proceedings of the National Academy of Science U S A, 102(30), 10712–10717.Find this resource:

Jalabert, C., Munley, K. M., Demas, G. E., & Soma, K. K. (2018). Aggressive behavior. In M. Skinner (Ed.), Encyclopedia of Reproduction (Vol. 1, pp. 242–247). New York, NY: Academic Press.Find this resource:

Johnson, F., & Bottjer, S. W. (1993). Hormone-induced changes in identified cell populations of the higher vocal center in male canaries. Journal of Neurobiology, 24(3), 400–418.Find this resource:

Johnson, F., & Bottjer, S. W. (1995). Differential estrogen accumulation among populations of projection neurons in the higher vocal center of male canaries. Journal of Neurobiology, 26(1), 87–108.Find this resource:

Johnson, M. A., Kircher, B. K., & Castro, D. J. (2018). The evolution of androgen receptor expression and behavior in Anolis lizard forelimb muscles. Journal of Comparative Physiology A, 204(1), 71–79.Find this resource:

Jürgens, U. (2009). The neural control of vocalization in mammals: A review. Journal of Voice, 23(1), 1–10.Find this resource:

Kingsbury, M. A., Kelly, A. M., Schrock, S. E., & Goodson, J. L. (2011). Mammal-like organization of the avian midbrain central gray and a reappraisal of the intercollicular nucleus. PLoS ONE, 6(6), e20720.Find this resource:

Konishi, M. (1965). The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Zeitschrift für Tierpsychologie, 22(7), 770–783.Find this resource:

Korsia, S., & Bottjer, S. W. (1991). Chronic testosterone treatment impairs vocal learning in male zebra finches during a restricted period of development. The Journal of Neuroscience, 11(8), 2362–2371.Find this resource:

Kroodsma, D. E. (1976). Reproductive development in a female songbird: Differential stimulation by quality of male song. Science, 192(4239), 574–575.Find this resource:

Kroodsma, D. E. (1986). Song development by castrated marsh wrens. Animal Behaviour, 34(5), 1572–1575.Find this resource:

Leary, C. J. (2009). Hormones and acoustic communication in anuran amphibians. Integrative and Comparative Biology, 49(4), 452–470.Find this resource:

Luo, M., Ding, L., & Perkel, D. J. (2001). An avian basal ganglia pathway essential for vocal learning forms a closed topographic loop. The Journal of Neuroscience, 21(17), 6836–6845.Find this resource:

Lynch, K. S., Crews, D., Ryan, M. J., & Wilczynski, W. (2006). Hormonal state influences aspects of female mate choice in the Túngara Frog (Physalaemus pustulosus). Hormones and Behavior, 49(4), 450–457.Find this resource:

Lynch, K. S., & Wilczynski, W. (2005). Gonadal steroids vary with reproductive stage in a tropically breeding female anuran. General and Comparative Endocrinology, 143(1), 51–56.Find this resource:

Mangiamele, L. A., & Fuxjager, M. J. (2018). Insight into the neuroendocrine basis of signal evolution: A case study in foot-flagging frogs. Journal of Comparative Physiology A, 204(1), 61–70.Find this resource:

Marler, P. (1970). A comparative approach to vocal learning: Song development in white-crowned sparrows. Journal of Comparative Physiology and Psychology Supplement, 71, 1–25.Find this resource:

Marler, P., Peters, S., Ball, G. F., Dufty, A. M., Jr., & Wingfield, J. C. (1988). The role of sex steroids in the acquisition and production of birdsong. Nature, 336(6201), 770–772.Find this resource:

Marler, P., Peters, S., & Wingfield, J. (1987). Correlations between song acquisition, song production, and plasma levels of testosterone and estradiol in sparrows. Journal of Neurobiology, 18(6), 531–548.Find this resource:

Martins, E. P. (1991). Individual and sex differences in the use of the push-up display by the sagebrush lizard, Sceloporus graciosus. Animal Behaviour, 41(3), 403–416.Find this resource:

Martins, E. P. (1993). A comparative study of the evolution of sceloporus push-up displays. American Naturalist, 142(6), 994–1018.Find this resource:

Maruska, K. P., Ung, U. S., & Fernald, R. D. (2012). The African cichlid fish Astatotilapia burtoni uses acoustic communication for reproduction: sound production, hearing, and behavioral significance. PLoS ONE, 7(5), e37612–e37612.Find this resource:

Matragrano, L. L., Beaulieu, M., Phillip, J. O., Rae, A. I., Sanford, S. E., Sockman, K. W., & Maney, D. L. (2012). Rapid effects of hearing song on catecholaminergic activity in the songbird auditory pathway. PLoS ONE, 7(6), e39388.Find this resource:

Noirot, I. C., Adler, H. J., Cornil, C. A., Harada, N., Dooling, R. J., Balthazart, J., & Ball, G. F. (2009). Presence of aromatase and estrogen receptor alpha in the inner ear of zebra finches. Hearing Research, 252(1–2), 49–55.Find this resource:

Nottebohm, F., Stokes, T. M., & Leonard, C. M. (1976). Central control of song in the canary, Serinus canarius. Journal of Comparative Neurology, 165(4), 457–486.Find this resource:

Odom, K. J., Hall, M. L., Riebel, K., Omland, K. E., & Langmore, N. E. (2014). Female song is widespread and ancestral in songbirds. Nature Communications, 5, 3379.Find this resource:

Oliveira, R. F. (2004). Social modulation of androgens in vertebrates: Mechanisms and function. In P. J. B. Slater, J. S. Rosenblatt, C. T. Snowdon, & T. J. Rope (Eds.), Advances in the Study of Behaviour (Vol. 34, pp. 165–239). New York, NY: Academic Press.Find this resource:

Oliveira, R. F., & Goncalves, D. M. (2008). Hormones and social behaviour of teleost fish. In C. Magnhagen (Ed.), Fish Behaviour (pp. 61–125). Boca Raton, FL: CRC Press.Find this resource:

Pradhan, G. R., Engelhardt, A., van Schaik, C. P., & Maestripieri, D. (2006). The evolution of female copulation calls in primates: A review and a new model. Behavioral Ecology and Sociobiology, 59(3), 333–343.Find this resource:

Purves-Tyson, T. D., Handelsman, D. J., Double, K. L., Owens, S. J., Bustamante, S., & Weickert, C. S. (2012). Testosterone regulation of sex steroid-related mRNAs and dopamine-related mRNAs in adolescent male rat substantia nigra. BMC Neuroscience, 13, 95.Find this resource:

Remage-Healey, L., Coleman, M. J., Oyama, R. K., & Schlinger, B. A. (2010). Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird. Proceedings of the National Academy of Science U S A, 107(8), 3852–3857.Find this resource:

Riters, L. V., & Ball, G. F. (1999). Lesions to the medial preoptic area affect singing in the male European starling (Sturnus vulgaris). Hormones and Behavior, 36(3), 276–286.Find this resource:

Ruiz, M., French, S. S., Demas, G. E., & Martins, E. P. (2010). Food supplementation and testosterone interact to influence reproductive behavior and immune function in Sceloporus graciosus. Hormones and Behavior, 57(2), 134–139.Find this resource:

Scharff, C., & Nottebohm, F. (1991). A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: Implications for vocal learning. The Journal of Neurosciencer, 11(9), 2896–2913.Find this resource:

Schlinger, B. A., & Brenowitz, E. A. (2017). Neural and hormonal control of birdsong. In M. Joëls (Ed.), Hormones, Brain and Behavior (3rd ed., pp. 255–290). Oxford, NY: Academic Press.Find this resource:

Searcy, W., & Brenowitz, E. A. (1988). Sexual differences in species recognition of avian song. Nature, 332, 152–154.Find this resource:

Searcy, W. A., & Marler, P. (1984). Interspecific differences in the response of female birds to song repertoires. Zeitschrift für Tierpsychologie, 66(2), 128–142.Find this resource:

Sipos, M. L., & Nyby, J. G. (1996). Concurrent androgenic stimulation of the ventral tegmental area and medial preoptic area: Synergistic effects on male-typical reproductive behaviors in house mice. Brain Research, 729(1), 29–44.Find this resource:

Smith, G. T. (2013). Evolution and hormonal regulation of sex differences in the electrocommunication behavior of ghost knifefishes (Apteronotidae). The Journal of Experimental Biology, 216(13), 2421–2433.Find this resource:

Smith, G. T., Brenowitz, E. A., Beecher, M. D., & Wingfield, J. C. (1997). Seasonal changes in testosterone, neural attributes of song control nuclei, and song structure in wild songbirds. The Journal of Neuroscience, 17(15), 6001–6010.Find this resource:

Smith, G. T., Brenowitz, E. A., Wingfield, J. C., & Baptista, L. F. (1995). Seasonal changes in song nuclei and song behavior in Gambel’s white-crowned sparrows. Journal of Neurobiology, 28(1), 114–125.Find this resource:

Sohrabji, F., Nordeen, E. J., & Nordeen, K. W. (1990). Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch. Behavioral and Neural Biology, 53(1), 51–63.Find this resource:

Sohrabji, F., Nordeen, K. W., & Nordeen, E. J. (1989). Projections of androgen-accumulating neurons in a nucleus controlling avian song. Brain Research, 488(1–2), 253–259.Find this resource:

Soma, K. K., Wissman, A. M., Brenowitz, E. A., & Wingfield, J. C. (2002). Dehydroepiandrosterone (DHEA) increases territorial song and the size of an associated brain region in a male songbird. Hormones and Behavior, 41(2), 203–212.Find this resource:

Stenberg, A. E., Wang, H., Sahlin, L., & Hultcrantz, M. (1999). Mapping of estrogen receptors α‎ and β‎ in the inner ear of mouse and rat. Hearing Research, 136(1), 29–34.Find this resource:

Suthers, R. A., & Zollinger, S. A. (2004). Producing song: The vocal apparatus. Annals of the New York Academy of Science, 1016, 109–129.Find this resource:

Thompson, C. K., Meitzen, J., Replogle, K., Drnevich, J., Lent, K. L., Wissman, A. M., . . . Brenowitz, E. A. (2012). Seasonal changes in patterns of gene expression in avian song control brain regions. PLoS ONE, 7(4), e35119.Find this resource:

Thorpe, W. H. (1958). The learning of song patterns by birds, with especial references to the song of the chaffinch. Ibis, 100, 535–570.Find this resource:

Vicario, D. S. (1991). Organization of the zebra finch song control system: II. Functional organization of outputs from nucleus Robustus archistriatalis. Journal of Comparative Neurology, 309(4), 486–494.Find this resource:

Voigt, C., Ball, G. F., & Balthazart, J. (2009). Sex differences in the expression of sex steroid receptor mRNA in the quail brain. Journal of Neuroendocrinology, 21(12), 1045–1062.Find this resource:

Whaling, C. S., Nelson, D. A., & Marler, P. (1995). Testosterone-induced shortening of the storage phase of song development in birds interferes with vocal learning. Developmental Psychobiology, 28(7), 367–376.Find this resource:

Wilczynski, W., & Burmeister, S. S. (2016). Effects of steroid hormones on hearing and communication in frogs. In A. H. Bass, J. A. Sisneros, A. N. Popper, & R. R. Fay (Eds.), Hearing and hormones (pp. 53–75). Cham, Switzerland: Springer International.Find this resource:

Wild, J. M. (2017). The ventromedial hypothalamic nucleus in the zebra finch (Taeniopygia guttata): Afferent and efferent projections in relation to the control of reproductive behavior. Journal of Comparative Neurology, 525(12), 2657–2676.Find this resource:

Wingfield, J., & Moore, M. C. (1987). Hormonal, social and environmental factors in the reproductive biology of free-living male birds. In D. Crews (Ed.), Psychobiology of reproductive behavior: An evolutionary perspective (pp. 149–175). Englewood Cliffs, NJ: Prentice-Hall.Find this resource:

Wingfield, J. C. (1994). Control of territorial aggression in a changing environment. Psychoneuroendocrinology, 19(5–7), 709–721.Find this resource:

Wingfield, J. C., Whaling, C. S., & Marler, P. (1994). Communication in vertebrate aggression and reproduction: The role of Hormones. In E. Knobil & J. D. Neill (Eds.), The Physiology of Reproduction (2nd ed., pp. 303–342). New York, NY: Raven Press.Find this resource:

Zakon, H. H. (1998). The effects of steroid hormones on electrical activity of excitable cells. Trends in Neuroscience, 21(5), 202–207.Find this resource:

Zakon, H. H. (2003). Insight into the mechanisms of neuronal processing from electric fish. Current Opinion in Neurobiology, 13(6), 744–750.Find this resource: