Dissociable effects of social context on song and doublecortin immunoreactivity in male canaries

Abstract

Variation in environmental factors such as day length and social context greatly affects reproductive behavior and the brain areas that regulate these behaviors. One such behavior is song in songbirds, which males use to attract a mate during the breeding season. In these species the absence of a potential mate leads to an increase in the number of songs produced, while the presence of a mate greatly diminishes singing. Interestingly, although long days promote song behavior, producing song itself can promote the incorporation of new neurons in brain regions controlling song output. Social context can also affect such neuroplasticity in these song control nuclei. The goal of the present study was to investigate in canaries (Serinus canaria), a songbird species, how photoperiod and social context affect song and the incorporation of new neurons, as measured by the microtubule-associated protein, doublecortin (DCX), in HVC, a key vocal production brain region of the song control system. We show that long days increased HVC size and singing activity. In addition, male canaries paired with a female for two weeks showed enhanced DCX-immunoreactivity in HVC relative to birds housed alone. Strikingly, however, paired males sang fewer songs that exhibited a reduction in acoustic features such as song complexity and energy, compared to birds housed alone, which sang prolifically. These results show that social presence plays a significant role in the regulation of neural and behavioral plasticity in songbirds and can exert these effects in opposition to what might be expected based on activity-induced neurogenesis.

Sex and seasonal differences in neurogenesis and volume of the song‐control system are associated with song in brood‐parasitic and non‐brood‐parasitic icterid songbirds

“…A negative relationship between neurogenesis levels and song rate is consistent with female blackbirds and cowbirds singing less than males and post‐breeding males singing less than breeding males (Nero, ; Beletsky, ; Kirn et al, ; King and West, ). A negative correlation between singing rate and DCX+ was also reported in male canaries that sing less in the presence of females, but show more DCX+ in HVC (Balthazart et al, ; Alward et al, ). However, Balthazart et al () also showed that castrated males exposed to testosterone and photosensitive and photostimulated birds, individuals that are expected to sing more, had higher levels of DCX+, indicating that the direction of the relationship between neurogenesis and singing is not always consistent.…”

“…Regardless, songbird males across studies sing less in post‐breeding condition and have higher levels of cell division than breeding males (see above). In addition, male canaries that were housed with a female sang less and had more DCX+ than males that were housed either alone or with another male (Balthazart et al, ; Alward et al, ). It seems that higher neurogenesis in HVC may be associated with less singing.…”

Adult Neurogenesis in the Songbird: Region-Specific Contributions of New Neurons to Behavioral Plasticity and Stability

“…At a mechanistic level, factors that rescue new neurons include neurotrophins such as BDNF [Alvarez-Borda et al, 2004], testosterone and its metabolites [Rasika et al, 1999;Yamamura et al, 2011;Alward et al, 2016] and other growth factors [Alshammari et al, 2015;Joppe et al, 2015;Bakos et al, 2016]. At a behavioral level, neuronal lifespan is influenced by exercise [van Praag et al, 1999;van Praag, 2008], stress [Gould et al, 1997], sleep [Guzman-Marin et al, 2005], social conditions [Lipkind et al, 2002;Alward et al, 2014;Holmes, 2016], learning [Shors et al, 2001[Shors et al, , 2002, and use of the brain region in the absence of learning [Li et al, 2000;Pytte et al, 2010].…”

How does testosterone act to regulate a multifaceted adaptive response? Lessons from studies of the avian song system

“…A suite of song features that are behaviourally significant can be discerned once birds transition to stages in their reproductive cycle that allow for reproduction. For example, in canaries, based on field studies of wild canaries and on captive studies, it has been shown that males produce longer songs in the breeding season and produce a higher rate of syllables that are rapid broadband frequency‐modulated syllables . These tend to be syllables that females find especially attractive when selecting mates .…”

“…During the breeding season, males are directing their songs at females while in the non‐breeding season they tend to sing in groups in a non‐directed manner . Thus, in the breeding season and under conditions of high testosterone, males produce long songs with a high percentage of syllables known to be especially attractive to females . Females in a breeding condition with high steroid hormone concentrations are more apt to respond to these songs …”