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Songbirds Happy
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.
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 females 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 M
(left) and 750 M (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 M.
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);
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);
[larger view].
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 birds 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 Hesslers 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.
Source
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.