Neurogenesis in the adult avian song-control system - PubMed (original) (raw)

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Neurogenesis in the adult avian song-control system

Eliot A Brenowitz et al. Cold Spring Harb Perspect Biol. 2015.

Abstract

New neurons are added throughout the forebrain of adult birds. The song-control system is a model to investigate the addition of new long-projection neurons to a cortical circuit that regulates song, a learned sensorimotor behavior. Neuroblasts destined for the song nucleus HVC arise in the walls of the lateral ventricle, and wander through the pallium to reach HVC. The survival of new HVC neurons is supported by gonadally secreted testosterone and its downstream effectors including neurotrophins, vascularization, and electrical activity of postsynaptic neurons in nucleus RA (robust nucleus of the arcopallium). In seasonal species, the HVC→RA circuit degenerates in nonbreeding birds, and is reconstructed by the incorporation of new projection neurons in breeding birds. There is a functional linkage between the death of mature HVC neurons and the birth of new neurons. Various hypotheses for the function of adult neurogenesis in the song system can be proposed, but this remains an open question.

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Figures

Figure 1.

Figure 1.

A schematic of the neurogenic regions in the avian brain overlaid on the avian song circuits. Neurogenic regions are shown in red. Note the proximity of HVC (and hippocampus [HC]) to the ventricular zone (VZ). A schematic version of the motor pathway for song production is shown in blue. A schematic of the ascending auditory pathway is shown in green. The dotted line indicates an indirect route through many nuclei of the ascending auditory pathway leading to field L in the telencephalon. The anterior forebrain circuit for song learning and plasticity is shown in yellow. NCM, Caudomedial nidopallium; RA, arcopallium; LMAN, lateral magnocellular nucleus of the anterior neostriatum; OB, olfactory bulb; DLM, dorsolateral medial; PAm, parambigualis; RAm, retroambigualis

Figure 2.

Figure 2.

A timeline of the processes of avian neurogenesis and the proportion of new neurons that persist through each of these processes. The timeline is based on the work of Alvarez-Buylla and Nottebohm (1988), Barami et al. (1994), and Scott et al. (2012). The percentages of survival through the various processes of avian neurogenesis are based on the findings of Kirn et al. (1991, 1999), Barnea and Nottebohm (1994), Nottebohm et al. (1994), Scott and Lois (2007), and Walton et al. (2012). VZ, Ventricular zone.

Figure 3.

Figure 3.

A schematic of the factors ranging from gene expression to behavior that influence the birth and migration of neuroblasts and the addition of new neurons to an HVC. The solid black lines indicate factors that positively influence the given cell, factor, or process to which it points. The dashed lines represent changes in cell process indicated (e.g., cell divisions and migration). The dotted lines represent indirect routes of influence (i.e., through other genes, factors, etc.). The breakout panel to the right summarizes patterns of gene expression in different brain regions that positively influence component processes of neurogenesis. In the ventricular zone (VZ), the (+) indicates genes that promote proliferation, whereas the (−) indicates genes the promote exit from the cell cycle. DCX+, Doublecortin-positive migratory neuroblast; IN, interneuron; NPC, neural progenitor cell; NSC, neural stem cell; PN, projection neuron. ER, endoplasmic reticulum; VEGF, vascular endothelial growth factor; BDNF, brain-derived neurotrophic factor; GABA, γ-aminobutyric acid; RA, arcopallium; PAm, parambigualis; RAm, retroambigualis.

Figure 4.

Figure 4.

Postsynaptic activity influences the addition of new robust nucleus of the arcopallium (RA)-projecting neurons to HVC. Spontaneous activity of neurons in RA was decreased by unilateral infusions of muscimol (2.8 mg/ml) or increased by infusion of KCl (100 m

m

). Inhibiting activity decreased neuronal addition (Larson et al. 2014). Increasing activity increased neuronal addition to HVC (ipsilateral to KCl infusion, 312 ± 75 new neurons; contralateral to KCl infusion, 160 ± 23 new neurons). Asterisks indicate p < 0.05 in post hoc _t_-test following two-way ANOVA. BrdU, 5-bromo-2′-deoxyuridine; SD, short day; LD, long day; T, testosterone.

Figure 5.

Figure 5.

A model of the seasonal changes in physiology, morphology, and behavior of songbirds. As day length increases at the onset of the breeding season, plasma testosterone (T) levels increase. The increase in T drives an increase in neuronal number in HVC along with changes in gene expression, morphology, and physiology of HVC and robust nucleus of the arcopallium (RA). All of these changes in morphology and physiology permit the production of stereotyped song. As day length decreases at the onset of the nonbreeding season, T levels drop, HVC neurons die, and song degrades. This cycle repeats annually.

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References

    1. Abrous DN, Wojtowicz JM. 2008. Neurogenesis and hippocampal memory system. In Adult neurogenesis (ed. Gage FH, Kempermann G, Song HJ), pp. 445–461. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. - PMC - PubMed
    1. Adar E, Nottebohm F, Barnea A. 2008a. The relationship between nature of social change, age, and position of new neurons and their survival in adult zebra finch brain. J Neurosci 28: 5394–5400. - PMC - PubMed
    1. Adar E, Lotem A, Barnea A. 2008b. The effect of social environment on singing behavior in the zebra finch (Taeniopygia guttata) and its implication for neuronal recruitment. Behav Brain Res 187: 178–184. - PubMed
    1. Altman J, Das GD. 1965. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124: 319–335. - PubMed
    1. Alvarez-Borda B, Nottebohm F. 2002. Gonads and singing play separate, additive roles in new neuron recruitment in adult canary brain. J Neurosci 22: 8684–8690. - PMC - PubMed

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