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Plasticity in Adult Avian Central Nervous System: Possible Relation Between Hormones, Learning, and Brain Repair

Fernando Nottebohm

10.1002/cphy.cp010503

Source: Supplement 5: Handbook of Physiology, The Nervous System, Higher Functions of the Brain

Originally published: 1987

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Description of Song
2 Song Learning in Birds
3 Temporal Constraints on Learning: Possible Role for Hormones
4 Hypoglossal Dominance: Animal Example of Handedness
5 Central Pathways for Song Control
6 Hemispheric Dominance and its Reversal
7 Sexual Dimorphism in Brain Anatomy and Function
8 Ontogeny of a Sexual Dimorphism: Early Hormonal Effects
9 Peripheral Effects of Testosterone
10 Testosterone Induces Dendritic Growth and Synaptogenesis in Adulthood
11 Space for Learned Skill
12 Seasonal Effects on Male Central Pathways for Song Control
13 Neurogenesis in Adulthood
14 Neuronal Replacement
15 Significance of Neuronal Replacement
16 Conclusion
Figure 1. Figure 1.

Sound spectrograph of fragment of adult male canary song showing 3 different syllable types. Repetition of same syllable forms phrase. Syllables are composed of 1 or more elements, preceded by silent gap. Each element is represented by a fundamental frequency and 1 or more harmonics. Calibration bar, 0.5 s.

From Nottebohm and Nottebohm 104.
Figure 2. Figure 2.

Monthly changes in blood testosterone levels and song. A: blood testosterone (T) levels in monthly samples from a group of 6 adult male canaries. First sample was taken in May when birds were 12 mo; last sample was taken the following May when birds were 24 mo. Vertical bars, SE. B: mean size of song repertoires measured in numbers of syllables from recordings obtained from same birds as in A. Mean size of song repertoire shows 2 significant increases: during September/October and during March. C: mean number of new syllable types produced each month by same birds shows waves of new syllable addition with peaks in September and March. Net increase in total syllable numbers is smaller than addition of new syllables because some older syllables are lost. Periods of enhanced song learning seem to be preceded by drop in blood testosterone levels. (F. Nottebohm, M. E. Nottebohm, L. Crane, and J. C. Wingfield, unpublished observations).
Figure 3. Figure 3.

A: ventral view of larynx, trachea, and bronchi of adult canary. Vocal organ, or syrinx, has its own complement of muscles and is surrounded by interclavicular air sac (icas), which is part of respiratory system. Branch of hypoglossal nerve (XII), cervicalis descendens inferior (cds) or tracheosyringealis, innervates muscles of ipsilateral syringeal half. Recurrens branch of vagus nerve (RX) innervates nearby crop (not shown). bd, Bronchidesmus; ca, cerivcalis ascendens branch of XII nerve; gcs, cervical superior and gp, petrosum ganglia of IX nerve; h′, h″, hypoglossal and c, cervical roots of XII nerve; m st tr, sternotrachealis muscle; m tr I, tracheolateralis muscle. B: longitudinal section through syrinx. Left muscle mass is heavier than its right counterpart. Sound production is thought to result from periodic interruptions of airflow during expiration as internal tympaniform membrane (ti) oscillates in and out of bronchial lumen, possibly locked in step with local air turbulence. Bronchidesmal membrane anchors medial wall of bronchi to dorsal wall of interclavicular air sac. T, tympanum; b1, b2, and b3, bronchial half rings; LB, left bronchus; RB, right bronchus; le, labium externum; pe, pessulus; sl, semilunar membrane; M, intrinsic syringeal muscles.

From Nottebohm and Nottebohm 104.
Figure 4. Figure 4.

Two adult male canaries recorded while producing stable, adult song (trace A). Subsequently bird 1 had its right syringeal half denervated and bird 15 had its left syringeal half denervated (trace B). Song of bird 1 remained unaltered; postoperative song of bird 15 suffered loss of most syllable types, which were replaced by silent gaps, clicks, and other modified sounds.

From Nottebohm and Nottebohm 104.
Figure 5. Figure 5.

Schematic sagittal view of brain of adult male canary. Field L, highest forebrain auditory projection sends fibers that appose ventrally to nucleus hyperstriatum ventralis pars caudalis (HVc); HVc projects to nucleus robustus archistrialis (RA), which sends direct pathway to motoneurons of nucleus nervi hypoglossi (nXIIts) that innervate muscles of syrinx. All projections are ipsilateral. Distance from rostral to caudal end of brain, 13 mm. Cb, cerebellum.
Figure 6. Figure 6.

Two adult male canaries recorded while producing stable, adult song (trace A). Subsequently bird 54 had its right HVc lesioned and bird 97 had its left HVc lesioned. Both lesions were complete, resulting in elimination of HVc on one side (trace B). Song of bird 54 became unstable after the lesion, with intrusion of other independent sounds; syllable and phrase structure otherwise remained recognizable. Postoperative song of bird 97 lost virtually all of its preoperative syllable and phrase structure.

From Nottebohm et al. 106.
Figure 7. Figure 7.

Typical type IV RA cells of female (top) and male (bottom) canaries shown from behind, with reference to midline (M) and lateral (L) edge of brain. Same cells are then turned 90° and viewed from side, with reference to anterior (A) and posterior (P) end of brain. Dendritic trees were drawn with a motor‐driven microscope stage yoked to a computer, which allowed a complete threedimensional reconstruction of dendrites and their relative positions. Dotted lines, boundaries between contiguous 100 μm‐thick tissue sections used for reconstruction. Dorsal (D) and ventral (V) coordinates are same for 2 views of same cell. Male dendrites reach farther away from soma than do female dendrites.

From De Voogd and Nottebohm 31.
Figure 8. Figure 8.

Normal song development in male canaries, kept under photoperiod conditions of New York state, shown as horizontal progression from subsong (SS) to plastic song (PS) to full song (FS). FS is stable song that adult canaries sing during breeding season. At end of breeding season PS recurs. HVc volume grows during the time song is first acquired and shrinks to that of 3‐ to 4‐mo‐old canary in late summer after breeding season is over and song becomes plastic again. Vertical axis, volume of nucleus HVc ± 1 SD. Open circles, samples of 4 birds killed at age shown on horizontal axis; filled circles, samples of 9 and 12 birds killed at 12 and 17 mo, respectively; open diamonds, samples of 10, 9, and 8 birds killed at end of their 1st, 2nd, and 3rd breeding seasons, respectively.
Figure 9. Figure 9.

Sound spectrographs of 3 recordings from same bird. A: plastic song when bird was 4 mo old. B: plastic song produced in late summer (September) after end of its 1st breeding season. C: stable song during preceding May when bird was 12 mo old and in full reproductive condition. In A and B song syllables are repeated in wavering, unstable fashion; in C syllables are virtual carbon copies of each other. Calibration bar, 0.5 s.
Figure 10. Figure 10.

Camera lucida tracing of dendritic and axonal processes of HVc cell labeled with horseradish peroxidase andthymidine. Heavy lines, dendrites; light lines, axons. Boundaries of HVc: solid line, ventricle; broken line, fibrous lamina. Calibration bar, 100 μm. D and M, dorsal and medial reaches of the brain. [From Paton and Nottebohm 111. Copyright 1984 by the American Association for the Advancement of Science.]

3H
Figure 11. Figure 11.

Anatomy of HVc cell bodies labeled with horseradish peroxidase and (3H)thymidine. Seperate photographs were taken of same field but were focused first at level of cell itself (A and C) and then at level of exposed silver grains in layer of emulsion above cell (B and D). A and B, same cell; C and D, same cell. Calibration bar, 10 μm. (From Paton and Nottebohm 111. Copyright 1984 by the American Association for the Advancement of Science.)
Figure 12. Figure 12.

1–3: Distribution of labeled cells in same frontal brain section from an adult female canary killed 26 days after last of series of 28 injections of (3H)thymidine spaced 12 h apart. Each dot corresponds to a labeled cell; HVc is demarcated by broken line curving under lateral ventricle (V) of forebrain. 1: Labeled neurons. 2: Labeled glia. 3: Labeled endothelial cells. 4: Rostral section of same brain showing distribution of labeled neurons. 5: Caudal section of same brain showing distribution of labeled neurons. 6: Frontal section of brain taken at the level of nucleus HVc from adult female canary killed 52 days after last of series of 28 injections of (3H)thymidine spaced 12 h apart. Each dot corresponds to a labeled neuron. Incubation period for autoradiography was 4 wk. Criterion for recognizing a labeled cell was 5 times background for all sections except 6, for which it was 10 times background. Using either criterion, there are many labeled neurons throughout forebrain (with exception of archistriatum) but very few, or none, outside forebrain. Sagittal view of brain (inset, lower left) shows level at which the 4 different sections were taken. A, archistriatum; APH, area parahippocampalis; Aq, aqueduct; Cb, cerebellum; FA, tractus frontoarchistriatalis; FLM, fasciculus longitudinalis medialis; HA, hyperstriatum accessorium; Hab, habenula; HD, hyperstriatum dorsalis; HP, hippocampus; HV, hyperstriatum ventralis; IM, nucleus isthmi pars magnocellularis; IPC, nucleus isthmi pars parvocellularis; LMD, lamina medullaris dorsalis; LPO, lobus parolfactorius; MLd, nucleus mesencephalicus lateralis pars dorsalis; N, neostriatum; NC, neostriatum caudalis; OM, tractus occipitomesencephalicus; PA, paleostriatum augmentatum; Pt, nucleus pretectalis; RA, nucleus robustus archistriatalis; SPM, nucleus spiriformis medialis; TPC, nucleus tegmenti pedunculopontinus pars compacta. Calibration bar, 1 mm.
Figure 13. Figure 13.

Histograms showing relative frequency with which various numbers of exposed silver grains occurred over nuclei of 100 labeled neurons (A), 100 labeled glia (B), and 100 labeled endothelial cells (C) taken from HVc and underlying neotriatum following systemic treatment with (3H)thymidine (see Fig. 12); this bird was killed 26 days after last (3H)thymidine injection. Brain sections were incubated for autoradiography for only 10 days and showed very low background labeling. As a result, criterion for accepting cell as labeled was only 3 exposed silver grains per nucleus, which corresponded to 10 times background label for area of similar size. Short incubation permitted counting all exposed silver grains, even over those nuclei that showed the heaviest concentration of label.


Figure 1.

Sound spectrograph of fragment of adult male canary song showing 3 different syllable types. Repetition of same syllable forms phrase. Syllables are composed of 1 or more elements, preceded by silent gap. Each element is represented by a fundamental frequency and 1 or more harmonics. Calibration bar, 0.5 s.

From Nottebohm and Nottebohm 104.


Figure 2.

Monthly changes in blood testosterone levels and song. A: blood testosterone (T) levels in monthly samples from a group of 6 adult male canaries. First sample was taken in May when birds were 12 mo; last sample was taken the following May when birds were 24 mo. Vertical bars, SE. B: mean size of song repertoires measured in numbers of syllables from recordings obtained from same birds as in A. Mean size of song repertoire shows 2 significant increases: during September/October and during March. C: mean number of new syllable types produced each month by same birds shows waves of new syllable addition with peaks in September and March. Net increase in total syllable numbers is smaller than addition of new syllables because some older syllables are lost. Periods of enhanced song learning seem to be preceded by drop in blood testosterone levels. (F. Nottebohm, M. E. Nottebohm, L. Crane, and J. C. Wingfield, unpublished observations).



Figure 3.

A: ventral view of larynx, trachea, and bronchi of adult canary. Vocal organ, or syrinx, has its own complement of muscles and is surrounded by interclavicular air sac (icas), which is part of respiratory system. Branch of hypoglossal nerve (XII), cervicalis descendens inferior (cds) or tracheosyringealis, innervates muscles of ipsilateral syringeal half. Recurrens branch of vagus nerve (RX) innervates nearby crop (not shown). bd, Bronchidesmus; ca, cerivcalis ascendens branch of XII nerve; gcs, cervical superior and gp, petrosum ganglia of IX nerve; h′, h″, hypoglossal and c, cervical roots of XII nerve; m st tr, sternotrachealis muscle; m tr I, tracheolateralis muscle. B: longitudinal section through syrinx. Left muscle mass is heavier than its right counterpart. Sound production is thought to result from periodic interruptions of airflow during expiration as internal tympaniform membrane (ti) oscillates in and out of bronchial lumen, possibly locked in step with local air turbulence. Bronchidesmal membrane anchors medial wall of bronchi to dorsal wall of interclavicular air sac. T, tympanum; b1, b2, and b3, bronchial half rings; LB, left bronchus; RB, right bronchus; le, labium externum; pe, pessulus; sl, semilunar membrane; M, intrinsic syringeal muscles.

From Nottebohm and Nottebohm 104.


Figure 4.

Two adult male canaries recorded while producing stable, adult song (trace A). Subsequently bird 1 had its right syringeal half denervated and bird 15 had its left syringeal half denervated (trace B). Song of bird 1 remained unaltered; postoperative song of bird 15 suffered loss of most syllable types, which were replaced by silent gaps, clicks, and other modified sounds.

From Nottebohm and Nottebohm 104.


Figure 5.

Schematic sagittal view of brain of adult male canary. Field L, highest forebrain auditory projection sends fibers that appose ventrally to nucleus hyperstriatum ventralis pars caudalis (HVc); HVc projects to nucleus robustus archistrialis (RA), which sends direct pathway to motoneurons of nucleus nervi hypoglossi (nXIIts) that innervate muscles of syrinx. All projections are ipsilateral. Distance from rostral to caudal end of brain, 13 mm. Cb, cerebellum.



Figure 6.

Two adult male canaries recorded while producing stable, adult song (trace A). Subsequently bird 54 had its right HVc lesioned and bird 97 had its left HVc lesioned. Both lesions were complete, resulting in elimination of HVc on one side (trace B). Song of bird 54 became unstable after the lesion, with intrusion of other independent sounds; syllable and phrase structure otherwise remained recognizable. Postoperative song of bird 97 lost virtually all of its preoperative syllable and phrase structure.

From Nottebohm et al. 106.


Figure 7.

Typical type IV RA cells of female (top) and male (bottom) canaries shown from behind, with reference to midline (M) and lateral (L) edge of brain. Same cells are then turned 90° and viewed from side, with reference to anterior (A) and posterior (P) end of brain. Dendritic trees were drawn with a motor‐driven microscope stage yoked to a computer, which allowed a complete threedimensional reconstruction of dendrites and their relative positions. Dotted lines, boundaries between contiguous 100 μm‐thick tissue sections used for reconstruction. Dorsal (D) and ventral (V) coordinates are same for 2 views of same cell. Male dendrites reach farther away from soma than do female dendrites.

From De Voogd and Nottebohm 31.


Figure 8.

Normal song development in male canaries, kept under photoperiod conditions of New York state, shown as horizontal progression from subsong (SS) to plastic song (PS) to full song (FS). FS is stable song that adult canaries sing during breeding season. At end of breeding season PS recurs. HVc volume grows during the time song is first acquired and shrinks to that of 3‐ to 4‐mo‐old canary in late summer after breeding season is over and song becomes plastic again. Vertical axis, volume of nucleus HVc ± 1 SD. Open circles, samples of 4 birds killed at age shown on horizontal axis; filled circles, samples of 9 and 12 birds killed at 12 and 17 mo, respectively; open diamonds, samples of 10, 9, and 8 birds killed at end of their 1st, 2nd, and 3rd breeding seasons, respectively.



Figure 9.

Sound spectrographs of 3 recordings from same bird. A: plastic song when bird was 4 mo old. B: plastic song produced in late summer (September) after end of its 1st breeding season. C: stable song during preceding May when bird was 12 mo old and in full reproductive condition. In A and B song syllables are repeated in wavering, unstable fashion; in C syllables are virtual carbon copies of each other. Calibration bar, 0.5 s.



Figure 10.

Camera lucida tracing of dendritic and axonal processes of HVc cell labeled with horseradish peroxidase andthymidine. Heavy lines, dendrites; light lines, axons. Boundaries of HVc: solid line, ventricle; broken line, fibrous lamina. Calibration bar, 100 μm. D and M, dorsal and medial reaches of the brain. [From Paton and Nottebohm 111. Copyright 1984 by the American Association for the Advancement of Science.]

3H


Figure 11.

Anatomy of HVc cell bodies labeled with horseradish peroxidase and (3H)thymidine. Seperate photographs were taken of same field but were focused first at level of cell itself (A and C) and then at level of exposed silver grains in layer of emulsion above cell (B and D). A and B, same cell; C and D, same cell. Calibration bar, 10 μm. (From Paton and Nottebohm 111. Copyright 1984 by the American Association for the Advancement of Science.)



Figure 12.

1–3: Distribution of labeled cells in same frontal brain section from an adult female canary killed 26 days after last of series of 28 injections of (3H)thymidine spaced 12 h apart. Each dot corresponds to a labeled cell; HVc is demarcated by broken line curving under lateral ventricle (V) of forebrain. 1: Labeled neurons. 2: Labeled glia. 3: Labeled endothelial cells. 4: Rostral section of same brain showing distribution of labeled neurons. 5: Caudal section of same brain showing distribution of labeled neurons. 6: Frontal section of brain taken at the level of nucleus HVc from adult female canary killed 52 days after last of series of 28 injections of (3H)thymidine spaced 12 h apart. Each dot corresponds to a labeled neuron. Incubation period for autoradiography was 4 wk. Criterion for recognizing a labeled cell was 5 times background for all sections except 6, for which it was 10 times background. Using either criterion, there are many labeled neurons throughout forebrain (with exception of archistriatum) but very few, or none, outside forebrain. Sagittal view of brain (inset, lower left) shows level at which the 4 different sections were taken. A, archistriatum; APH, area parahippocampalis; Aq, aqueduct; Cb, cerebellum; FA, tractus frontoarchistriatalis; FLM, fasciculus longitudinalis medialis; HA, hyperstriatum accessorium; Hab, habenula; HD, hyperstriatum dorsalis; HP, hippocampus; HV, hyperstriatum ventralis; IM, nucleus isthmi pars magnocellularis; IPC, nucleus isthmi pars parvocellularis; LMD, lamina medullaris dorsalis; LPO, lobus parolfactorius; MLd, nucleus mesencephalicus lateralis pars dorsalis; N, neostriatum; NC, neostriatum caudalis; OM, tractus occipitomesencephalicus; PA, paleostriatum augmentatum; Pt, nucleus pretectalis; RA, nucleus robustus archistriatalis; SPM, nucleus spiriformis medialis; TPC, nucleus tegmenti pedunculopontinus pars compacta. Calibration bar, 1 mm.



Figure 13.

Histograms showing relative frequency with which various numbers of exposed silver grains occurred over nuclei of 100 labeled neurons (A), 100 labeled glia (B), and 100 labeled endothelial cells (C) taken from HVc and underlying neotriatum following systemic treatment with (3H)thymidine (see Fig. 12); this bird was killed 26 days after last (3H)thymidine injection. Brain sections were incubated for autoradiography for only 10 days and showed very low background labeling. As a result, criterion for accepting cell as labeled was only 3 exposed silver grains per nucleus, which corresponded to 10 times background label for area of similar size. Short incubation permitted counting all exposed silver grains, even over those nuclei that showed the heaviest concentration of label.

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Article Title: Plasticity in Adult Avian Central Nervous System: Possible Relation Between Hormones, Learning, and Brain Repair
 

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Fernando Nottebohm. Plasticity in Adult Avian Central Nervous System: Possible Relation Between Hormones, Learning, and Brain Repair. Compr Physiol 2011, Supplement 5: Handbook of Physiology, The Nervous System, Higher Functions of the Brain: 85-108. First published in print 1987. doi: 10.1002/cphy.cp010503