Precise auditory–vocal mirroring in neurons for learned vocal communication
Abstract
Brain mechanisms for communication must establish a correspondence between sensory and motor codes used to represent the signal. One idea is that this correspondence is established at the level of single neurons that are active when the individual performs a particular gesture or observes a similar gesture performed by another individual. Although neurons that display a precise auditory-vocal correspondence could facilitate vocal communication, they have yet to be identified. Here we report that a certain class of neurons in the swamp sparrow forebrain displays a precise auditory-vocal correspondence. We show that these neurons respond in a temporally precise fashion to auditory presentation of certain note sequences in this songbird's repertoire and to similar note sequences in other birds' songs. These neurons display nearly identical patterns of activity when the bird sings the same sequence, and disrupting auditory feedback does not alter this singing-related activity, indicating it is motor in nature. Furthermore, these neurons innervate striatal structures important for song learning, raising the possibility that singing-related activity in these cells is compared to auditory feedback to guide vocal learning.
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The comparable latencies found for singing and passive listening imply that there is a delay function performed by a corollary discharge.
“The comparable latencies that were found for singing and passive listening imply that there is a delay function performed by a CD.”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [74]
Evidence for this corollary discharge function was recently found in neurons in the high vocal centre that fired with the same latency irrespective of whether the bird was actively singing or passively listening.
“Evidence for this CD function was recently found in neurons in the high vocal centre (HVC) that fired with the same latency irrespective of whether the bird was actively singing or passively listening74.”
From Corollary discharge across the animal kingdom (2008) · cites this paper as [74]
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“…singing finches, from regions analogous to the mammalian secondary auditory cortex, detect neurons that are similarly activated during singing and in response to song playback, consistent with their role in processing singing-related auditory feedback (Keller & Hahnloser 2009, Prather et al. 2008).”
BackgroundInfluentialSelf-citationIdentification of a motor-to-auditory pathway important for vocal learning
Roberts, T. F., Hisey, E. E., Tanaka, M., Kearney, M. G., Chattree, G., Yang, C. F., Shah, N. M., & MOONEY, R. D. (2017) · Nature Neuroscience · doi:10.1038/nn.4563 · Cited by 106 · see citing works
“Various findings indicate that HVC RA neurons are a source of premotor signals that contribute to song timing and that HVC X neurons convey song motor-related information to the basal ganglia 24,35–38 , 40 .”
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Rhythmic Continuous-Time Coding in the Songbird Analog of Vocal Motor Cortex
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“Both types of PNs generate sparse and brief (5- to 10-ms) bursts of spikes reliably active at one or a few times in the song, with different neurons active at different times (Fujimoto et al., 2011; Kozhevnikov and Fee, 2007; Long et al., 2010; Prather et al., 2008).”
BackgroundLong-range Order in Canary Song
Markowitz, J. E., Ivie, E. J., Kligler, L., & Gardner, T. J. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003052 · Cited by 99 · see citing works
“example, some species such as the swamp sparrow engage in antiphonal song type-matching—selecting a song that best matches what the neighbor just sang [18].”
BackgroundPepperberg, I. (2010) · Brain and Language · doi:10.1016/j.bandl.2009.11.002 · Cited by 89 · see citing works
“Interestingly, however, HVCx neurons (those proposed as possibly connected to an MN system) but not HVCRA neurons respond robustly to bird’s own song (Prather et al., 2008), and HVCx neurons may trigger LMAN activity through disinhibitory mechanisms (see Mooney, 2004; note Doupe et al., 2004).”
BackgroundCattaneo, L., Barchiesi, G., Tabarelli, D., Arfeller, C., Sato, M., & Glenberg, A. M. (2011) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsq099 · Cited by 99 · see citing works
“…has been identified in multimodal neurons called mirror neurons, that have now been recorded in humans (Mukamel et al., 2010), non-human primates (Gallese et al., 1996; Fogassi et al., 2005; Kraskov et al., 2009) and in non-mammalian vertebrates (Prather et al., 2008; Keller and Hahnloser, 2009).”
BackgroundNeural Mechanisms for the Coordination of Duet Singing in Wrens
Fortune, E. S., Carlos, R., Li, D., Ball, G. F., & Coleman, M. J. (2011) · Science · doi:10.1126/science.1209867 · Cited by 93 · see citing works
Evolution of mirror systems: a simple mechanism for complex cognitive functions
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Perspectives on observational learning in animals.
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The role of efference copy in striatal learning
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Representing actions through their sound
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“…(the caudal part of the ventral hyperstriatum, HVc) in swamp sparrows revealed that neurons whose frequency discharge increased during song production were the same as those whose frequency discharge increased when the birds heard a similar song produced by a conspecific (Prather et al. 2008).”
BackgroundMechanisms of social learning across species boundaries
Avarguès‐Weber, A., Dawson, E. H., & Chıttka, L. (2013) · Journal of Zoology · doi:10.1111/jzo.12015 · Cited by 86 · see citing works
“These neurons, described in primates and birds (Prather et al., 2008), not only fire for a particular movement performed by the animal (e.”
BackgroundSocial learning and culture in animals
van Schaik, C. P. (2010) · Springer eBooks · doi:10.1007/978-3-642-02624-9_20 · Cited by 86 · see citing works
“It is not clear how thecommunicative variants are learned socially, although vocal learning in birds is known to involve dedicated neural circuits (Prather et al. 2008).”
BackgroundShared song detector neurons in Drosophila male and female brains drive sex-specific behaviors
Deutsch, D., Clemens, J., Thiberge, S. Y., Guan, G., & Murthy, M. (2019) · Current Biology · doi:10.1016/j.cub.2019.08.008 · Cited by 67 · see citing works
Mirror neuron research: the past and the future
Ferrari, P. F., & Rizzolatti, G. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0169 · Cited by 85 · see citing works
“The work by Mooney and coworkers ([33], see also [34]) clearly demonstrates that, in songbirds, areas involved in song production and learning (i.”
BackgroundHeart rate modulation in bystanding geese watching social and non-social events
Wascher, C. A. F., Scheiber, I. B. R., & Kotrschal, K. M. (2008) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2008.0146 · Cited by 85 · see citing works
“This is the more plausible, as mirror neurons have recently been found in birds (Prather et al. 2008).”
BackgroundThrough the looking glass: Self and others
Sinigaglia, C., & Rizzolatti, G. (2011) · Consciousness and Cognition · doi:10.1016/j.concog.2010.11.012 · Cited by 84 · see citing works
Gale, S. D., & Perkel, D. J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3585-09.2010 · Cited by 81 · see citing works
“…singing-related activity of HVC neurons providing input to area X is not acutely affected by auditory-feedback perturbations, these same neurons are active during identical portions of BOS regardless of whether the bird is singing or hearing them (Kozhevnikov and Fee, 2007; Prather et al., 2008).”
BackgroundAuditory synapses to song premotor neurons are gated off during vocalization in zebra finches
Hamaguchi, K., Tschida, K., Yoon, I., Donald, B. R., & MOONEY, R. D. (2014) · eLife · doi:10.7554/elife.01833 · Cited by 81 · see citing works
“However, the singing-related action potential activity of HVCX cells does not change when auditory feedback is masked by noise bursts (Kozhevnikov and Fee, 2007; Prather et al., 2008).”
BackgroundInfluentialSelf-citationMaeda, K., Ishida, H., Nakajima, K., Inase, M., & Murata, A. (2014) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00742 · Cited by 80 · see citing works
“As such, mirror neurons likely play a role in acquiring motor skill (Cooper, Cook, Dickinson, & Heyes, 2013; Prather et al., 2008; Tchernichovski & Wallman, 2008).”
BackgroundInvestigation of musicality in birdsong
Rothenberg, D. J., Roeske, T. C., Voss, H. U., Naguib, M., & Tchernichovski, O. (2013) · Hearing Research · doi:10.1016/j.heares.2013.08.016 · Cited by 79 · see citing works
“It is the same neurons in the song system that can switch, within seconds, from premotor to auditory responses of very similar patterns (Prather et al., 2008).”
Remage‐Healey, L., & Joshi, N. R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1114-12.2012 · Cited by 79 · see citing works
“for song production and perception (Brenowitz, 1991; Gentner et al., 2000; Long and Fee, 2008; Prather et al., 2008).”
BackgroundInfluentialThe function and mechanism of vocal accommodation in humans and other primates
Ruch, H., Zürcher, Y., & Burkart, J. M. (2017) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12382 · Cited by 77 · see citing works
“The idea that vocal perception and production at least in part share the same neural system has been supported by work on both humans (Fadiga et al., 2002; Watkins, Strafella & Paus, 2003; D’Ausilio et al., 2014) and songbirds (Prather et al., 2008).”
BackgroundImitation as an inheritance system
Shea, N. J. (2009) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0061 · Cited by 79 · see citing works
Extending the mirror neuron system model, II: what did I just do? A new role for mirror neurons
Bonaiuto, J. J., & Arbib, M. A. (2010) · Biological Cybernetics · doi:10.1007/s00422-010-0371-0 · Cited by 77 · see citing works
“Aspects of such a system are seen in the song learning systems of some birds in which neurons fire during listening and producing songs (Prather et al. 2008).”
BackgroundKeshavan, M. S., Mehta, U. M., Padmanabhan, J. L., & Shah, J. L. (2015) · Development and Psychopathology · doi:10.1017/s095457941500019x · Cited by 76 · see citing works
Melissa Bateson, B., & Feenders, G. (2010) · ILAR Journal · doi:10.1093/ilar.51.4.394 · Cited by 73 · see citing works
Auditory–vocal mirroring in songbirds
MOONEY, R. D. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0179 · Cited by 72 · see citing works
“However, the singing-related activity of these cells is unperturbed by acoustic manipulations that disrupt auditory feedback, suggesting that HVCX cells switch from auditory to purely motor-related activity as the bird transitions from listening to singing [38,57].”
BackgroundMethodInfluentialSelf-citationHypothalamic neurons that mirror aggression
Yang, T., Bayless, D. W., Wei, Y., Landayan, D., Marcelo, I. M., Wang, Y., DeNardo, L. A., Luo, L., Druckmann, S., & Shah, N. M. (2023) · Cell · doi:10.1016/j.cell.2023.01.022 · Cited by 68 · see citing works
Osmanski, M. S., & Dooling, R. J. (2009) · The Journal of the Acoustical Society of America · doi:10.1121/1.3158928 · Cited by 67 · see citing works
Hidden neural states underlie canary song syntax
Cohen, Y., Shen, J., Semu, D., Leman, D. P., Liberti, W. A., Perkins, L. N., Liberti, D. C., Kotton, D. N., & Gardner, T. J. (2020) · Nature · doi:10.1038/s41586-020-2397-3 · Cited by 65 · see citing works
Hoffmann, S., Trost, L., Voigt, C., Leitner, S., Lemazina, A., Sagunsky, H., Abels, M., Kollmansperger, S., Maat, A. T., & Gahr, M. L. (2019) · Nature Communications · doi:10.1038/s41467-019-10593-3 · Cited by 65 · see citing works
Persistent Representation of Juvenile Experience in the Adult Songbird Brain
Prather, J. F., Peters, S. S., Nowicki, S., & MOONEY, R. D. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.6042-09.2010 · Cited by 64 · see citing works
“We examined the auditory responses of HVC neurons in our laboratory-raised birds to determine whether those cells expressed stronger responses to songs in the bird’s adult repertoire than to other swamp sparrow songs, as reported for wild sparrows (Margoliash and Konishi, 1985; Margoliash, 1986; Mooney et al., 2001; P…”
BackgroundMethodResultInfluentialSelf-citationPerceptuomotor compatibility effects in speech
Galantucci, B., Fowler, C. A., & Goldstein, L. M. (2009) · Attention Perception & Psychophysics · doi:10.3758/app.71.5.1138 · Cited by 64 · see citing works
“In birds, Prather, Peters, Nowicki, and Mooney (2008) demonstrated that mirror-like neurons in the higher vocal center of swamp sparrows display nearly identical patterns of activity when the bird either hears a birdsong or sings it in the absence of auditory feedback.”
BackgroundMethodSocial calls provide novel insights into the evolution of vocal learning
Sewall, K. B., Young, A. M., & Wright, T. F. (2016) · Animal Behaviour · doi:10.1016/j.anbehav.2016.07.031 · Cited by 60 · see citing works
Songbirds work around computational complexity by learning song vocabulary independently of sequence
Lipkind, D., Zai, A. T., Hanuschkin, A., Marcus, G., Tchernichovski, O., & Hahnloser, R. H. R. (2017) · Nature Communications · doi:10.1038/s41467-017-01436-0 · Cited by 59 · see citing works
Sleep, off-line processing, and vocal learning
Margoliash, D., & Schmidt, M. F. (2010) · Brain and Language · doi:10.1016/j.bandl.2009.09.005 · Cited by 105 · see citing works
“Although beyond the scope of this review, such mirror neurons have also been observed in songbirds (Prather et al., 2008).”
BackgroundEvidence for a causal inverse model in an avian cortico-basal ganglia circuit
Giret, N., Kornfeld, J. M. R., Ganguli, S., & Hahnloser, R. H. R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1317087111 · Cited by 59 · see citing works
“The premotor area HVC is involved in generating the stereotyped song motifs of adult birds (13), whereas the lateral magnocellular nucleus of the anterior nidopallium (LMAN) forms the output of a basal-ganglia pathway involved in generating subtle song variability (14–17).”
BackgroundResultInfluentialThe origins of vocal learning: New sounds, new circuits, new cells
Nottebohm, F., & Liu, W. (2010) · Brain and Language · doi:10.1016/j.bandl.2010.05.002 · Cited by 58 · see citing works
Neural Mechanisms of Communication
Sliwa, J., Takahashi, D. Y., & Shepherd, S. V. (2016) · Wiley eBooks · doi:10.1002/9781118316757.ch16 · Cited by 58 · see citing works
Test of a motor theory of long-term auditory memory
Schulze, K., Vargha‐Khadem, F., & Mishkin, M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1204717109 · Cited by 56 · see citing works
Tschida, K., & MOONEY, R. D. (2012) · Neuron · doi:10.1016/j.neuron.2011.12.038 · Cited by 56 · see citing works
“…electrophysiological recordings failed to detect feedback-driven changes in the singing-related activity of HVC X neurons (Kozhevnikov and Fee, 2007; Prather et al., 2008), in vivo imaging permitted detection of subtle changes in HVC X dendritic spines within the first few days of deafening.”
Self-citationYildiz, I. B., von Kriegstein, K., & Kiebel, S. J. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003219 · Cited by 55 · see citing works
“Much more is known experimentally about the exact neuronal mechanisms in songbirds than in humans, due to detailed electrophysiological studies which have shown that songbirds use a sequence of auditory dynamics to generate and recognize song in a highly effective manner [6,13].”
BackgroundAudio–vocal system regulation in children with autism spectrum disorders
Russo‐Ponsaran, N. M., Larson, C. R., & Kraus, N. (2008) · Experimental Brain Research · doi:10.1007/s00221-008-1348-2 · Cited by 55 · see citing works
“A noteworthy model of audio–vocal interaction derives from birdsong literature (Margoliash 2002; Prather et al. 2008).”
BackgroundThe Neural Basis of Vocal Pitch Imitation in Humans
Belyk, M., Pfordresher, P. Q., Mario Liotti, A., & Brown, S. (2015) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00914 · Cited by 55 · see citing works
Local and system mechanisms for action execution and observation in parietal and premotor cortices
Ferroni, C. G., Albertini, D., Lanzilotto, M., Livi, A., Maranesi, M., & Bonini, L. (2021) · Current Biology · doi:10.1016/j.cub.2021.04.034 · Cited by 54 · see citing works
“76 This mechanism has been shown to be optimized for shaping so-cialresponses and mayalsocontributetothe previouslyobserved overall suppression of discharge of pyramidal (especially cortico-spinal) neurons during action observation.”
BackgroundNeural Correlates of Intentional Communication
Noordzij, M. L., Newman-Norlund, S. E., de Ruiter, J. P., Peter Hagoort, A., Levinson, S. C., & Toni, I. (2010) · Frontiers in Neuroscience · doi:10.3389/fnins.2010.00188 · Cited by 54 · see citing works
“This communicative phenomenon is widespread in the animal world (Bargh et al., 1996; Dyer, 2002; Hauser, 1996; Mather, 2004), and it could be supported by “mirror” neurons that couple perceived and executed behaviors (Prather et al., 2008).”
InfluentialBrains for birds and babies: Neural parallels between birdsong and speech acquisition
Prather, J., Okanoya, K., & Bolhuis, J. (2017) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.12.035 · Cited by 49 · see citing works
“Because these neurons continue to fire during singing even when auditory feedback is distorted (Kozhevnikov and Fee, 2007; Prather, 2013; Prather et al., 2008), the activity of these neurons is thought to be related to the motor performance of song.”
InfluentialSelf-citationVocal learning: a language-relevant trait in need of a broad cross-species approach
Lattenkamp, E. Z., & Vernes, S. C. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.04.007 · Cited by 54 · see citing works
Understanding ‘what’ others do: mirror mechanisms play a crucial role in action perception
Avenanti, A., & Urgesi, C. (2011) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsr004 · Cited by 53 · see citing works
“In the last two decades, neuroscientific research has demonstrated that humans (Mukamel et al., 2010), non-human primates (Rizzolatti and Craighero, 2004) and birds (Prather et al., 2008) are equipped with a particular class of multimodal neurons active during action execution and action perception.”
Background
- Authors
- Prather, J. F., Peters, S., Nowicki, S., & Mooney, R.
- Affiliations
- Duke Medical Center (US)
- Duke University (US)
- Corresponding author
- Mooney, R.
- Venue
- Nature
- Published
- 2008-01
- Volume
- 451
- Issue
- 7176
- Pages
- 305-310
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2009465679
- Cited by
- 463
- References
- 44
- Citations by year
- 2026: 5 · 2025: 13 · 2024: 16 · 2023: 24 · 2022: 19 · 2021: 16 · 2020: 49 · 2019: 16 · 2018: 19 · 2017: 23 · 2016: 16 · 2015: 23 · 2014: 31 · 2013: 38 · 2012: 30
- FWCI
- 31.39
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institutes of Health
- National Institute on Deafness and Other Communication Disorders
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Developmental Biology › Animal Vocal Communication and Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
- Keywords
- mirror neurons, vocal learning, songbirds, swamp sparrow, auditory feedback, song learning, striatum, vocal communication
- MeSH terms
- Acoustic Stimulation, Action Potentials, Animals, Auditory Perception, Electrophysiology, Imitative Behavior, Learning, Male, Neurons, Vocalization, Animal, Finches, Sparrows, High Vocal Center
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