Core and shell song systems unique to the parrot brain
Open accessAbstract
The ability to imitate complex sounds is rare, and among birds has been found only in parrots, songbirds, and hummingbirds. Parrots exhibit the most advanced vocal mimicry among non-human animals. A few studies have noted differences in connectivity, brain position and shape in the vocal learning systems of parrots relative to songbirds and hummingbirds. However, only one parrot species, the budgerigar, has been examined and no differences in the presence of song system structures were found with other avian vocal learners. Motivated by questions of whether there are important differences in the vocal systems of parrots relative to other vocal learners, we used specialized constitutive gene expression, singing-driven gene expression, and neural connectivity tracing experiments to further characterize the song system of budgerigars and/or other parrots. We found that the parrot brain uniquely contains a song system within a song system. The parrot "core" song system is similar to the song systems of songbirds and hummingbirds, whereas the "shell" song system is unique to parrots. The core with only rudimentary shell regions were found in the New Zealand kea, representing one of the only living species at a basal divergence with all other parrots, implying that parrots evolved vocal learning systems at least 29 million years ago. Relative size differences in the core and shell regions occur among species, which we suggest could be related to species differences in vocal and cognitive abilities.
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Parrot pallial song nuclei underwent a further duplication event to evolve a unique additional circuit, the shell song system, which is particularly well developed in large-brained parrots.
“Intriguingly, parrot pallial song nuclei underwent a further duplication event to evolve a unique additional circuit, the so-called shell song system, which seems to be particularly well developed in large-brained parrots (45).”
From Birds have primate-like numbers of neurons in the forebrain (2016) · cites this paper as [45]
The Introduction and Discussion describe a parrot-specific shell system that evolved after a core-like system, and the Results report larger shell regions in larger-brained species. However, the paper does not establish that the pallial song nuclei underwent a duplication event; it presents the system’s evolutionary sequence as a hypothesis. The Discussion also notes a larger-brained exception, the kea, whose shell specialization is not robust. The indexed passages provide section labels but no page numbers. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe relatively enlarged subpallium in large parrots is likely associated with their greater learning skills, including vocal learning, and enhanced foot and beak dexterity.
“Because subpallial structures play an important role in sensory and motor learning and execution of motor behavior (15, 44), we suggest that the relatively enlarged subpallium in large parrots is likely associated with their greater learning skills, including vocal learning, and enhanced foot and beak dexterity (5, 6, 13, 45).”
From Birds have primate-like numbers of neurons in the forebrain (2016) · cites this paper as [45]
The Results section on core and shell area ratios reports larger song-nucleus shell regions in larger-brained parrot species typically considered to have more advanced vocal and cognitive abilities. The paper does not establish that the subpallium as a whole is relatively enlarged in large parrots or link that enlargement to foot and beak dexterity. (LLM, conf=0.83)
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BackgroundVocal learning: Beyond the continuum
Martins, P. T., & Boeckx, C. A. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000672 · Cited by 51 · see citing works
“Besides those pathways, parrots were discovered to have a “shell” song system in addition to the “core” song system in all vocal learning birds [19].”
BackgroundCahill, J. A., Armstrong, J. C., Deran, A., Khoury, C. J., Paten, B., Haussler, D. H., & Jarvis, E. D. (2021) · Genome Research · doi:10.1101/gr.275989.121 · Cited by 41 · see citing works
Self-citationWhat animals can teach us about human language: the phonological continuity hypothesis
Fitch, W. T. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.01.014 · Cited by 27 · see citing works
“Neurally, Jarvis and colleagues have suggested that the song system in vocal learning birds results from duplication and differentiation of general motor system circuitry [60,61].”
BackgroundA survey of vocal mimicry in companion parrots
Benedict, L., Charles, A. P., Brockington, A., & Dahlin, C. (2022) · Scientific Reports · doi:10.1038/s41598-022-24335-x · Cited by 23
The Comparative Psychology of Intelligence: Some Thirty Years Later
Pepperberg, I. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.00973 · Cited by 19 · see citing works
“However, lest we are tempted to use this information to argue for the lack of differences between human-non-human abilities or among nonhuman species, we also know that even within related species— for example, among closely-related corvids and also among lessclosely related parrots—there exist subtle and not-so-subtl…”
BackgroundBeat-based dancing to music has evolutionary foundations in advanced vocal learning
Patel, A. D. (2024) · BMC Neuroscience · doi:10.1186/s12868-024-00843-6 · Cited by 18 · see citing works
“The elaborate vocal learning circuitry of parrots was demonstrated by Jarvis and colleagues in neural research using gene expression and tract tracing to compare parrot brains from several species to the brain of a well-studied songbird species (the zebra finch) [82].”
BackgroundRecent developments in parrot cognition: a quadrennial update
Rössler, T., & Auersperg, A. (2022) · Animal Cognition · doi:10.1007/s10071-022-01733-2 · Cited by 18 · see citing works
A dual larynx motor networks hypothesis
Belyk, M., Eichert, N., & McGettigan, C. (2021) · Philosophical Transactions of the Royal Society B · doi:10.1098/rstb.2020.0392 · Cited by 17 · see citing works
“The parrot brain is unusual in containing two parallel song systems [150].”
BackgroundNonhuman and Nonhuman-Human Communication: Some Issues and Questions
Pepperberg, I. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2021.647841 · Cited by 17 · see citing works
Brain Size Associated with Foot Preferences in Australian Parrots
Kaplan, G., & Rogers, L. (2021) · Symmetry · doi:10.3390/sym13050867 · Cited by 16 · see citing works
“Even more puzzling, from a functional point of view, is, as Chakraborty and colleagues [38,39] discovered, that parrots have a core and shell song systems, i.”
BackgroundDuplications and domain-generality.
Endress, A. D. (2019) · Psychological Bulletin · doi:10.1037/bul0000213 · Cited by 15 · see citing works
Sex differences in behavioural and neural responsiveness to mate calls in a parrot
Eda-Fujiwara, H., Satoh, R., Hata, Y., Yamasaki, M., Watanabe, A., Zandbergen, M. A., Okamoto, Y., Miyamoto, T., & Bolhuis, J. (2016) · Scientific Reports · doi:10.1038/srep18481 · Cited by 16
“A recent study reported that, unlike other vocal learning bird lineages, the parrot song system has core and shell regions 35 .”
Can a bird brain do phonology?
Samuels, B. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01082 · Cited by 15 · see citing works
Zhao, Z.-L., Teoh, H. K., Carpenter, J., Nemon, F., Kardon, B., Cohen, I., & Goldberg, J. H. (2023) · bioRxiv · doi:10.1101/2023.05.04.539392 · Cited by 14
“For example, while LMAN and MMAN project to RA and HVC, respectively, MO and NAO both project to both AAC and NLC, forming a feedforward loop 20,22,25,26 .”
BackgroundInfluentialWright, T. F., & Derryberry, E. (2021) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.02.022 · Cited by 13 · see citing works
SRGAP2 and the gradual evolution of the modern human language faculty
Martins, P. T., Marí, M., & Boeckx, C. (2017) · bioRxiv · doi:10.1101/143248 · Cited by 13
“SRGAP2C may have had other functional consequences [66, 65, 68], but we have provided evidence that mechanistically we can expect SRGAP2C to have had an effect on the SLIT-ROBO axon guidance pathway, and — no doubt together with other genetic changes — may have contributed to the establishment of a critical aspect of…”
BackgroundResultInfluentialSchuppe, E. R., Cantin, L. J., Chakraborty, M., Biegler, M. T., Jarvis, E. R., Chen, C.-C., Hara, E., Bertelsen, M., Witt, C. C., Jarvis, E., et al. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001751 · Cited by 12 · see citing works
Self-citationPlace preference and vocal learning rely on distinct reinforcers in songbirds
Murdoch, D., Chen, R.-D., & Goldberg, J. H. (2018) · Scientific Reports · doi:10.1038/s41598-018-25112-5 · Cited by 10 · see citing works
Cockatiels sing human music in synchrony with a playback of the melody
Seki, Y. (2021) · PLoS ONE · doi:10.1371/journal.pone.0256613 · Cited by 8 · see citing works
Contrafreeloading in kea (Nestor notabilis) in comparison to Grey parrots (Psittacus erithacus)
Smith, G. E., Bastos, A. P. M., Chodorow, M. S., Taylor, A. H., & Pepperberg, I. M. (2022) · Scientific Reports · doi:10.1038/s41598-022-21370-6 · Cited by 7 · see citing works
Vocal development in nestling kea parrots (Nestor notabilis)
Wein, A., Schwing, R., Yanagida, T., & Huber, L. (2020) · doi:10.1080/09524622.2019.1705184 · Cited by 7
Moran, I. G., Loo, Y. Y., Louca, S., Young, N., Whibley, A., Withers, S. J., Salloum, P. M., Hall, M. L., Stanley, M. C., & Cain, K. (2024) · Communications Biology · doi:10.1038/s42003-024-06253-y · Cited by 6 · see citing works
“While advanced vocal learning is well established in parrots (Psittaciformes) 7 , hummingbirds (Trochiliformes) 6 , and oscine songbirds (Passeriformes) 8 , the picture is less clear for suboscines (Passeriformes) and the New Zealand wrens (Passeriformes and sister sub-order to oscines and…”
Auditory Pattern Discrimination in Budgerigars (Melopsittacus undulatus).
Fishbein, A. (2022) · Behavioural Processes · doi:10.1016/j.beproc.2022.104742 · Cited by 5
Zhao, Q., & Sun, Y. (2016) · Avian Research · doi:10.1186/s40657-016-0048-z · Cited by 14 · see citing works
“2015; Sherry and MacDougall-Shackleton 2015); the size of auditory areas is linked to song learning behavior in bird (Nottebohm 1981; Chakraborty et al. 2015); and the size of the forebrain region is link to social behavior (Lipkind et al.”
BackgroundBaciadonna, L., Cornero, F. M., Emery, N. J., & Clayton, N. S. (2020) · Learning & Behavior · doi:10.3758/s13420-020-00434-5 · Cited by 43 · see citing works
“Most parrots, with the exception of the New Zealand keas, have also been found to have an additional “song system” in their brains, forming a shell around the primary song system common to parrots, songbirds, and hummingbirds (species considered to be vocal learners; Chakraborty et al., 2015).”
BackgroundInfluentialSubcortical Contributions to the Uniqueness of Human Cognition
Shi, E. R., & Zhang, E. Q. (2021) · Biolinguistics · doi:10.5964/bioling.9189 · Cited by 3 · see citing works
“…that neocortex is important for the evolution of high-level cognition, studies on birds who lack neocortices show that they exhibit high intelligence, like crows’ tool use (Hunt 1996) and parrots’ vocal imitation (Chakraborty et al. 2015), suggesting an important role of subcortex in cognition.”
BackgroundCan AI help with the hardest thing: pro health behavior change
Miller, D. D. (2026) · npj Cardiovascular Health · doi:10.1038/s44325-025-00101-6 · Cited by 3 · see citing works
“Natural languages are uniquely human among information fl ows, being primarily used during face-to-face communication 47 .”
Wilson, B., & Petkov, C. (2018) · Benjamins Current Topics · doi:10.1075/is.17038.wil · Cited by 3 · see citing works
Vocal Conditioning in Kea Parrots (Nestor notabilis)
Wein, A., Schwing, R., Hausberger, M., Rodríguez, R., & Huber, L. (2017) · Journal of Comparative Psychology · doi:10.1037/com0000098 · Cited by 3
Third-party imitation is not restricted to humans
Haldar, E., Sanchez, A. H., Tennie, C., Ortiz, S. T., Vos, J., Valbert, M., & von Bayern, A. V. (2025) · bioRxiv · doi:10.1038/s41598-025-11665-9 · Cited by 2 · see citing works
“Parrots are among the very few animal taxa possessing vocal imitation ability 47–49 tool-making skills 50,51 foraging cultures 52 and vocal dialects 36 .”
Comparative approaches to the neurobiology of avian vocal learning
Zhao, Z.-L., & Goldberg, J. H. (2025) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2025.102993 · Cited by 2 · see citing works
Walløe, S., Chakraborty, M., Balsby, T., Jarvis, E., Dabelsteen, T., & Pakkenberg, B. (2021) · Brain, Behavior and Evolution · doi:10.1159/000517489 · Cited by 2 · see citing works
“Further, it has recently been discovered that the parrot vocal control system has unique shell nuclei surrounding the core nuclei, the latter similar to songbirds and hummingbirds, where the shell system, particularly that of MO, is relatively larger than the core in species with greater vocal learning abilities [Chak…”
BackgroundMethodResultInfluentialSelf-citationMemory-specific correlated neuronal activity in higher-order auditory regions of a parrot
Satoh, R., Eda-Fujiwara, H., Watanabe, A., Okamoto, Y., Miyamoto, T., Zandbergen, M. A., & Bolhuis, J. (2021) · Scientific Reports · doi:10.1038/s41598-020-80726-y · Cited by 2 · see citing works
Human–Grey Parrot Comparisons in Cognitive Performance
Pepperberg, I. (2020) · The Cambridge Handbook of Evolutionary Perspectives on Human Behavior · doi:10.1017/9781108131797.002 · Cited by 2 · see citing works
Neuroendocrine regulation of vocalizations and other sounds in nonsongbirds
Tobiansky, D. J., & Fuxjager, M. J. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-815160-0.00019-0 · Cited by 2 · see citing works
Expanding the Scope of Cultural Linguistics: Taking Parrots Seriously
Frank, R. M. (2017) · Cultural linguistics · doi:10.1007/978-981-10-4056-6_24 · Cited by 2 · see citing works
Vocal sequences of diverse parrots suggest an important role for note repetitionPreprint
Dhati, A. M., Wewhare, N., Devasthale, N. S., Sundar, S., Parulekar, N., & Krishnan, A. (2025) · bioRxiv · doi:10.1101/2025.10.24.684295 · Cited by 1 · see citing works
“Many bird species learn song sequences at an early age, crystallizing them into a fixed pattern, whereas others learn and continuously modify their vocalizations throughout their lives (open-ended learning) (14,24,25).”
Dance behaviour in cockatoos: Implications for cognitive processes and welfare
Lubke, N., Held, S., Massaro, M., & Freire, R. (2025) · PLoS ONE · doi:10.1371/journal.pone.0328487 · Cited by 1 · see citing works
“The ability to dance in parrots may be related to their exceptional vocal learning [6] and vocal mimicry abilities [1,7].”
Watanabe, A., Kitahara, M., Sano, A., Satoh, R., Miyamoto, T., & Eda-Fujiwara, H. (2025) · Behavioural Processes · doi:10.1016/j.beproc.2025.105171 · Cited by 1
McLean, C. R., Mata, A., Kline, R. J., & Berg, K. S. (2024) · Journal of neuroendocrinology · doi:10.1111/jne.13365 · Cited by 1 · see citing works
Seki, Y. (2019) · Japanese Journal of Animal Psychology · doi:10.2502/janip.69.1.9 · Cited by 1 · see citing works
“…でもあった。この研究では,一定間隔で呈示される (LED の点灯と純音からなる)視聴覚メトロノー ム(450-1800ミリ秒までの範囲。セッション内で は固定の間隔;後に聴覚のみのメトロノームも使用) に応じてキーをつつくようトリを訓練した。次に, 数回連続してヒットする,つまり,一定間隔で呈示 される刺激に対し,その呈示ごとに一定のタイムウィ ンドウの範囲内で一度だけキーをつつき,それを繰 り返すようトリを訓練した。そして,そのつつきタ イミングを分析したところ,セキセイインコのつつ き運動は,個々の刺激に対する単なる個々の応答と して生じたものではなく,先に呈示された刺激から,…”
Eda-Fujiwara, H., & Tobari, Y. (2021) · doi:10.1016/b978-0-12-815160-0.00017-7 · Cited by 1
Parrots imitate song and dance with mixed vocal-gestural neural signals
Jones, C., Teoh, H. K., Carpenter, J., Roeser, A., Chen, R.-D., Kardon, B., Zhao, Z.-L., Cohen, I., & Goldberg, J. H. (2026) · bioRxiv · doi:10.64898/2026.10.21.760654
A sparse neural code for acoustic targets enables speech-like vocal flexibility in parrots
Zhao, Z.-L., Plump, A. N. D., Jones, C., Teoh, H. K., Kardon, B., & Goldberg, J. H. (2026) · bioRxiv · doi:10.64898/2026.10.21.760739
Blue-throated macaws ( Ara glaucogularis ) copy conspecifics in bidirectional control tasks
Haldar, E., Arun, D., & von Bayern, A. V. (2026) · Royal Society Open Science · doi:10.1098/rsos.251941
Principles of Brain Region Evolution: Insights from the Cerebellar Nuclei.
Anant, M., Faltine-Gonzalez, D., Lacava, S. A., & Kebschull, J. (2026) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-082625-101819
Moehn, K. M., Villalba, A., Abraham, A. C., Ulmer, K., Jawor, J., & Wright, T. (2026) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2026.114900
What imitating an iconic robot reveals on allospecific vocal imitation in parrots and starlings
Dam, N. C. P., Honing, H., & Spierings, M. (2025) · Scientific Reports · doi:10.1038/s41598-025-23444-7
Dam, N. C. P., Honing, H., & Spierings, M. (2024) · bioRxiv · doi:10.1101/2024.10.10.617563
“Amongst the parrots, the smaller brained budgerigars and cockatiels were more accurate at imitating both monophonic and multiphonic sounds than the larger brained parrots, contradictory to results from studies on variation in core and shell nuclei size (25).”
BackgroundResultInfluentialRole of von Economo and fork neurons in the evolution of vocal learning
Srivastava, S. (2023) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-022-01341-0
Hypotheses and Definitions in Language Evolution Research
Hartmann, S., Pleyer, M., Wacewicz, S., Benítez-Burraco, A., & Żywiczyński, P. (2021) · Biolinguistics · doi:10.5964/bioling.9191
Murdoch, D., Chen, R.-D., & Goldberg, J. H. (2017) · bioRxiv · doi:10.1101/236273
Boeckx, C. A. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-820584-6.00038-6
- Authors
- Chakraborty, M., Walløe, S., Nedergaard, S., Fridel, E. E., Dabelsteen, T., Pakkenberg, B., Bertelsen, M. F., Dorrestein, G. M., Brauth, S. E., Durand, S. E., & Jarvis, E. D.
- Affiliations
- Howard Hughes Medical Institute (US)
- University of Copenhagen (DK)
- Danish National Police (DK)
- Duke Medical Center (US)
- Bispebjerg Hospital (DK)
- Copenhagen Zoo (DK)
- University of Maryland, College Park (US)
- LaGuardia Community College (US)
- Corresponding author
- Chakraborty, Mukta
- Walløe, Solveig
- Nedergaard, Signe
- Fridel, Emma E.
- Dabelsteen, Torben
- Pakkenberg, Bente
- Bertelsen, Mads F.
- Dorrestein, Gerry M.
- Brauth, Steven E.
- Durand, Sarah E.
- Jarvis, Erich D.
- ORCID
- Venue
- PLOS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2015-06-24
- Volume
- 10
- Issue
- 6
- Pages
- e0118496
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC4479475
- OpenAlex
- W1598996539
- Cited by
- 86
- References
- 89
- Citations by year
- 2026: 8 · 2025: 9 · 2024: 8 · 2023: 6 · 2022: 6 · 2021: 15 · 2020: 9 · 2019: 4 · 2018: 6 · 2017: 3 · 2016: 9 · 2015: 2 · 2014: 1
- FWCI
- 5.80
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by)
- CUNY Academic Works (City University of New York) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- DukeSpace (Duke University) (submittedVersion, cc-by-nc-nd)
- Figshare (submittedVersion, cc-by)
- Funders
- Howard Hughes Medical Institute
- Danmarks Frie Forskningsfond
- National Institutes of Health
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Developmental Biology › Animal Vocal Communication and Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- vocal learning, vocal mimicry, budgerigars, avian brain evolution
- MeSH terms
- Animals, Brain, Humans, Learning, Music, New Zealand, Parrots, Vocalization, Animal
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