Developmental origin and identity of song system neurons born during vocal learning in songbirds

Abstract

New neurons are added to the forebrain song control regions high vocal center (HVC) and Area X of juvenile songbirds but the identity and site of origin of these cells have not been fully characterized. We used oncoretroviral vectors to genetically label neuronal progenitors in different regions of the zebra finch lateral ventricle. A region corresponding to the mammalian medial and lateral ganglionic eminences generated medium spiny neurons found in Area X and in the striatum surrounding Area X, and at least two classes of interneurons found in HVC. In addition, our experiments indicate that the HVC projection neurons that project into nucleus robust nucleus of the arcopallium (RA) are born locally from the ventricular region immediately dorsal to HVC. The ability to genetically target neuron subpopulations that give rise to different song system cell types provides a tool for specific genetic manipulations of these cell types. In addition, our results suggest striking similarities between neurogenesis in the embryonic mammalian brain and in the brain of the juvenile songbird and provide further evidence for the existence of conserved cell types in the forebrain for birds and mammals.

Wandering Neuronal Migration in the Postnatal Vertebrate Forebrain

“…HVC X neurons are born almost exclusively during embryonic development and many persist for the lifetime of the animal (Alvarez-Buylla et al, 1988a), whereas most HVC RA neurons are born postnatally and continue to be added throughout adult life (Kirn et al, 1999). We previously determined that HVC RA neurons, which are born during the critical period for vocal learning in zebra finches (40 -90 d after hatching), are derived from the pallial VZ dorsal to HVC (Scott and Lois, 2007). Neurons born in this region migrate to targets within HVC and to surrounding regions up to 3 mm away from the VZ.…”

“…All oncoretroviral vectors used were based on the Moloney murine leukemia virus. Gene expression was driven by the internal promoter of the Rous sarcoma virus, which we have shown previously to be a strong promoter in migrating neurons in the zebra finch (Scott and Lois, 2007). Viral particles were produced as described previously (Lois et al, 2002) and concentrated to 0.5-5 ϫ 10 6 infectious units per microliter.…”

“…Histological procedures are similar to those described previously (Scott and Lois, 2007). Eight days after injection with retroviral vectors, animals were deeply anesthetized and perfused with 3% paraformaldehyde (Sigma).…”

“…The addition of new neurons to HVC is increased by both the death of mature neurons (Scharff et al, 2000) and by behavioral demands, such as song learning (Nordeen and Nordeen, 1988;Kirn et al, 1994) and high rates of singing (Alvarez-Borda and Nottebohm, 2002). New neurons are born in the walls of the lateral ventricle (AlvarezBuylla et al, 1990b;Scott and Lois, 2007) and migrate for 1-2 weeks before they reach their final location (Alvarez-Buylla et al, 1988b). However, little is known about how these new neurons move through the mature nervous system and integrate into existing circuits.…”

Neuronal Stability and Drift across Periods of Sleep: Premotor Activity Patterns in a Vocal Control Nucleus of Adult Zebra Finches

“…Undirected singing is characterized by increased temporal variability in acoustic output (Kao et al, 2005;Olveczky et al, 2005), and greater variability in activity of the neurons of the lateral magnocellular nucleus of the nidopallium (LMAN) (Hessler and Doupe, 1999;Leonardo, 2004) that help regulate auditory-feedback-mediated song maintenance (Brainard and Doupe, 2000). Adult neurogenesis is prominent in the population of HVC-RAns (Alvarez-Buylla and Kirn, 1997;Scott and Lois, 2007;Scotto-Lomassese et al, 2007). Incorporation of new functional synapses could increase excitability of RA neurons.…”