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Forebrain nuclei linked to woodpecker territorial drum displays mirror those that enable vocal learning in songbirds [1]

['Eric R. Schuppe', 'Department Of Biology', 'Wake Forest University', 'Winston-Salem', 'North Carolina', 'United States Of America', 'Department Of Neurobiology', 'Behavior', 'Cornell University', 'Ithaca']

Date: 2022-09 

Vocal learning is thought to have evolved in 3 orders of birds (songbirds, parrots, and hummingbirds), with each showing similar brain regions that have comparable gene expression specializations relative to the surrounding forebrain motor circuitry. Here, we searched for signatures of these same gene expression specializations in previously uncharacterized brains of 7 assumed vocal non-learning bird lineages across the early branches of the avian family tree. Our findings using a conserved marker for the song system found little evidence of specializations in these taxa, except for woodpeckers. Instead, woodpeckers possessed forebrain regions that were anatomically similar to the pallial song nuclei of vocal learning birds. Field studies of free-living downy woodpeckers revealed that these brain nuclei showed increased expression of immediate early genes (IEGs) when males produce their iconic drum displays, the elaborate bill-hammering behavior that individuals use to compete for territories, much like birdsong. However, these specialized areas did not show increased IEG expression with vocalization or flight. We further confirmed that other woodpecker species contain these brain nuclei, suggesting that these brain regions are a common feature of the woodpecker brain. We therefore hypothesize that ancient forebrain nuclei for refined motor control may have given rise to not only the song control systems of vocal learning birds, but also the drumming system of woodpeckers.

Funding: This work was funded by the National Science Foundation grants IOS-1947472 and OISE-1952542 (to M.J.F.), Wake Forest University Center for Molecular Signaling seed grant (to M.J.F.), HHMI and NIH Director’s Pioneer Award (to E.D.J.) and Wake Forest University Center for Molecular Signaling Graduate Research Fellowship (to E.R.S.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Introduction

Advanced vocal learning is a rare trait, which thus far has been found in only 3 of over 40 avian lineages (songbirds, parrots, and hummingbirds) and 5 of over 30 mammalian lineages (humans, cetaceans, pinnipeds, elephants, and bats; [1]). Among primates, humans are the only vocal learner, where this trait is a critical component of spoken language. Similar to their behavior, vocal learning birds and humans have been found to have specialized forebrain circuits for the acquisition and production of learned vocalizations [2]. These vocal learning brain regions are embedded in or adjacent to ancient forebrain motor pathways, and they show specialized expression of specific genes [3–5]. Vocal nonlearning birds, including close relatives to vocal learners, have thus far been found to either not contain these forebrain regions or contain rudimentary regions without the same gene expression specializations [4–6]. For these reasons, it is proposed that vocal learning pathways might have arisen by the duplication of brain pathways from surrounding motor learning circuits, which subsequently become specialized for sets of genes involved in neural connectivity, physiology, and plasticity [2,4,7]. This idea also suggests that similar circuits might have evolved for other specialized communication behaviors, such as those that demand extraordinary performance skill and exquisite motor control.

Woodpecker drumming is a highly specialized communication behavior that is performed when individuals rapidly hammer their bill on a tree to generate specific patterns of sounds. Drumming is used to help negotiate territorial interactions (Fig 1A), much like birdsong in some species [8–10], and thus it is markedly different than other woodpecker beak behaviors, such as drilling for food and excavating nest cavities in old trees [9]. Field studies show that increasing drum speeds (beats/s), or increasing drum length by a few beats, profoundly enhances the display’s threat to competitors [8,10]. In fact, birds will attempt to match the tempo of these high-speed drums, even if many individuals fall short of this feat [8,9]. Additionally, a drum’s rhythm encodes information about species identity, such that changes to its cadence and/or acceleration distort the signal’s recognizability to conspecifics [8,10,11]. Studies in multiple woodpecker species also suggest that drums may encode individual identity [12–14] and that woodpeckers can distinguish drums produced by their neighbors compared to those that they have never encountered before [14]. Furthermore, similar to oscine and suboscine [15] passerine birds, woodpeckers appear to have a protracted drum ontogeny, in which signal production becomes less variable during their second breeding season [14]. Thus, content-based selection on drumming should strongly favor the evolution of mechanisms that mediate exquisite motor control of the head and neck to generate an optimal communication signal. Although it is unclear whether woodpecker drumming has a learned component, one possibility is that the mechanisms at the level of the brain may resemble those that mediate vocal communication in vocal learning birds (Fig 1B and 1C).

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TIFF original image Download: Fig 1. Brain regions identified for vocalization and drumming behavior across the avian phylogeny. (A) Waveform and spectrogram diagrams of a spontaneous male downy woodpecker drum recorded at dawn during the breeding season. Image of downy woodpecker from Greg Schechter (CC Public Domain via WikiMedia). (B) Avian phylogeny from [73] further annotated where specialized brain regions have been either identified [red circles: oscine songbirds, parrots, hummingbirds; red circle with black outline: suboscines, which only has RA-like nucleus), and woodpeckers] or investigated and not found (black circles). Note that this figure includes the 7 genera never examined before our current study. (C) Schematic diagram of the oscine “song circuit” that is characterized by a set specialized forebrain song nuclei essential for producing learned vocalizations. This circuit is composed of 2 main interconnected neural pathways: the vocal motor pathway (VMP; HVC and RA) and anterior forebrain pathway (AFP; LMAN, Area X, and DLM). While the VMP is necessary for both the acquisition and production of learned song, the AFP largely only necessary for acquisition. https://doi.org/10.1371/journal.pbio.3001751.g001

Here, we screened the brains of 7 key avian species that represent major lineages assumed to consists of only vocal nonlearners but that have never been tested for such specialized brain regions (Fig 1B and 1C). We used the parvalbumin (PV) gene, which is highly conserved and constitutively up-regulated in the adult forebrain song nuclei of all avian vocal learners examined to-date and the speech cortical regions of humans, but not in their closest vocal nonlearning relatives [4,16,17]. PV codes for a Ca2+ buffering protein, involved in neuroprotection and neural plasticity [18,19]. We found no clear evidence of analogous telencephalic brain nuclei with specialized PV expression in the nonvocal learning birds examined, with one notable exception—the woodpeckers (Fig 1B). These birds contained several pallial nuclei with specialized PV up-regulation, which were in regions where song nuclei of vocal learners are located. However, instead of showing activation during vocalization, these regions showed activation during drumming. Our findings suggest that the drumming system of woodpeckers and the song system of vocal learning birds may have evolved by parallel neural mechanisms.

Parvalbumin (PV) specializations occur in both sexes and other woodpecker species Both male and female downy woodpeckers drum [10]. Thus, we would expect to find the aforementioned brain regions in both sexes, if these areas were in fact involved in drumming behavior. We obtained 3 female downy woodpeckers, and we found the same regions of specialized up-regulated PV expression in dAN, dA, and DLN (Figs 4A, 4B, S3E and S3F). PPT PowerPoint slide

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TIFF original image Download: Fig 4. Parvalbumin (PV) specialization in dorsal arcopallial (dA) and nidopallial (dAN) nuclei in female downy woodpeckers, as well as 2 other woodpecker species. (A, B) Female downy woodpecker. (C, D) Male red-bellied woodpecker. (E, F) Male hairy woodpecker. Shown are representative in situ hybridization microscope images (inverted black and white colormetric) of PV expression (white), with fast red as a counterstain (grey). Nido, nidopallium; Meso, mesopallium; Arco, arcopallium; Ot, optic tectum. Scale bars = 500 μm. White dashed lines in images indicate boundaries for different telencephalic regions. White dashed lines in high-magnification images indicate boundaries for different telencephalic regions (e.g., boundary between nidopallium and mesopallium), whereas blue dashed lines indicate specialized PV regions identified in woodpeckers. Photo credits: Female downy woodpecker from Ken Thomas (Public Domain via WikiMedia); male red-bellied woodpecker from Neal Lewis (Public Domain Mark 1.0 via Flickr); and male hairy woodpecker from David Whelan (Public Domain via WikiMedia). https://doi.org/10.1371/journal.pbio.3001751.g004 Nearly all extant woodpecker species drum to mediate sociosexual interactions [28], and thus we tested whether other taxa in the woodpecker family show the same PV specializations as the downy woodpecker. We examined the brains of male hairy woodpeckers (Leuconotopicus villosus, n = 2) and red-bellied woodpeckers (Melanerpes carolinus, n = 3). Although both taxa are distantly related to downy woodpeckers, they showed PV specializations similar forebrain nuclei as in male downy woodpeckers (Fig 4C–4F).

Lack of detectable specialization thus far in the woodpecker striatum Because PV does not show convergent specialized expression in striatal vocal regions, we sought another marker that does exhibit convergent expression patterns in the striatal vocal nucleus of vocal learners (including humans [4])—regulator of G-protein signaling 12 (RGS12). Specialized up-regulation of this gene marks songbird Area X within the striatum, a nucleus involved in song learning, and the anterior vocal part of the human putamen within the striatum, which is involved in speech learning [4,29]. Whereas we confirmed a clear RGS12 signature in zebra finch Area X (S5C and S5E Fig), we did not find such a signature in the striatum of the downy woodpecker (S5D and S5F Fig). Accordingly, an Area X–like nucleus in the woodpecker brain either does not exist or it does not share a common molecular signature of RGS12 with vocal learning species.

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[1] Url: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3001751

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