Enriched expression and developmental regulation of the middle‐weight neurofilament (NF‐m) gene in song control nuclei of the zebra finch

Abstract

Songbirds evolved a complex set of dimorphic telencephalic nuclei that are essential for the learning and production of song. These nuclei, which together make up the oscine song control system, present several neurochemical properties that distinguish them from the rest of the telencephalon. Here we show that the expression of the gene encoding the middle-weight neurofilament (NF-M), an important component of the neuronal cytoskeleton and a useful tool for studying the cytarchitectonic organization of mammalian cortical areas, is highly enriched in large neurons within pallial song control nuclei (nucleus HVC, robustus nucleus of the arcopallium, and lateral magnocellular nucleus of the nidopallium) of male zebra finches (Taeniopygia guttata). We also show that this transcript is highly expressed in large neurons in the medulla, pons, midbrain, and thalamus. Moreover, we demonstrate that NF-M expression in song control nuclei changes during postembryonic development, peaking during an early phase of the song-learning period that coincides with the maturation of the song system. We did not observe changes in NF-M expression in auditory areas or in song control nuclei in the contexts of hearing song or singing, although these contexts result in marked induction of the transcription factor ZENK. This observation suggests that NF-M might not be under the regulatory control of ZENK in auditory areas or in song control nuclei. Overall, our data indicate that NF-M is a neurochemical marker for pallial song control nuclei and provide suggestive evidence of an involvement of NF-M in the development and/or maturation of the oscine song control system.

Dynamic gene expression in the song system of zebra finches during the song learning period

“…These include COL12A1 and TAC1 , which showed a peak expression in HVC and X, respectively. This developmental pattern resembles that previously described for other genes, including NF‐M , which peaks in HVC between 35 and 50 dph (Velho et al, ), ALDH1A2 , which peaks in HVC between 35 and 50 dph (Olson et al, ), and CNTNAP2 , a target of the song‐related gene FOXP2 which undergoes increased expression in male LMAN between 50 and 75 days (Panaitof et al, ). We suggest that such genes may be associated with processes that peak around that age (e.g., when vocal plasticity is high) but then declines into adulthood.…”

“…The distinct cytoarchitectonic and connectivity characteristics of the song system are presumed to be driven by gene regulatory differences in the circuit, relative to the neighboring tissues. Studies of single or few molecular markers provided early hints that the song system nuclei are distinct in terms of gene expression (Gahr and Metzdorf, ; Wade, ; Denisenko‐Nehrbass et al, ; London et al, ; Kim et al, ; Wada et al, ; Chen et al, ; Kim and Arnold, ; Wade et al, ; Agate et al, ; Pinaud et al, ; Velho et al, ; Shahbazi et al, ). The use of high‐throughput approaches, in particular microarray screenings (Jarvis et al, ; Li et al, ; Lovell et al, ; Tomaszycki et al, ; Kato and Okanoya, ), has greatly expanded our knowledge of differential gene expression and molecular regulatory pathways within the song system.…”

Conservation and expression of IQ‐domain‐containing calpacitin gene products (neuromodulin/GAP‐43, neurogranin/RC3) in the adult and developing oscine song control system

“…Various calcium binding proteins (parvalbumin, calbindin, calretinin) are present in complex cellular distributions within individual song nuclei (Wild et al, 2001;Wild et al, 2005). Among RNAs enriched in specific song nuclei during development, the RNA for the medium-weight subunit for neurofilament is enriched in HVC, RA, and lMAN but not Area X (somewhat like NRGN) and reaches a peak in lMAN and RA at day 35 and in HVC at day 50 (Velho et al, 2007). Doublecortin RNA is enriched in HVC and RA in nestlings but not adults whereas the opposite developmental pattern is seen in Area X, with enrichment in adults but not nestlings (Kim et al, 2006).…”

Organization and development of zebra finch HVC and paraHVC based on expression of zRalDH, an enzyme associated with retinoic acid production

“…Throughout the song‐learning period the song control pathways are characterized by a high degree of neuronal plasticity that corresponds to changing patterns of gene expression (Clayton, 1997; Wada et al, 2006; Velho et al, 2007; Wissman and Brenowitz, 2009). Most notably, HVC volume and cell number increase dramatically during the song‐learning period (Bottjer et al, 1986).…”