While monogamy is rare within the animal kingdom, some species – including humans and many birds – can be highly social and yet sustain monogamous relationships. Zebra finches, for example, are among a number of species of songbirds in which numerous males and females live closely together but maintain monogamous partnerships. Male songbirds use their songs to attract females, who do not themselves sing. But if female birds are attracted to any male song, how do they manage to remain monogamous when surrounded by potential suitors?

In songbirds, and in humans too, a region of the brain called the striatum regulates both social and sexual behaviors. It does this by modulating the release of a molecule called dopamine, which is the brain’s reward signal. Tokarev et al. show that hearing songs triggers dopamine release within the striatum of unattached male zebra finches, but has no such effect in single females. Unattached male songbirds will also put up with irritating puffs of air in exchange for being able to watch videos of singing birds, whereas unattached females will not. Female songbirds with partners will tolerate the air puffs, but only if the videos are accompanied with the songs of their own mate.

These findings suggest that song serves as a generic social stimulus for zebra finch males, helping large numbers of birds to live together. By contrast, for a female zebra finch, the song of her partner is a highly selective sexual stimulus. These sex-specific responses to the same socially-relevant stimuli may explain how gregarious animals are able to maintain monogamous pair bonds. More generally, these results are a step towards understanding how brain reward systems regulate social interactions. Studying these mechanisms in songbird species with different social and mating systems could ultimately provide insights into social and sexual behavior in people.

Many species of highly gregarious and colonial birds form long-term monogamous pairs (Goodson et al., 2012; Goodson and Kingsbury, 2011; Griffith et al., 2010; Zann, 1994). Pair bonding and flocking behaviors are regulated by neuropeptides and dopaminergic reward system (Goodson et al., 2012; Goodson and Kingsbury, 2011). However, for an animal to be highly social and at the same time monogamous, it must possess two distinct reinforcement systems: one with low selectivity for social stimuli to promote aggregation, and another highly selective for sexual stimuli to promote monogamy. But many communicative stimuli, including birdsong, may serve both social and sexual functions. In such cases, reinforcement may depend on stimulus context: for example, in many solitary songbird males, producing the same song may either attract females or repel rival males (Kroodsma and Byers, 1991; Slater, 2003). In social songbirds, however, many females and males live in close proximity, which gives females immediate access to numerous males whose songs may sexually attract them. What is it, then, that allows gregariousness and monogamy to coexist? We investigated this question in zebra finches, which are highly social, yet monogamous songbirds (Griffith et al., 2010; Zann, 1994). Male zebra finches produce a single stereotyped song that can be female-directed or undirected (Jarvis et al., 1998; Scharff and Nottebohm, 1991; Sossinka and Böhner, 1980; ten Cate, 1985; Woolley and Doupe, 2008). Males typically tolerate the singing behavior of their neighbors even when housed in crowed cages, although the song is occasionally used in an aggressive context too (Ihle et al., 2015). Female zebra finches are attracted to male songs (Holveck and Riebel, 2007), but do not sing (Nottebohm and Arnold, 1976).

The zebra finch striatal dopaminergic reward circuitry is activated in both social and sexual context (Banerjee et al., 2013; Ihle et al., 2015; Iwasaki et al., 2014; Sasaki et al., 2006). In general, there are more dopamine-producing neurons in social than in territorial songbirds (Goodson et al., 2009). In zebra finches, gregariousness is correlated with the level of activity in dopaminergic neurons (Kelly and Goodson, 2015). Striatal dopamine increases in social situations, e.g., when adult males interact with females (Ihle et al., 2015; Sasaki et al., 2006), or juvenile males with adult male tutors, and importantly, even without singing in either of these contexts (Ihle et al., 2015). During pair formation striatal dopamine levels increase in both sexes (Banerjee et al., 2013; Iwasaki et al., 2014). In the context of song learning, striatal dopaminergic input is modulated during singing (Gadagkar et al., 2016; Hoffmann et al., 2016; Simonyan et al., 2012). However, although song is an important sexual stimulus in songbirds (Kroodsma and Byers, 1991; Slater, 2003), there is no direct evidence that hearing songs may affect striatal dopamine in either sexual or affiliative (Hausberger et al., 1995) context. Here we performed in vivo imaging and behavioral experiments that show the forebrain dopaminergic system response to song stimulation in zebra finches across sexes and breeding states, in order to distinguish between social and sexual components of song reinforcement in social songbirds.

We developed two complementary experimental approaches. First, we used a delayed positron emission tomography (PET) procedure (Patel et al., 2008) in order to measure dopamine neurotransmission (Laruelle, 2000) in awake and unrestrained birds. Zebra finches were injected with [¹¹C]raclopride radiotracer, which binds to dopamine type 2 (D2) receptors. Instead of acquiring PET immediately, we first stimulated them with song playbacks for 20 min while awake and behaving and scanned them just after the stimulation under general anesthesia (delayed PET, Figure 1, see protocol in Materials and methods). Second, we developed an apparatus for assessing song reinforcement behaviorally. This approach is a variant on drug addiction experiments, which typically measure how much rodents are willing to work, or exchange mild punishment, in return for access to dopaminergic stimulants such as cocaine (Shaham et al., 2000) (Figure 2). We used a song stimulus instead of the drug and measured the extent to which birds were willing to receive mildly aversive air puffs (Tokarev and Tchernichovski, 2014) in exchange for hearing song playbacks. Finally, in order to test for causality between dopamine neurotransmission and song reinforcement behavior, we blocked dopamine neurotransmission with a selective antagonist of D2 receptors L-741,626 (Li et al., 2010; Watson et al., 2012). We used PET to determine the localization of dopaminergic blockage, and then tested behaviorally if blocking of dopamine D2 receptors was sufficient to diminish reinforcing effect of songs.

Figure 1

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Figure 2

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We first tested if our delayed PET technique could detect changes in striatal dopamine neurotransmission after hearing song playbacks. We scanned eight unmated female zebra finches, where we expected to find higher levels of dopamine neurotransmission after song playbacks (i.e., lower levels of [¹¹C]raclopride binding), and eight unmated males, where we expected to find a weaker effect, if any. Each bird was scanned twice: after stimulation with a variety of unfamiliar songs (both female-directed and undirected) over 20 min, and after silence over the same duration (Figure 1). As expected from the distribution of dopamine receptors in the songbird brain (Kubikova et al., 2010), the averaged PET map showed that the striatum was the major site of [¹¹C]raclopride binding in both conditions in males (Figure 3a) and in females (Figure 3b). However, against our expectations, lower level of [¹¹C]raclopride binding after hearing songs (suggesting increased striatal dopamine neurotransmission) was detected only in the male group. In males, the song minus silence parametric difference map showed that song stimulation resulted in significantly lower level of [¹¹C]raclopride binding in a part of the striatum (Figure 3c; cluster-level p_corrected = 0.024, paired t-test corrected for multiple comparisons). Exploratory analysis of individual changes (within the cluster of significant change) showed that [¹¹C]raclopride binding was at lower levels in all males after hearing songs by 29 ± 8% (mean ± s.e.m. hereafter; Figure 3d; p=0.015, pair-wise t-test). These results, based on PET of D2 receptors, are comparable to the 26.5 ± 8.4% increase in dopamine detected with microdialysis in a study where male zebra finches were presented with females (Ihle et al., 2015), confirming that [¹¹C]raclopride binding at D2 receptors is a robust indicator of the overall striatal dopamine neurotransmission.

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Surprisingly, females lacked any brain areas with significant change in [¹¹C]raclopride binding in response to song playbacks. Nevertheless, we produced a mask image from the cluster of significant change in males (Figure 3c) and used it as a volume of interest to assess for a possible effect in females. Exploratory analysis of individual changes in females showed no apparent change in striatal [¹¹C]raclopride binding in response to song playbacks (Figure 3e; 0.4 ± 6%, p=0.737, pair-wise t-test). A direct comparison between males and females showed statistically significant differences in striatal [¹¹C]raclopride binding after hearing songs (Figure 3—figure supplement 1; p=0.015, t-test). Note, however, that the difference in the magnitude of change between males and females is, at least partially, driven by the low baseline (silence) [¹¹C]raclopride binding in females (Figure 3e).

The sexually dimorphic striatal response to songs could reflect behavioral or anatomical differences between sexes not related to reinforcement. First, as striatal dopamine neurotransmission correlates with movement (Cousins and Salamone, 1996; Gadagkar et al., 2016; Howe and Dombeck, 2016), we tested if birds tended to move more when hearing song playbacks, in a manner that could explain our results. We analyzed movement in eight males and eight females, in similar conditions to those in our experiments before PET scan: injection of raclopride followed by 20 min of silence or song playbacks. We observed very little of such body movements as flying, hopping and wing-whirring, and also quantitatively tracked the whole body movement (analyzed every 0.3 s for the center of body mass), but there were no significant differences between conditions or sexes (Figure 3—figure supplement 2; Table 1). Tracking head movement, we observed a significant trend to move the head more during song playbacks in most birds (Figure 3—figure supplement 2). However, there was no significant difference between males and females in this respect (Table 2). Therefore, mere movement is unlikely to explain our finding of male-specific dopamine response to songs.

Another concern is that our results could simply reflect anatomical dimorphism in the basal ganglia pathway of the premotor song system: in particular, Area X, which has high density of dopamine D2 receptors (Kubikova et al., 2010) and receives dopamine during female-directed singing (Sasaki et al., 2006), exists only in zebra finch males. However, Area X was mostly excluded from the cluster of significant change (Figure 3c and Figure 3—figure supplement 3), suggesting that its contribution was small, if any. This is in line with the finding that Area X does not respond to auditory stimulation in awake songbirds, except for error signals during singing (Gadagkar et al., 2016).

Given that the expectation of reward is only one of several scenarios that could explain the unanticipated pattern of striatal dopamine neurotransmission that we observed (Cousins and Salamone, 1996; Gadagkar et al., 2016; Hoffmann et al., 2016; Howe and Dombeck, 2016; Kubikova and Kostál, 2010; Riters, 2011; Salimpoor et al., 2011; Schultz, 2002; Stuber et al., 2008), we developed an independent method for assessing the effect of song reinforcement in male and female zebra finches. In order to directly estimate song reinforcement we paired the song stimulus with a mild punishment. We presented the same birds that had been scanned earlier for dopamine with video of a perching male (Figure 2). Each bird was presented with two daily sessions of videos over ten days (20 sessions, 20 min each). In ten sessions the video was played in silence, and in the alternating ten sessions, it was accompanied by song playbacks (the same mix of initially unfamiliar songs as in the PET experiments). When a bird perched next to the window facing the video display, it would occasionally receive a mildly aversive air puff, in random intervals and without warning. We assessed reinforcement by measuring the number of air puffs the bird was willing to tolerate in return for the stimulus, comparing the silent sessions to the song playback sessions.

We found that males voluntarily received many more air puffs during song playback sessions compared to silent sessions (Figure 4; p=0.001, paired t-test); they appeared attentive during the sessions but did not show any aggressive behavior. Females, on the other hand, showed little motivation to hear song playbacks: their tendencies to receive air-puffs were moderate and did not differ significantly across song playback and silent sessions (Figure 4; p=0.267, paired t-test).

Figure 4

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To test whether the song reinforcement we observed in males was dependent on dopamine neurotransmission, we used the D2 receptor antagonist L-741,626 to interfere with D2 receptors. First, we performed a whole brain PET after injections of L-741,626 in order to determine the localization of dopaminergic blockage: as expected, changes in [¹¹C]raclopride binding were observed exclusively in the striatum (Figure 5). We found substantially lower levels of the striatal binding of [¹¹C]raclopride after L-741,626 injection compared to saline (Figure 5—figure supplement 1). Therefore, L-741,626 blocks D2 receptors in the songbird striatum as it does in rodents (Li et al., 2010; Watson et al., 2012) and primates (Achat-Mendes et al., 2010). We then tested song reinforcement in four males with our air-puff apparatus as described before, but after injections of either L-741,626 or saline on alternate sessions. On the days of L-741,626 injections, the animals were still active and approached the video, but stimulation with song playbacks no longer increased the number of air puffs they were willing to receive, while on the alternate days of saline injections, song reinforcement was similar to that of untreated males (Figure 6; see Table 3 for statistics).

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Figure 6

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How is it that song stimuli are reinforcing in unmated males but not in unmated females? We hypothesized that the non-selective dopamine neurotransmission by unfamiliar songs in males might reflect a social function, but in females, song reinforcement might be exclusively sexually driven, as a part of the mate choice (Riebel, 2009). A possible explanation to those counterintuitive results is that reinforcement could be much more selective in females. We therefore measured song reinforcement in six mated females that were ready to breed (Figure 7—figure supplement 1). We compared song reinforcement in three conditions: video accompanied with the songs of their mates, video accompanied with songs of other, unfamiliar mated males, and video alone. The mated females showed little interest in the videos and minimal motivation to tolerate air puffs in return to hearing non-mate songs. However, they were willing to receive many air puffs in return for hearing their mates’ songs (Figure 7; see Table 4 for statistics).

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Based on these behavioral results, we tested if the pattern of striatal dopamine neurotransmission would be also mate-selective in these females. Using delayed PET, we compared two sets of stimuli: playbacks of mates’ songs versus playbacks of songs produced by other mated males (in both conditions we played a mix of both female-directed and undirected songs). We detected a cluster of voxels with lower [¹¹C]raclopride binding in response to mate song in a small part of the medial dorsal striatum (Figure 8a,b); however, the difference across those voxels did not survive correction for multiple comparisons (Figure 8b). An exploratory post-hoc analysis of individual differences in the same area found that [¹¹C]raclopride binding was 12 ± 4% lower in response to mate song compared to non-mate song (Figure 8c; p=0.042, paired t-test). These differences suggested a weak trend for higher levels of dopamine transmission in response to mates’ songs in females, but this borderline effect should be treated with caution and validated in future studies.

Figure 8

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We found in the zebra finch an unanticipated pattern of sexual dimorphism in dopaminergic responses to song. In males, stimulation with songs resulted in higher levels of striatal dopamine neurotransmission compared to silence condition. Behaviorally too, unfamiliar song playbacks were strongly reinforcing in males. Blocking striatal dopamine D2 receptors extinguished song reinforcement, suggesting involvement of the striatal dopaminergic reward system. In unmated females, hearing songs did not affect dopamine neurotransmission, and playbacks were not reinforcing behaviorally either. In mated females, mate song was strongly reinforcing, with high specificity, but we observed only slightly higher levels of dopamine neurotransmission in response to mate song compared to non-mate song. Thus, in males, both striatal dopamine neurotransmission and behavioral responses to song playbacks indicate low-threshold and non-specific positive reinforcement. This is consistent with a social, perhaps affiliative function of birdsong to promote aggregation (Hausberger et al., 1995). In females, both behavioral and dopaminergic responses to song were high-threshold and mate-selective, consistent with a sexual function to promote monogamy. However, even though behaviorally mated females showed strong reinforcement to mate song, their striatal dopaminergic responses to mate song were barely detectable. This discrepancy will require further assessment in future studies. Note that there are several open questions about the receptor mechanisms that could account for the sexual dimorphism we observed, including different receptors expression levels, different densities of dopaminergic cells, different reuptake mechanisms and different ratios of D1/D2 receptors. For example, it should be tested whether D1 receptors, which are known to be important for reinforcement (Robbins and Everitt, 1996), are also crucial in the reward mechanism of song in zebra finches.

A simple evolutionary scenario can explain the pattern of sexual dimorphism we observed. Territorial songbird males respond aggressively to intruders and are easy to irritate with conspecific song playbacks (Kroodsma and Byers, 1991; Slater, 2003). Females may show strong preference to certain male song features but are generally attracted to conspecific songs (Kroodsma and Byers, 1991; Slater, 2003). Monogamy could be sustained during an evolutionary transition from the territorial to gregarious behavior if male evolved high tolerance to song while female simultaneously co-evolved highly selective reinforcement threshold to songs. Our results are consistent with such a scenario. Future studies could test this hypothesis further by systematic examination of sexual dimorphism across territorial and social species of songbirds, and in species where both sexes sing. We would expect to see a lack of song reinforcement in non-social territorial songbirds, at least outside the breeding period. But possibly, aggressive reaction might also increase brain dopamine, and one should try to carefully dissect such effects. For example, it was shown that fighting cocks (Thompson, 1964) and Siamese fighting fish (Thompson, 1963) may perceive seeing a potential opponent as a reinforcing stimulus; so, either they may look forward to the fight, or it is an anticipation of reward after winning the fight. In Siamese fighting fish, it was shown that dominant males are more likely to use such stimuli than subordinate (Baenninger, 1970). Avian species demonstrate a wide range of social structures, so the reinforcement value of social clues may vary greatly among them. In sum, a sexually dimorphic activation of the dopaminergic reward circuitry that we observed in our study could provide a joint mechanism for aggregation and pair-bonding, two seemingly conflicting characteristics of the social structure of zebra finches and other gregarious yet monogamous species.

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Author details

1. Kirill Tokarev

   1. Department of Psychology, Hunter College, City University of New York, New York, United States
   2. Department of Radiology, Weill Cornell Medicine, New York, United States

   Contribution

   Conceptualization, Data curation, Software, Formal analysis, Funding acquisition, Validation, Investigation, Visualization, Methodology, Writing—original draft, Writing—review and editing

   For correspondence

   kt66@hunter.cuny.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-2129-1324

2. Julia Hyland Bruno

   1. Department of Psychology, Hunter College, City University of New York, New York, United States
   2. Department of Psychology, Graduate Center of the City University of New York, New York, United States

   Contribution

   Data curation, Investigation, Writing—review and editing

   Competing interests

   No competing interests declared

3. Iva Ljubičić

   1. Department of Psychology, Hunter College, City University of New York, New York, United States
   2. Department of Biology, Graduate Center of the City University of New York, New York, United States

   Contribution

   Data curation, Software, Validation, Methodology, Writing—review and editing

   Competing interests

   No competing interests declared

4. Paresh J Kothari

   Department of Radiology, Weill Cornell Medicine, New York, United States

   Contribution

   Resources, Methodology, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1590-8682

5. Santosh A Helekar

   Department of Neurology, Houston Methodist Research Institute, Houston, United States

   Contribution

   Conceptualization, Data curation, Validation, Methodology, Writing—review and editing

   Competing interests

   No competing interests declared

6. Ofer Tchernichovski

   1. Department of Psychology, Hunter College, City University of New York, New York, United States
   2. Department of Psychology, Graduate Center of the City University of New York, New York, United States
   3. Department of Biology, Graduate Center of the City University of New York, New York, United States

   Contribution

   Conceptualization, Resources, Data curation, Software, Supervision, Funding acquisition, Validation, Methodology, Writing—original draft, Project administration, Writing—review and editing

   Competing interests

   No competing interests declared

7. Henning U Voss

   Department of Radiology, Weill Cornell Medicine, New York, United States

   Contribution

   Conceptualization, Resources, Data curation, Software, Formal analysis, Supervision, Funding acquisition, Validation, Investigation, Visualization, Methodology, Project administration, Writing—review and editing

   Competing interests

   No competing interests declared

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