A pair of wild Zebra (Chestnut-eared) Finches, Poephila guttata.
Image: Adelaide Zebra Finch Society [larger view].
People have been known to “sing for joy” and we often experience happiness when others sing for us. Additionally, birdsong has often brought joy to those who have listened, but what about the birds themselves? Do birds experience “happiness” when they hear birdsong, or when they sing for others? According to newly published research, male songbirds do apparently experience happiness when they sing to females.
Happiness is an emotion, so it is a slippery concept that is difficult to define scientifically. But it is known that brains experience a positive emotional response to obtaining rewards, such as food and sex. This is identifiable by the release of the neuropeptide, dopamine, within specific brain regions after receiving a sought-after reward.
These neural pathways can be readily exploited by addictive drugs, and they are the reason that addictions are maintained long-term. But these neural pathways evolved because they are essential for maintaining normal social behaviors necessary for life. It is reasonable to assume that natural social interactions should stimulate the same reward pathways in the brain as do addictive drugs, this has not well-documented.
Ya-Chun Huang and Neal Hessler, researchers at the RIKEN Brain Science Institute in Saitama, Japan, hypothesized that the same neural activity resulting from addictive drug use can also be triggered by a naturally-occurring social situation. To investigate their hypothesis, they studied zebra finches, small Australian songbirds that have been extensively studied for decades by scientists and ornithologists.
They noted that male zebra finches typically sing in two social situations: the birds produce “directed song” when in the presence of a female, and they also produce “undirected song” when alone. Undirected song is identifiable to a keen listener because it is slightly slower in tempo and more variable in structure than directed song, so it is probably used either for practice or to communicate with unseen birds, while directed song is intended to attract the female’s attention.
Previous research noted that neurons in a specific avian brain region, the ventral tegmental area (VTA), become strongly stimulated when a male zebra finch sings to a female. But it was not known if this stimulation resulted in increased dopamine concentrations, nor whether the resulting dopamine concentrations are the same for both directed and undirected song. To investigate this phenomenon, Huang and Hessler documented whether dopamine concentrations increase in the VTA in response to singing for a female as compared to singing alone.
First, Huang and Hessler identified specific neurons in the VTA that send neural connections, or projections, to one of the well-known song control regions, Area X, by filling individual neurons with a fluorescent dye. These labeled neurons were further characterized by recording their electrical activity and by identifying whether they were dopamine-releasing — “dopaminergic” — neurons after they had been stimulated by one of four specific social situations; silent male alone (control), singing male alone, silent male with female, and singing male with female (figure 1);
Figure 1. Anatomical identification of VTA cell types. (A) Schematic diagram of sagittal view of singing-related areas in the songbird brain. Motor control nuclei (gray) are critically involved in structuring song output, while nuclei of the anterior forebrain pathway (AFP, orange) are required for song plasticity, and appear to be involved in the communicative function of singing. Area X receives a especially strong dopaminergic input from VTA. Below right is an image of a representative bilateral tracer (Fluoro-ruby) injection in Area X. Image of fluorescent tracer (magenta) is overlaid on image of nissl stain in one brain section including Area X (darkly stained oval nucleus). To the left is an overlay of fluorescently labeled cell body retrogradely labeled by an injection in Area X with IR-DIC image visualized in living brain slice. Scale bars indicate 15 μM (left) and 750 μM (right). (B,C). Post-recording confirmation of cell type by immunohistochemistry and electrode-filling dye. Green label for tyrosine hydroxylase (TH) antibody is overlaid with magenta label of neurons filled with fluorescent dye from the recording electrode (Alexa 568, Molecular Probes) – white signal indicates overlap of two signals. Left panel presents example of post recording confirmation of TH-positive dopaminergic neuron, and right panel shows example of recording from TH-negative presumptive gammaaminobutyric acid (GABA) -ergic neuron. Scale bars indicate 30 μM.
DOI: 10.1371/journal.pone.0003281 [larger view].
The recordings of the electrical activity of these individual neurons revealed a stronger response in male zebra finches after they sang for a female when compared to males who either remained silent in the presence of a female, or who sang alone (figure 2a);
Figure 2. AMPA/NMDA ratio of synapses onto VTA dopaminergic neurons is increased after males are exposed to female birds. (A) Representative plots of average EPSCs mediated by AMPA and NMDA glutamate receptors onto VTA dopaminergic neurons. Left, EPSCs recorded after undirected singing session; Center, after directed singing session; Right, after female exposure without singing. Scale bar in left panel applies to left and middle panels, that in right to the right panel; each indicates 50 ms, 40 pA. (B) Average AMPA/NMDA ratios recorded from dopaminergic (filled) and non-dopaminergic (open) neurons after four behavioral contexts. Mean +/- 6s.e.m. are shown for control (colony housed), undirected singing (U), directed singing (FD), and female exposure without singing (FNS) groups (error bar for directed singing FD group is obscured by plot symbol). The number of neurons recorded in each group is indicated above axis.
DOI: 10.1371/journal.pone.0003281 [larger view].
Additionally, Huang and Hessler found that dopamine concentrations were significantly higher for both male birds that sang for females (FD), and in males who remained silent in the presence of females (FNS) (figure 2b).
So far, these data suggest that male birds experience a positive emotional response to the presence of a female, identified by the increased concentrations of dopamine, but how to distinguish between a male bird singing for a female versus who one remains silent in the presence of a female? Interestingly, the stress response suggested a way to distinguish between these possibilities: acute stress also causes increased concentrations of stress hormones, the glucocorticoids, that trigger physiological changes in both brain and body — including a generalized release of dopamine in the brain.
Because Huang and Hessler had no way to know whether simply being in the presence of a female or if being in the presence of a female but being unable to sing is stressful for a male bird, they designed an experiment to test this possibility. They injected the male birds with a drug, mifepristone, that blocks the action of glucocorticoids, before the birds were allowed to see, and sing for, a female (figure 3);
According to the data above, males who saw a female but did not sing (FNS) showed no clear changes in either brain electrical activity nor in VTA dopamine concentrations, whereas males who did sing for females (FD) showed dramatic changes to both their brain activity and dopamine levels. This experiment suggests that acute stress does not play a role in the increased levels of dopamine in the male bird’s brain, because the stress pathway was chemically blocked. So these changes were due to the only other possibility: the act of singing to a female.
Huang and Hessler’s work presents the clearest evidence so far that singing to a female is rewarding for male birds. Evolutionarily speaking, courtship and reproduction are essential life events so they are inherently rewarding, but it was not known if such behaviors are actually experienced as a positive emotional state by birds. These findings are consistent with some mammalian studies that suggest that sexual behavior and attachment (as well as playing video games and consuming chocolate) also stimulate the same brain reward areas and trigger increased dopamine levels. So, despite the distant evolutionary relationship between birds and humans, it may be that during such intense social interactions as courtship, birds share a similar emotional state with us.
Besides identifying potential similarities in the emotional lives of songbirds and humans, this research also suggests that a natural social interaction can trigger the same synaptic activity in VTA dopamine neurons as those documented for addictive drugs in humans, while singing alone did not affect these neurons. Thus, further study of this neural system could provide insights into how both natural and artificial rewards interact with each other, and how addictive drugs can damage the brain reward systems by disrupting the processing of natural rewards such as social interactions.
Ya-Chun Huang, Neal A. Hessler, Kenji Hashimoto (2008). Social Modulation during Songbird Courtship Potentiates Midbrain Dopaminergic Neurons PLoS ONE, 3 (10) DOI: 10.1371/journal.pone.0003281.