As we celebrate our 20th anniversary, Lisa Maier shares the story of how one PLOS Biology paper set the course for her…
In this ‘behind the paper’ post, Eric Schuppe discusses how seeing a woodpecker drumming up close and a new collaboration changed the course of his dissertation.
Our new paper is a result of a multi-year collaboration between the labs of my PhD advisor, Matthew Fuxjager, and of Erich Jarvis, to study how the brain might control metrically complex forms of non-vocal “gestural” communication.
The use of gesture is one of the most ubiquitous forms of communication in the animal kingdom. Iconic examples of these social signals include frogs that wave their feet to compete with rivals or birds that perform elaborate acrobatic maneuvers to court potential mates. Non-vocal gestural communication is even frequently used by primates, including humans, to navigate complex social interactions. This includes waving at your friend from a distance or pointing in the direction that you want to go. Despite the importance of this behavior, the mechanisms that allow animals to control these elaborate displays is still a mystery.
When I first started in Matt’s lab, we were interested in identifying potential organisms to use to study the neural and muscular adaptations that allow animals to produce gestures that incorporate physically demanding body and limb movements. Not too long after starting my PhD, my advisor suggested that there was a promising organism right in our backyard – woodpeckers. At the time, I knew nothing about these birds or their social signals. Early one spring morning on my walk into the lab, I heard the loud staccato sound of a downy woodpecker drumming on a tree nearby. It was incredible to watch this bird rapidly strike its bill against the tree with such force. The unusual nature of these displays fascinated me, and made me want to learn more about why this form of communication evolved in the first place. My first dissertation chapters showed that woodpeckers exhibit complex species-specific drums with unique rhythms, speeds (beats/sec) and lengths (number of beats). My work even identified that components of this signal, including drum length and speed, influenced the outcome of territorial interactions. Indeed, it turns out that downy woodpeckers will adjust their own drums to match the tempo of high-speed drums.
These observations got us curious about how the brain might control and refine the temporally precise movements of drumming. To identify brain regions associated with drumming, we began a collaboration with Erich Jarvis’ lab. We hypothesized that neural circuits for gesture might be established through the evolutionary reconfiguration of ancient circuits that control other complex movements. If this were the case, then regions that underlie drumming might have emerged from ancestral motor pathways that generally control motor refinement, including circuits that gave rise to the forebrain nuclei that allow songbirds to master the fine motor skills necessary to produce intricate songs. It is generally assumed that specialized forebrain nuclei that control and modulate skill-based displays do not exist outside of vocal-learning birds (songbirds, parrots, and hummingbirds). However, there have been no comprehensive investigations that use conserved markers to look for anatomically and functionally similar brain areas for displays across the avian tree of life. We used parvalbumin, a gene that is enriched in the specialized nuclei that control learned song, to scan the brains of 7 species across diverse avian lineages that have never been tested for such specialized brain regions. These non-vocal-learning birds exhibited no trace of specialized parvalbumin expression that would be reminiscent of forebrain nuclei in songbirds. To our surprise, the one exception was woodpeckers! Conventional wisdom would suggest that these brain regions should not exist in these birds, but we could so clearly see them under the microscope. As we continued to look across other woodpecker species, we also found that they exhibited three parvalbumin-rich nuclei that were in anatomically similar positions to those found in songbirds.
Given these striking results, we next investigated how these forebrain nuclei might participate in drumming by looking at immediate early gene (IEG) expression as a proxy for recent neural activity. This was perhaps one of the most difficult parts of the study. It required me to catch wild downy woodpeckers that responded to playback of drums with different aggressive responses, including birds that did not drum. To do this, I would often go into the woods before dawn with nothing but the light from my headlamp to guide me to previously identified territories where I wanted to set up my behavioral assay. Our findings from these experiments demonstrated that only woodpeckers that drummed exhibited significant IEG induction in these parvalbumin-rich regions. Furthermore, the amount of drumming was positively related to IEG expression, suggesting that these nuclei likely participate in the production of this display.
Altogether, our findings suggest that woodpeckers exhibit forebrain nuclei that appear to be analogous to the substrates within the ‘song circuit’ of vocal-learning birds (i.e., oscines, hummingbirds, parrots). This unexpected finding is the first piece of evidence, in any vertebrate, that specialized brain regions can control non-vocal gestural communication. We expect that these substrates arose through an ancient motor learning and refinement pathway. In this way, the evolutionary repurposing and specialization of existing circuits may provide an avenue for display diversification.
Overall, my experiences have left me with a newfound appreciation for the challenges that others have faced when performing neuroethological studies on field-collected animals. We had to painstakingly work to create controlled behavioral experiments in nature. Despite the difficultly of these field experiments, I am left incredibly excited about the range of interesting questions to test in the future. For instance, planned future experiments in woodpeckers will explore how these nuclei influence woodpecker drumming behavior and whether they are necessary to acquire stereotypical species-specific drum rhythms. What I find even more intriguing is that our results raise the exciting possibility that similar forebrain substrates may be present in other avian species that produce complex body and limb movements to communicate. As I wrap up my work on woodpeckers, I remain inspired by the research questions that I began with for this paper. My current research investigates how ancient neural circuits that underlie vocal communication in fish might be shared across diverse vertebrate species.