Seasonal Activation and Inactivation of Song Motor Memories in Wild Canaries Is Not Reflected in Neuroanatomical Changes of Forebrain Song Areas

Seasonal, testosterone-dependent changes in sexual behaviors are common in male vertebrates. In songbirds such seasonal changes occur in a learned behavior--singing. Domesticated male canaries (Serinus canaria) appear to lose song units (syllables) after the breeding season and learn new ones until the next breeding season. Here we demonstrate in a longitudinal field study of individual, free-living nondomesticated (wild) canaries (S. canaria) a different mode of seasonal behavioral plasticity, seasonal activation, and inactivation of auditory-motor memories. The song repertoire composition of wild canaries changes seasonally: about 25% of the syllables are sung seasonally; the remainder occur year-round, despite seasonal changes in the temporal patterns of song. In the breeding season, males sing an increased number of fast frequency-modulated syllables, which are sexually attractive for females, in correlation with seasonally increased testosterone levels. About 50% of the syllables that were lost after one breeding season reappear in the following breeding season. Furthermore, some identical syllable sequences are reactivated on an annual basis. The seasonal plasticity in vocal behavior occurred despite the gross anatomical and ultrastructural stability of the forebrain song control areas HVc and RA that are involved in syllable motor control.

[1]  M. Konishi The role of auditory feedback in the control of vocalization in the white-crowned sparrow. , 1965, Zeitschrift fur Tierpsychologie.

[2]  J DeFelipe,et al.  A simple and reliable method for correlative light and electron microscopic studies. , 1993, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[3]  M. Kreutzer,et al.  Female canaries are sexually responsive to special song phrases , 1995, Animal Behaviour.

[4]  M. Gahr,et al.  Identification, distribution, and developmental changes of a melatonin binding site in the song control system of the zebra finch , 1996, The Journal of comparative neurology.

[5]  Eliot A. Brenowitz,et al.  Seasonal plasticity in the adult brain , 2000, Trends in Neurosciences.

[6]  E. Nordeen,et al.  Individual variation in neuron number predicts differences in the propensity for avian vocal imitation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[7]  R. Hartley,et al.  Left Syringeal Dominance in Testosterone-Treated Female Canaries , 1997, Neurobiology of Learning and Memory.

[8]  M. Gahr,et al.  Seasonal expression of androgen receptors, estrogen receptors, and aromatase in the canary brain in relation to circulating androgens and estrogens. , 2000, Journal of neurobiology.

[9]  F. Nottebohm A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. , 1981, Science.

[10]  F. Nottebohm,et al.  High-affinity androgen binding proteins in syringeal tissues of songbirds. , 1979, General and comparative endocrinology.

[11]  F. Nottebohm,et al.  Testosterone increases the recruitment and/or survival of new high vocal center neurons in adult female canaries. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[12]  E.C.L. Vu,et al.  Identification of a forebrain motor programming network for the learned song of zebra finches , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  H. Güttinger,et al.  Consequences of domestication on the song structures in the canary , 1985 .

[14]  C. Hegstrom,et al.  Seasonal plasticity of neuromuscular junctions in adult male Siberian hamsters (Phodopus sungorus) , 1999, Brain Research.

[15]  A. C. Yu,et al.  Temporal Hierarchical Control of Singing in Birds , 1996, Science.

[16]  A. Álvarez-Buylla,et al.  Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. , 1997, Journal of neurobiology.

[17]  R. Clower,et al.  Song-related brain regions in the red-winged blackbird are affected by sex and season but not repertoire size. , 1989, Journal of neurobiology.

[18]  B F O'Hara,et al.  Gene Expression in the Brain across the Hibernation Cycle , 1999, The Journal of Neuroscience.

[19]  M. Gahr,et al.  Delineation of a brain nucleus: Comparisons of cytochemical, hodological, and cytoarchitectural views of the song control nucleus HVC of the adult canary , 1990, The Journal of comparative neurology.

[20]  P. Marler Three models of song learning: evidence from behavior. , 1997, Journal of neurobiology.

[21]  F. Nottebohm,et al.  Birth of projection neurons in adult avian brain may be related to perceptual or motor learning. , 1990, Science.

[22]  F. Nottebohm,et al.  Production and survival of projection neurons in a forebrain vocal center of adult male canaries , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  F. Nottebohm,et al.  Cell death and neuronal recruitment in the high vocal center of adult male canaries are temporally related to changes in song. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[24]  F. Nottebohm,et al.  The life span of new neurons in a song control nucleus of the adult canary brain depends on time of year when these cells are born. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[25]  D. Kroodsma Reproductive Development in a Female Songbird: Differential Stimulation by Quality of Male Song , 1976, Science.

[26]  B. Mcewen,et al.  Sex and seasonal changes in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles , 1999, Neuroscience.

[27]  F. Nottebohm,et al.  Targeted Neuronal Death Affects Neuronal Replacement and Vocal Behavior in Adult Songbirds , 2000, Neuron.

[28]  S. Leitner,et al.  Breeding biology of the Island Canary Serinus canaria (Aves: Fringillidae) on the Desertas Island Ilhéu Chão , 1998 .

[29]  J. Wingfield,et al.  The determination of five steroids in avian plasma by radioimmunoassay and competitive protein-binding , 1975, Steroids.