Context-dependent activation of a social behavior brain network during learned vocal production
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Abstract
Neural activation in brain regions for vocal control is social context dependent. This context-dependent brain activation reflects social context-appropriate vocal behavior but has unresolved mechanisms. Studies of non-vocal social behaviors in multiple organisms suggest a functional role for several evolutionarily conserved and highly interconnected brain regions. Here, we use neural activity-dependent gene expression to evaluate the functional connectivity of this social behavior network within zebra finches in non-social and social singing contexts. We found that activity in one social behavior network region, the medial preoptic area (POM), was strongly associated with the amount of non-social undirected singing in zebra finches. In addition, in all regions of the social behavior network and the paraventricular nucleus (PVN), a higher percentage of EGR1 expression was observed during a social female-directed singing context compared to a non-social undirected singing context. Furthermore, we observed distinct patterns of significantly correlated activity between regions of the social behavior network during non-social undirected and social female-directed singing. Our results suggest that non-social vs. social contexts differentially activate this social behavior network and PVN. Moreover, neuronal activity within this social behavior network, PVN, and POM may alter context-appropriate vocal production.
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In adult male zebra finches, social singing contexts revealed upregulation of the mRNA expression of the neuronal activation marker Egr1 in various brain areas including the PVN.
“Another recent study assessed activation patterns in the social behaviour network (O ' Connell and Hofmann, 2012) during social singing contexts in adult male zebra finches, revealing upregulation of the mRNA expression of the neuronal activation marker Egr1 in various brain areas including the PVN (Anderson et al., 2023).”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Anderson et al., 2023
The Introduction reports upregulation of EGR1 mRNA in several regions, including the PVN, during social singing in adult male zebra finches. The Results qualify this finding: the increase was observed after normalizing expression to singing rate; they found no significant difference in unnormalized expression between social and non-social contexts. The citing sentence omits that important qualification. (LLM, conf=0.86)
Experimental — accuracy not yet measuredCollectively, studies in zebra finches, butterflyfishes, and other species emphasize the significance of the interplay between OXT and DA and their combined impact on pair bonding, extending beyond the context of humans and rodents.
“Collectively, these studies (Anderson et al., 2023; Day et al., 2019; Nowicki et al., 2020) emphasize the significance of the interplay between OXT and DA and their combined impact on pair bonding, extending beyond the context of humans and rodents.”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Anderson et al., 2023
The Abstract and Introduction propose an oxytocin–dopamine pathway in male zebra finches, and the Discussion reports neural activity associated with social versus non-social singing. The paper presents that pathway as a hypothesis about vocal behavior, not as evidence that oxytocin and dopamine jointly affect pair bonding. (LLM, conf=0.88)
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Ntamati, N. R., Creed, M. C., Achargui, R., & Lüscher, C. (2018) · PLoS ONE · doi:10.1371/journal.pone.0190297 · Cited by 38 · see citing works
A minimally invasive procedure for sexing young zebra finches
Soderstrom, K., Qin, W., & Leggett, M. H. (2007) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2007.04.007 · Cited by 37 · cited 3× · see citing works
“The sex of the birds as juveniles was determined using standard PCR (Soderstrom et al.”
MethodInfluentialİyilikci, O., Balthazart, J., & Ball, G. F. (2016) · eNeuro · doi:10.1523/eneuro.0283-16.2016 · Cited by 33 · see citing works
Shimogawa, Y., Sakuma, Y., & Yamanouchi, K. (2014) · Neuroscience Research · doi:10.1016/j.neures.2014.10.016 · Cited by 31 · see citing works
Kabelik, D., Weitekamp, C. A., Choudhury, S. C., Hartline, J. T., Smith, A. N., & Hofmann, H. A. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.06.013 · Cited by 31 · cited 2× · see citing works
“2008), reptiles (Sakata et al. 2000; Sakata and Crews 2004; Kabelik et al. 2018), fish (Goodson and Bass 2002), and birds (Edwards et al.”
BackgroundKwong-Brown, U., Tobias, M. L., Elias, D. O., Hall, I. C., Elemans, C. P. H., & Kelley, D. B. (2019) · eLife · doi:10.7554/elife.39946 · Cited by 31 · see citing works
Hypothalamic Neuroanatomy: Steroid Hormone Binding and Patterns of Axonal Projections
Pfaff, D. W., & Conrad, L. C. A. (1978) · International review of cytology · doi:10.1016/s0074-7696(08)60170-9 · Cited by 30 · see citing works
Neural Circuits Underlying Nest Building in Male Zebra Finches
Edwards, S. C., Hall, Z. J., Ihalainen, E., Bishop, V. R., Nicklas, E. T., Healy, S. D., & Meddle, S. (2020) · Integrative and Comparative Biology · doi:10.1093/icb/icaa108 · Cited by 27 · see citing works
Prior, N. H., Bentz, E. J., & Ophir, A. G. (2021) · Genes Brain & Behavior · doi:10.1111/gbb.12781 · Cited by 27 · see citing works
A consideration of brain networks modulating social behavior
Kelly, A. M. (2022) · Hormones and Behavior · doi:10.1016/j.yhbeh.2022.105138 · Cited by 24 · cited 1× · see citing works
“Although the potential integration of the social behavior network into other defined neural systems is not well established (Kelly 2022), the involvement of this network in motivating the context-appropriate performance of learned behaviors is highly plausible.”
Gene expression in the social behavior network of the wire‐tailed manakin ( Pipra filicauda ) brain
Horton, B. M., Ryder, T. B., Moore, I. T., & Balakrishnan, C. N. (2019) · Genes Brain & Behavior · doi:10.1111/gbb.12560 · Cited by 18 · see citing works
Avian models for brain mechanisms underlying altered social behavior in autism
Csillag, A., Ádám, Á., & Zachár, G. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.1032046 · Cited by 17 · cited 1× · see citing works
“Multiple bird species are inherently social (Csillag et al. 2022), and songbirds, such as the zebra finch, can identify conspecific individuals based on unique vocal signatures (Elie and Theunissen 2018).”
Sakata, J. T., & Crews, D. P. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.4.857 · Cited by 15 · cited 2× · see citing works
“2008), reptiles (Sakata et al. 2000; Sakata and Crews 2004; Kabelik et al. 2018), fish (Goodson and Bass 2002), and birds (Edwards et al.”
Convergent and divergent neural circuit architectures that support acoustic communication
Kelley, D. B. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.976789 · Cited by 14 · cited 1× · see citing works
“Moreover, research on social vocal behavior has revealed both the convergence and divergence of brain circuits for vocal production (Jarvis 2019; Kelley 2022).”
Dopamine physiology in the basal ganglia of male zebra finches during social stimulation
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Early onset of postnatal individual vocal recognition in a highly colonial mammal species
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“In other species, such as seals, where rapid mother-young social recognition is crucial for offspring survival, postnatal individual vocal recognition can occur within hours (Martin et al. 2022).”
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Rappeneau, V., & Castillo Díaz, F. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105675 · Cited by 51 · see citing works
“…activation patterns in the social behaviour network (O ’ Connell and Hofmann, 2012) during social singing contexts in adult male zebra finches, revealing upregulation of the mRNA expression of the neuronal activation marker Egr1 in various brain areas including the PVN (Anderson et al., 2023).”
BackgroundGonzález-Usigli, H., Ortíz, G. G., Charles‐Niño, C., Mireles-Ramírez, M. A., Pacheco-Moisés, F. P., Torres-Mendoza, B. M., Hernández-Cruz, J. J., Delgado-Lara, D. L. C., & Ramírez-Jirano, L. J. (2023) · Brain Sciences · doi:10.3390/brainsci13030508 · Cited by 27 · see citing works
Savoy, A., Anderson, K. L., & Gogola, J. V. (2024) · BMC Neuroscience · doi:10.1186/s12868-024-00919-3 · Cited by 4 · see citing works
Hutchens, S., Khurram, I., & Hurley, L. M. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1446866 · Cited by 1 · see citing works
Integrative neural mechanisms for social communication of learned vocal behavior
Anderson, K. L., & Whitney, O. (2025) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2025.1650323 · Cited by 1 · see citing works
“For example, inhibition of the auditory system using GABA receptor agonist diminishes sound-triggered activation of the lateral VMH of the social behavior network (Spool et al., 2024).”
InfluentialOcytocine versus dopamine : l’équilibre délicat entre lien social et addiction
Rappeneau, V., & Díaz, F. C. (2025) · Biologie Aujourd hui · doi:10.1051/jbio/2025012
- Authors
- Anderson, K. L., Colón, L., Doolittle, V., Rosario Martinez, R., Uraga, J., & Whitney, O.
- Affiliations
- The Graduate Center, CUNY (US)
- City College of New York (US)
- Corresponding author
- Whitney, Osceola
- Venue
- Brain Structure and Function
- Published
- 2023-08-24
- Volume
- 228
- Issue
- 7
- Pages
- 1785-1797
- ISSN
- 1863-2653 (ISSN-L)
- 1863-2661
- PMC
- PMC9949236
- OpenAlex
- W4386116836
- Cited by
- 6
- References
- 101
- Citations by year
- 2025: 2 · 2024: 3 · 2023: 1
- FWCI
- 1.48
- Type
- journal article
- Language
- en
- Open access
- green
- dx.doi.org
- Licence
- Locations
- Brain Structure and Function (publishedVersion)
- Research Square (acceptedVersion, cc-by)
- PubMed (publishedVersion)
- PubMed Central (submittedVersion, cc-by)
- Funders
- G-RISE (5T32GM136499-02)
- James Bruce Llewelyn Fellowship
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Developmental Biology › Animal Vocal Communication and Behavior
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- zebra finch, social behavior network, medial preoptic area, paraventricular nucleus, functional connectivity
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
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