During communication, animals integrate sensory and social information to produce signals tuned to their audience and context. Attending to external information can modulate when animals choose to communicate as well as the structure of their communication signals (Bernal and Page, 2023; Greenfield, 2002; Logue and Krupp, 2016; Snijders and Naguib, 2017). For example, Ueno's brown frog, a diurnal species of frog, ceases calling in the presence of birds (Kim et al., 2020), a common strategy among prey to avoid detection from eavesdroppers (Bernal and Page, 2023). Conversely, nuthatches produce alarm calls in response to predators, and the acoustic features of the alarm calls vary depending on both the threat level of the predator as well as the source (self or public) of the predator information (Carlson et al., 2020). During courtship, Drosophila use visual cues about motion and female position to guide transitions between pulse and sine song, and the choice of song is significant for influencing female responses (Clemens et al., 2018; Coen et al., 2014). In zebra and Bengalese finches, males adjust acoustic features of their songs depending on their social context, producing longer, faster, and more stereotyped songs during courtship interactions compared to when males sing while alone (Kao and Brainard, 2006; Sakata et al., 2008; Sossinka and Böhner, 1980; Woolley and Doupe, 2008). However, while many species modify their signals depending on context, there are few instances in which the mechanisms by which signals are modified have been studied.

Dopamine is well-positioned to drive context-dependent changes to vocal behavior across species through its actions across multiple receptor subtypes (Berke, 2018). Throughout vertebrates, dopamine is produced in conserved neuronal populations and dopamine neurons share similar projections to sensory, motor, and cognitive regions across taxa (O'Connell and Hofmann, 2011, O'Connell and Hofmann, 2012; Yamamoto and Vernier, 2011). Dopamine affects the vigor and performance of motor behaviors, for example, depletion of dopamine synthesizing neurons leads to an overall reduction of movement speed (e.g., Parkinson's disease; Bologna et al., 2020; Panigrahi et al., 2015). Additionally, dopamine shapes learning and plasticity, leading to learned place preferences in frogs (Presley et al., 2010), as well as vocal plasticity in birds (Hisey et al., 2018; Kubikova and Košťál, 2010; Macedo-Lima et al., 2021; Woolley, 2019; Xiao et al., 2018). Social and environmental context can drive activity of dopaminergic neurons, thereby producing context-dependent changes to motivation, motor performance, and plasticity. For example, the shift in song performance that occurs from singing alone to directed courtship song in zebra and Bengalese finches (such as increases in stereotypy and speed) may depend on dopamine release into sensorimotor and basal ganglia regions (Ben-Tov et al., 2023; Hara et al., 2007; Matheson and Sakata, 2015; Singh Alvarado et al., 2021; Woolley et al., 2014).

While dopaminergic modulation of context-dependent vocalizations has been especially well-studied in birds, few studies have addressed a similar role in other species. Frogs (anurans) offer a particularly useful group for these investigations given that they produce relatively simple and stereotyped vocalizations that are modulated by social context, and, as basal tetrapods, they offer key phylogenetic insight into the evolution of dopaminergic systems during the vertebrate transition to land. Administration of a general dopamine agonist in frogs induces behavioral effects such as modulation of sleep-wakefulness cycles (Aristakesyan, 2011), feeding behaviors (Glagow and Ewert, 1999, Glagow and Ewert, 1996), and general movement (Chu and Wilczynski, 2007), but little is known about effects on communication behaviors. A dopamine D2 agonist has been shown to reduce calling in green tree frogs (Creighton et al., 2013), however, whether dopamine modulates social decision-making aspects of communication in frogs is unknown.

Túngara frog males produce calls that attract females, and this well-studied sexual communication system is ideal to investigate the role of dopamine in frog social decision-making during acoustic communication (Ryan, 1985). For a calling male túngara frog, there are two primary decisions he must make that are influenced by the social context: when to call and what call to produce. Frogs aggregate into choruses (leks) where they vocally interact. Males typically avoid overlapping their calls with each other, but also time their calls to occur during specific windows relative to other males which can increase their attractiveness to females (Larter and Ryan, 2024a). They also dynamically adjust the quality of their calls in response to other calling males, most notably by appending ‘chucks’ to the ends of their calls. The simple call of this species consists of a ‘whine’, and males will typically append 1–3 chucks to the end of the whine to produce a ‘complex’ call which induces a five-fold increase in attractiveness to females (Ryan, 1985; Ryan et al., 2019).

Here, we used a general dopamine agonist (apomorphine) to pharmacologically activate dopamine sensitive neurons in male túngara frogs during evoked vocal responses to playback stimuli. Because we used a broad-spectrum agonist and did not target a specific brain area, we anticipated broad and diverse effects including modulation of motivational, vocal motor, and cognitive aspects of calling. We specifically hypothesized that treatment with a dopamine agonist would (1) increase overall calling (vigor), (2) increase vocalization speed (performance), and (3) affect the social decision-making processes during competitive vocal interaction with the playback stimuli, enhancing the attractiveness of calls (cognitive effects).