Time course of changes in Gambel's white-crowned sparrow song behavior following transitions in breeding condition - PubMed (original) (raw)
Time course of changes in Gambel's white-crowned sparrow song behavior following transitions in breeding condition
John Meitzen et al. Horm Behav. 2009 Jan.
Abstract
Seasonal changes in behavior and in its underlying neural substrate are common across animal taxa. These changes are often triggered by steroid sex hormones. Song in seasonally breeding songbirds provides an excellent example of this phenomenon. In these species, dramatic seasonal changes mediated by testosterone and its metabolites occur in adult song behavior and in the neural circuitry controlling song. While song rate can quickly change in response to seasonal breeding cues, it is unknown how quickly other aspects of song change, particularly the stereotypy of song phonology and syntax. In this study we determined whether and how quickly song rate, phonology, and syntax change in response to breeding and non-breeding physiological cues. We asked these questions using Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii), a closed-ended learner with well-characterized changes in the neural circuitry controlling song behavior. We exposed ten photosensitive sparrows to long-day photoperiod and implanted them with subcutaneous testosterone pellets (day 0) to simulate breeding conditions. We continuously recorded song and found that song rate increased quickly, reaching maximum around day 6. The stereotypy of song phonology changed more slowly, reaching maximum by day 10 or later. Song syntax changed minimally after day 6, the earliest time point examined. After 21 days, we transitioned five birds from breeding to non-breeding condition. Song rate declined precipitously. These results suggest that while song rate changes quickly, song phonology changes more slowly, generally following or in parallel with previously investigated changes in the neural substrate.
Figures
Figure 1
LD photoperiod and systemic T significantly increase song rate. Mean ± SEM is plotted. The number above each point indicates how many birds sang that day. The mean includes birds that did not sing. See Results for P values. A) The song rate of ten birds exposed to LD photoperiod and systemic T beginning on day 0. Song rates on day 2 through day 21 all significantly differed from day 0. Maximum average song rate was reached around day 6. B) The song rate of five birds in which systemic T was removed and photoperiod was decreased on day 21. Song rates on days 22 – 26 did not differ significantly when compared with day 0.
Figure 2
Representative songs from day 6 and 21 of LD photoperiod and systemic T treatment. Song from three different birds is shown (top, middle and bottom, respectively). Day 21 song is more stereotyped compared with day 6 song.
Figure 3
LD photoperiod and systemic T significantly increase song phonological stereotypy. Horizontal line indicates the mean. Different letters denote significant differences; groups with the same letter do not differ significantly (see Results for P values). A) % Similarity for songs recorded from within day 6, 8, 10 and 21 of LD photoperiod and systemic T treatment, calculated using Sound Analysis Pro. Higher percentage values indicate higher within-day stereotypy. B) Mean coefficient of variation (CV; SD/mean; higher CV indicates less stereotypy) of each bird’s song across days. C) Comparison of mean CV values for individual song attributes across days. Each point represents the mean CV of one of the 16 song characteristics measured across 10 birds.
Figure 4
LD photoperiod and systemic T significantly increased individual syllable phonological stereotypy. Each graph plots the mean CV per bird of one spectral syllable property across time. Horizontal line indicates the mean. Different letters denote significant differences; groups with the same letter do not significantly differ (see Results for P values). A) Whistle pitch. B) Whistle entropy. We note that entropy is negatively signed. C) Warble FM. D) Warble entropy. E) 1st buzz pitch. F) 2nd buzz entropy. G) 3rd buzz pitch goodness.
Figure 5
Buzz duration significantly increases in response to LD photoperiod and systemic T. Horizontal line indicates the mean. Different letters denote significant differences; groups with the same letter do not significantly differ (see Results for P values). A) Top: Example day 6 buzzes. Bottom: Example day 21 buzzes. All buzzes are from the same bird. B) Duration of first buzz. C) Duration of second buzz.
Figure 6
Song syntax changes minimally between days 6 and 21 of LD photoperiod and systemic T treatment. Horizontal line indicates the mean. Different letters denote significant differences; groups with the same letter do not significantly differ (see Results for P values). Lack of letters indicates no significant differences. A) Internal linearity (a measure of the number of transitions between syllables) B) Consistency (a measure of the number of song variations) C) The percentage of complete songs out of the total number of songs sung. D) The mean number of syllables produced per song, including both complete and incomplete song. E) The mean number of syllables sung per incomplete song significantly increases from day 6 compared with day 21. F) Song duration significantly increases from day six compared with day eight.
Similar articles
- Seasonal changes in song nuclei and song behavior in Gambel's white-crowned sparrows.
Smith GT, Brenowitz EA, Wingfield JC, Baptista LF. Smith GT, et al. J Neurobiol. 1995 Sep;28(1):114-25. doi: 10.1002/neu.480280110. J Neurobiol. 1995. PMID: 8586961 - Seasonal-like growth and regression of the avian song control system: neural and behavioral plasticity in adult male Gambel's white-crowned sparrows.
Meitzen J, Thompson CK. Meitzen J, et al. Gen Comp Endocrinol. 2008 Jul;157(3):259-65. doi: 10.1016/j.ygcen.2008.03.014. Epub 2008 Mar 25. Gen Comp Endocrinol. 2008. PMID: 18457836 Free PMC article. Review. - Plastic and stable electrophysiological properties of adult avian forebrain song-control neurons across changing breeding conditions.
Meitzen J, Weaver AL, Brenowitz EA, Perkel DJ. Meitzen J, et al. J Neurosci. 2009 May 20;29(20):6558-67. doi: 10.1523/JNEUROSCI.5571-08.2009. J Neurosci. 2009. PMID: 19458226 Free PMC article. - Peripheral auditory processing changes seasonally in Gambel's white-crowned sparrow.
Caras ML, Brenowitz E, Rubel EW. Caras ML, et al. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2010 Aug;196(8):581-99. doi: 10.1007/s00359-010-0545-1. Epub 2010 Jun 20. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2010. PMID: 20563817 Free PMC article. - Photoperiodic control of seasonality in birds.
Dawson A, King VM, Bentley GE, Ball GF. Dawson A, et al. J Biol Rhythms. 2001 Aug;16(4):365-80. doi: 10.1177/074873001129002079. J Biol Rhythms. 2001. PMID: 11506381 Review.
Cited by
- Adult neurogenesis is necessary for functional regeneration of a forebrain neural circuit.
Brenowitz EA, Lent KL, Miller KE, Perkel DJ. Brenowitz EA, et al. Proc Natl Acad Sci U S A. 2024 Jul 9;121(28):e2400596121. doi: 10.1073/pnas.2400596121. Epub 2024 Jul 5. Proc Natl Acad Sci U S A. 2024. PMID: 38968119 - Neuroendocrine patterns underlying seasonal song and year-round territoriality in male black redstarts.
Villavicencio CP, Windley H, D'Amelio PB, Gahr M, Goymann W, Quispe R. Villavicencio CP, et al. Front Zool. 2021 Feb 24;18(1):8. doi: 10.1186/s12983-021-00389-x. Front Zool. 2021. PMID: 33627161 Free PMC article. - Inflammation Induced by Natural Neuronal Death and LPS Regulates Neural Progenitor Cell Proliferation in the Healthy Adult Brain.
Larson TA, Tokareva Y, Cole MM, Brenowitz EA. Larson TA, et al. eNeuro. 2020 Jul 2;7(4):ENEURO.0023-20.2020. doi: 10.1523/ENEURO.0023-20.2020. Print 2020 Jul/Aug. eNeuro. 2020. PMID: 32424053 Free PMC article. - Neuroestrogen synthesis modifies neural representations of learned song without altering vocal imitation in developing songbirds.
Vahaba DM, Hecsh A, Remage-Healey L. Vahaba DM, et al. Sci Rep. 2020 Feb 27;10(1):3602. doi: 10.1038/s41598-020-60329-3. Sci Rep. 2020. PMID: 32108169 Free PMC article. - Brain-Derived Neurotrophic Factor Has a Transsynaptic Trophic Effect on Neural Activity in an Adult Forebrain Circuit.
Miller KE, Wood WE, Brenowitz EA, Perkel DJ. Miller KE, et al. J Neurosci. 2020 Feb 5;40(6):1226-1231. doi: 10.1523/JNEUROSCI.2375-19.2019. Epub 2019 Dec 19. J Neurosci. 2020. PMID: 31857358 Free PMC article.
References
- Austen MJW, Handford PT. Variation in the songs of breeding gambel’s white-crowned sparrows near Churchill, Manitoba. Condor. 1991;93:147–152.
- Ball GF. Pathways for hormonal influence of birdsong. In: Marler P, Slabbekoorn H, editors. Nature’s Music, The Science of Birdsong. San Diego: Elsevier; 2004.
- Ball GF, Auger CJ, Bernard DJ, Charlier TD, Sartor JJ, Riters LV, Balthazart J. Seasonal plasticity in the song control system: multiple brain sites of steroid hormone action and the importance of variation in song behavior. Ann N Y Acad Sci. 2004;1016:586–610. - PubMed
- Baptista LE. Geographic variation in song and dialects of the Puget Sound White-crowned Sparrow. Condor. 1977;79:356–370.
Publication types
MeSH terms
Substances
Grants and funding
- T32 GM007108/GM/NIGMS NIH HHS/United States
- R21 MH068530-02/MH/NIMH NIH HHS/United States
- R01 MH053032-14/MH/NIMH NIH HHS/United States
- MH068530/MH/NIMH NIH HHS/United States
- R21 MH068530/MH/NIMH NIH HHS/United States
- 5 T32 GM07108/GM/NIGMS NIH HHS/United States
- T32 GM007108-34/GM/NIGMS NIH HHS/United States
- MH53032/MH/NIMH NIH HHS/United States
- R01 MH053032/MH/NIMH NIH HHS/United States
LinkOut - more resources
Full Text Sources