Adult female and male zebra finches show distinct patterns of spine deficits in an auditory area and in the song system when reared without exposure to normal adult song

Abstract

Male songbirds typically require exposure to normal adult conspecific song during development in order to learn a normal song of their own. Females require exposure to conspecific song during development in order to select high-quality, learned song over the incomplete song produced by males reared in isolation. Altering males' opportunity for song learning during development affects the neuroanatomy of brain regions involved in song production (the song system), but in females the neural effects of song learning are unknown. We raised male and female zebra finches (Taeniopygia guttata) with differing amounts of exposure to singing males during development. At 120 days, we Golgi-stained their brains and measured the frequency of dendritic spines in brain areas used in song perception or production. We found that females reared with little or no exposure to song have 31% fewer dendritic spines per unit length of dendrite in caudomedial nidopallium (NCM), a brain area activated by song perception, compared to control females. The deprived females had small deficits in the frequency of spines in HVC, a region activated by song production in males. Males with limited exposure to song had a 24% lower spine density in HVC than controls but only a 10% lower density in NCM. These data support the hypothesis that NCM is important in auditory learning, while HVC is involved in sensorimotor learning, and that these capacities are differentially emphasized in the two sexes.

Late-postnatal cannabinoid exposure persistently elevates dendritic spine densities in area X and HVC song regions of zebra finch telencephalon

“…Assuming that Area X- and lMAN-like decreases in spine densities also occur within HVC following the sensorimotor stage of song learning through adulthood, a second pruning stage must follow spine stabilization associated with auditory learning. If this is the case then (as indicated above for lMAN) cannabinoid-altered vocal development must be mechanistically distinct from effects produced by social isolation, as lack of a tutor decreases HVC spine densities measured in adults (by 24 %, Lauay et al, 2005). Combined with our findings, this suggests that normal vocal development is associated with finite range of dendritic spine densities within HVC, as both increased and decreased densities are associated with altered song learning.…”

“…Furthermore, Rausch and Scheich report that in young mynah birds trained to imitate human speech, vocal learning is accompanied by significant reductions in spine densities, enlargement of remaining spine heads, lengthened dendrites, as well as gradual increases in perikaryon diameter in HVC (Rausch and Scheich, 1982). Proper vocal learning and processing of sensory information depends upon developmental changes within a number of brain regions (Airey et al, 2000; Devoogd et al, 1985; Lauay et al, 2005), including telencephalic regions lMAN, Area X, HVC and RA that distinctly and densely express CB 1 cannabinoid receptors (Soderstrom and Tian, 2006). Thus, we hypothesized that cannabinoid-altered vocal learning may involve effects on spine densities and neuron size within these song learning and control regions.…”

Experience-dependence of neural responses to social versus isolate conspecific songs in the forebrain of female Zebra Finches

“…Applying analyses of neuronal spectrotemporal receptive fields (STRFs) in response to natural stimuli (Theunissen et al 2000;Woolley et al , 2006, or information theoretic analysis of spike patterns (Hsu et al 2004;Wang et al 2007), to electrophysiological recordings from female Zebra Finches can address these questions more fully, but our playback paradigm of three exemplars per stimulus type did not allow for this. It also remains to be explored whether or how auditory selectivity in response to different natural and synthetic stimuli arises along the auditory pathway between the cochlear nuclei through the auditory mid-brain to Field L (Wild 1995;Hsu et al 2004;Woolley et al , 2006, and how it is further modified in upstream auditory areas in the telencephalon of female Zebra Finches (Bailey and Wade 2003;Lauay et al 2005) across ontogeny (Amin et al 2007). …”

“…The neural correlates of patterns of behavioural discrimination described above were first documented using anatomical (Lauay et al 2005) and immediate early gene activation (IEG) methods in nonsinging female Zebra Finches (Tomaszycki et al 2006), as well as using neurophysiological data in singing European Starlings (Sturnus vulgaris) (Cousillas et al 2006) that differed in their early social/acoustic experiences. Here, we recorded spike rate responses in the forebrain of female Zebra Finches that differed in their early conspecific auditory experiences.…”

Experience dependence of neural responses to different classes of male songs in the primary auditory forebrain of female songbirds

“…To parallel these results, several studies based on neurophysiological recordings from males of different songbird species, also revealed differential responses to familiar songs vs. unfamiliar songs, using repeated presentations of songs of both unrelated individuals and songs fathers or tutors, in CMM (Gentner and Margoliash 2003) and NCM (Amin et al 2004). Similarly, prior work using lesioning, physiological, and/or IEG approaches on female zebra finches specifically also implied that these secondary auditory forebrain areas (CMM and NCM) underlie behavioral discrimination between conspecific and heterospecific songs (MacDougall-Shackleton et al 1998, Stripling et al 2001, Bailey et al 2002, Phan and Vicario 2010) and its experience-dependent modulation (Lauay et al 2005, Tomaszycki et al 2006, Terleph et al 2008). …”