Annual cycle of the black-capped chickadee: seasonality of singing rates and vocal-control brain regions

Black-capped chickadees have a rich vocal repertoire including learned calls and the learned fee-bee song. However, the neural regions underlying these vocalizations, such as HVC, area X, and RA (robust nucleus of arcopallium), remain understudied. Here, we document seasonal changes in fee-bee song production and show a marked peak in singing rate during March through May. Despite this, we found only minimal seasonal plasticity in vocal control regions of the brain in males. There was no significant effect of time of year on the size of HVC, X, or RA in birds collected in January, April, July, and October. We then pooled birds into two groups, those with large testes (breeding condition) and those with small testes (nonbreeding), regardless of time of year. Breeding birds had slightly larger RA, but not HVC or X, than nonbreeding birds. Breeding birds had slightly larger HVC and RA, but not X, as a proportion of telencephalon volume than did nonbreeding birds. Birds collected in July had heavier brains than birds at other times of year, and had the greatest loss in brain mass during cryoprotection. The absence of any overall seasonal change in the vocal-control regions of chickadees likely results from a combination of individual differences in the timing of breeding phenology and demands on the vocal-control regions to produce learned calls year-round.     

Failure to detect seasonal changes in the song system nuclei of the black‐capped chickadee (Poecile atricapillus)

Most temperate songbird species sing seasonally, and the brain areas involved in producing song (the song system) vary in size alongside the changes in behavior. Black‐capped chickadees (Poecile atricapillus) also sing seasonally, and we find that there are changes in the stereotypy and the length of the fee‐bee song from the nonbreeding to the breeding season. Yet despite these changes, we fail to find any evidence of seasonal changes in the song system. The song system of males is larger than that of females, as is typical in songbirds, but the ratio between the sexes is small compared to other species. We suggest three hypotheses to explain our failure to find seasonal variation in the chickadee song system. © 2006 Wiley Periodicals, Inc. J Neurobiol, 2006     

Immediate early gene activity in song control nuclei and brain areas regulating motivation relates positively to singing behavior during, but not outside of, a breeding context

In some species, such as songbirds, much is known about how the brain regulates vocal learning, production, and perception. What remains a mystery is what regulates the motivation to communicate. European starlings (Sturnus vulgaris) sing throughout most of the year, but the social and environmental factors that motivate singing behavior differ seasonally. Male song is highly sexually motivated during, but not outside of, the breeding season. Brain areas outside the song control system, such as the medial preoptic nucleus (POM) and ventral tegmental area (VTA), have been implicated in regulating sexually motivated behaviors in birds, including song. The present study was designed to explore whether these regions, as well as three song control nuclei [area X, the high vocal center (HVC), and the robust nucleus of the arcopallium (RA)], might be involved differentially in song produced within compared to outside of a breeding context. We recorded the behavioral responses of breeding and nonbreeding condition male starlings to the introduction of a female conspecific. Males did not show context-dependent differences in the overall amount of song sung. However, immunocytochemistry for the protein product of the immediate early gene cFOS revealed a positive linear relationship between the total amount of songs sung and number of cFOS-labeled cells in POM, VTA, HVC, and RA for birds singing during, but not outside of, a breeding context. These results suggest that these regions differentially regulate male song production depending on reproductive context. Overall the data support the hypothesis that the POM and VTA interact with the song control system, specifically HVC and RA, to regulate sexually motivated vocal communication in songbirds.     

白腰文鸟发声行为的性别差异及其机制

通过声谱分析,研究了５－１２０日龄雌、雄白腰文鸟（Lonchura striata swinhoei)的声谱变化,及该时段３个主要发声控制核团）ＨＶＣ、ＲＡ、Ａrea X)体积、睾丸（睾酮）的相应改变。结果如下：①４５日龄以前,雌雄鸟只能发出简单鸣叫（call),鸣声基本不会鸣唱。②雄性ＨＶＣ,ＲＡ,ＡreaX体积均比雌性大２－６部。３个核团的大小发育不完全一致。各核团的快速生长期与鸣唱学习的主要时段（６０－１２０日龄）不同步,说明核团的个体发育可能不完全受发声行为的影响。③睾丸的充分发育（１２０日龄后）及血液中具有较高的睾酮水平是雄鸟发出成熟鸣唱语句的重要条件。     

Rapamycin blocks the neuroprotective effects of sex steroids in the adult birdsong system

In adult songbirds, the telencephalic song nucleus HVC and its efferent target RA undergo pronounced seasonal changes in morphology. In breeding birds, there are increases in HVC volume and total neuron number, and RA neuronal soma area compared to nonbreeding birds. At the end of breeding, HVC neurons die through caspase‐dependent apoptosis and thus, RA neuron size decreases. Changes in HVC and RA are driven by seasonal changes in circulating testosterone (T) levels. Infusing T, or its metabolites 5α‐dihydrotestosterone (DHT) and 17 β‐estradiol (E2), intracerebrally into HVC (but not RA) protects HVC neurons from death, and RA neuron size, in nonbreeding birds. The phosphoinositide 3‐kinase (PI3K)‐Akt (a serine/threonine kinase)‐mechanistic target of rapamycin (mTOR) signaling pathway is a point of convergence for neuroprotective effects of sex steroids and other trophic factors. We asked if mTOR activation is necessary for the protective effect of hormones in HVC and RA of adult male Gambel's white‐crowned sparrows (Zonotrichia leucophrys gambelii). We transferred sparrows from breeding to nonbreeding hormonal and photoperiod conditions to induce regression of HVC neurons by cell death and decrease of RA neuron size. We infused either DHT + E2, DHT + E2 plus the mTOR inhibitor rapamycin, or vehicle alone in HVC. Infusion of DHT + E2 protected both HVC and RA neurons. Coinfusion of rapamycin with DHT + E2, however, blocked the protective effect of hormones on HVC volume and neuron number, and RA neuron size. These results suggest that activation of mTOR is an essential downstream step in the neuroprotective cascade initiated by sex steroid hormones in the forebrain.     

Differential estrogen accumulation among populations of projection neurons in the higher vocal center of male canaries

The higher vocal center (HVC) of adult male canries undergoes a seasonal change in volume that corresponds to seasonal modifications of vocal behavior: HVC is large when birds produce stereotyped song (spring) and is small when birds produce plastic song and add new song syllables into their vocal repertoires (fall). We reported previously that systemic exposure to testosterone (T) produces an increase in the volume of HVC similar to that observed with long-day photoperiods. T-induced growth of HVC occured regardless of wheter the borders of HVC were defined by Nissl-staining, the distribution of androgen-concentrating cells, or the distribution of projection neurons [separate neuronal populations within HVC project to the robust nucleus of the archistriatum (RA) and to Area X of the avian striatum (X)]. In the present study we used steroid autoradiography to determine whether T can influence the distribution of HVC cells that bind estrogen, and we combined estrogen autoradiography with retrograde labeling to determine whether HVC neurons that project to RA versus X differ in their ability to accumulate estrogen. Results showed that T increased the volume of Nissl-defined HVC and although HVC contained a low density of estrogen-concentrating cells, T increased the spatial distribution of these cells to match the Nissl borders of HVC. We also identified a region containing a high density of estrogenconcentrating cells located medial to HVC [we call this region paraHVC (pHVC)], and T also increased the volume of pHVC. pHVC also contained numerous X-projecting neurons, but few if any RA-projecting neurons. Double-labeling analysis revealed the RA-projecting neurons did not accumulate estrogen, a small percentage of X-projecting neurons in HVC accumulated estrogen, and the majority of X-projecting neurons in pHVC showed heavy accumulation of estrogen. The data reported here and in our previous article suggest distinct roles for gonadal steroids within the HVC-pHVC complex: estrogens are concentrated by neurons that project to a striatal region that influences vocal production during song learning (X), whereas androgens are concentrated primarily by neurons that project to a motor region that is involved in vocal production during both song learning and the recitation of already-learned song (RA). © 1995 John Wiley & Sons, Inc.     

Forebrain circuits underlying the social modulation of vocal communication signals

Across vertebrate species, signalers alter the structure of their communication signals based on the social context. For example, male Bengalese finches produce faster and more stereotyped songs when directing song to females (female‐directed [FD] song) than when singing in isolation (undirected [UD] song), and such changes have been found to increase the attractiveness of a male's song. Despite the importance of such social influences, little is known about the mechanisms underlying the social modulation of communication signals. To this end, we analyzed differences in immediate early gene (EGR‐1) expression when Bengalese finches produced FD or UD song. Relative to silent birds, EGR‐1 expression was elevated in birds producing either FD or UD song throughout vocal control circuitry, including the interface nucleus of the nidopallium (NIf), HVC, the robust nucleus of the arcopallium (RA), Area X, and the lateral magnocellular nucleus of the anterior nidopallium (LMAN). Moreover, EGR‐1 expression was higher in HVC, RA, Area X, and LMAN in males producing UD song than in males producing FD song, indicating that social context modulated EGR‐1 expression in these areas. However, EGR‐1 expression was not significantly different between males producing FD or UD song in NIf, the primary vocal motor input into HVC, suggesting that context‐dependent changes could arise de novo in HVC. The pattern of context‐dependent differences in EGR‐1 expression in the Bengalese finch was highly similar to that in the zebra finch and suggests that social context affects song structure by modulating activity throughout vocal control nuclei. © 2015 Wiley Periodicals, Inc. Develop Neurobiol 76: 47–63, 2016     

Sex and seasonal differences in neurogenesis and volume of the song‐control system are associated with song in brood‐parasitic and non‐brood‐parasitic icterid songbirds

The song‐control system in the brain of songbirds is important for the production and acquisition of song and exhibits both remarkable seasonal plasticity and some of the largest neural sex differences observed in vertebrates. We measured sex and seasonal differences in two nuclei of the song‐control system of brood‐parasitic brown‐headed cowbirds (Molothrus ater) and closely‐related non‐parasitic red‐winged blackbirds (Agelaius phoeniceus). These species differ in both the development and function of song. Brown‐headed cowbirds have a larger sex difference in song than red‐winged blackbirds. Female cowbirds never sing, whereas female blackbirds do though much less than males. In cowbirds, song primarily functions in mate choice and males modify their song as they approach sexual maturity and interact with females. In red‐winged blackbirds, song is used primarily in territorial defence and is crystalized earlier in life. We found that the HVC was more likely to be discernable in breeding female blackbirds than in breeding female cowbirds. Compared to males, females had a smaller HVC and a smaller robust nucleus of the arcopallium (RA). However, females had higher doublecortin immunoreactivity (DCX+) in HVC, a measure of neurogenesis. Consistent with sex differences in song, the sex difference in RA volume was greater in cowbirds than in blackbirds. Males of both species had a smaller HVC with higher DCX+ in post‐breeding condition than in breeding condition when song is more plastic. Sex and seasonal differences in the song‐control system were closely related to variation in song in these two icterid songbirds. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 76: 1226–1240, 2016     

Testosterone-induced changes in adult canary brain are reversible

Brain nuclei that control song are larger in male canaries, which sing, than in females, which sing rarely or not at all. Treatment of adult female canaries with testosterone (T) induces song production and causes song-control nuclei to grow, approaching the volumes observed in males. For example, the higher vocal center (HVC) of adult females approximately doubles in size by 1 month following the onset of T treatment. Male HVC projects to a second telencephalic nucleus, RA (the robust nucleus of the archistriatum), which projects in turn to the vocal motor neurons. Whether HVC makes a similar connection in female canaries is not known, although HVC and RA are not functionally connected in female zebra finches, a species in which testosterone does not induce neural or behavioral changes in the adult song system. This experiment investigated whether HVC makes an efferent projection to RA in normal adult female canaries, or if T is necessary to induce the growth of this connection. In addition, we examined whether T-induced changes in adult female canary brain are reversible. Adult female canaries received systemic T implants that were removed after 4 weeks; these birds were killed 4 weeks after T removal (Testosterone-Removal, T-R). Separate groups of control birds received either (a) T implants for 4 weeks which were not removed (Testosterone-Control, T-C) or (b) empty implants (Untreated Control, øO-C). Crystals of the fluorescent tracer DiI were placed in the song-control nucleus HVC in order to anterogradely label both efferent targets of HVC, RA and Area X. Projections from HVC to RA and Area X were present in all treatment groups including untreated controls, and did not appear to differ either qualitatively or quantitatively. Thus, formation of efferent connections from HVC may be prerequisite to hormone-induced expression of song behavior in adult songbirds. The volumes of RA and Area X were measured using the distribution of anterograde label as well as their appearance in Nissl-stained tissue. RA was larger in T-treated control birds than in untreated controls. Experimental birds in which T was given and then removed (T-R) had RA volumes closer in size to untreated controls (ø-C). Because the volume of RA in T-treated controls (T-C) was larger than that of birds that did not receive T (ø-C), we conclude that the volume of RA increased in both T-C and T-R birds but regressed upon removal of T in T-R birds. Surprisingly, the volume of Area X did not increase in T-treated birds. Birds in this study were maintained on short days, suggesting that T-induced growth of Area X reported previously may have resulted from an interaction between T and another seasonal or photoperiodic factor induced by exposure to long daylengths. © 1993 John Wiley & Sons, Inc.     

Temporal patterning of song production: Participation of nucleus uvaeformis of the thalamus

Birdsong is a learned vocal behavior used in intraspecific communication. The motor pathway serving learned vocalizations includes the forebrain nuclei NIf, HVC, and RA; RA projects to midbrain and brain stem areas that control the temporal and acoustic features of song. Nucleus Uvaeformis of the thalamus (Uva) sends input to two of these forebrain nuclei (NIf and HVC) but has not been thought to be important for song production. We used three experimental approaches to reexamine Uva's function in adult male zebra finches. (1) Electrical stimulation applied to Uva activated HVC and the vocal motor pathway, including tracheosyringeal motor neurons that innervate the bird's vocal organ. (2) Bilateral lesions of Uva including the dorso-medial portion of the nucleus affected the normal temporal organization of song. (3) Chronic multiunit recordings from Uva during normal song and calls show bursts of premotor activity that lead the onset of some song components, and also larger bursts that mark the end of complete song motifs. These results implicate Uva in the production of learned vocalizations, and further suggest that Uva contributes more to the temporal structure than to the acoustic characteristics of song. © 1993 John Wiley & Sons, Inc.     

Seasonal variation of vocal behaviour in a temperate songbird: assessing the effects of laboratory housing on wild-caught, seasonally breeding birds

Many laboratories are conducting research using songbirds as their animal model. In particular, songbirds are widely used for studying the behavioural and neural mechanisms underlying vocal learning. Many researchers use wild-caught birds to conduct this research, although few studies of behaviour have been conducted to determine the effects of captive housing on these species. We investigated the vocal production pattern of wild-caught black-capped chickadees (Poecile atricapillus) over an entire season in laboratory housing. We documented the frequency of production of four vocalizations (fee-bee song, chick-a-dee calls, dee calls, and gargle calls) across seasons and diurnal pattern and compared the observed pattern of laboratory vocalizations to those previously observed and reported in the wild. Laboratory-housed chickadees had seasonal and diurnal vocal production shifts that were related to both photoperiodic changes (season) and diurnal pattern. For instance, there was significantly more fee-bee song in the spring than summer, autumn, and winter with the most fee-bee song occurring at spring dawn as seen in the wild. Our results also confirmed that the general pattern of vocalizations was consistent between wild and laboratory populations, with no significant differences for either the seasonal or diurnal pattern of fee-bee song production between populations. Differences between settings were observed in the pattern of chick-a-dee calls at dawn and sunset between field and laboratory populations. However, differences in the quantity of vocalization types between laboratory and wild populations suggest that housing conditions are influencing the normal vocal behavioural patterns.     

Neurotensin and neurotensin receptor 1 mRNA expression in song‐control regions changes during development in male zebra finches

Learned vocalizations are important for communication in some vertebrate taxa. The neural circuitry for the learning and production of vocalizations is well known in songbirds, many of which learn songs initially during a critical period early in life. Dopamine is essential for motor learning, including song learning, and dopamine‐related measures change throughout development in song‐control regions such as HVC, the lateral magnocellular nucleus of the anterior nidopallium (LMAN), Area X, and the robust nucleus of the arcopallium (RA). In mammals, the neuropeptide neurotensin strongly interacts with dopamine signaling. This study investigated a potential role for the neurotensin system in song learning by examining how neurotensin (Nts) and neurotensin receptor 1 (Ntsr1) expression change throughout development. Nts and Ntsr1 mRNA expression was analyzed in song‐control regions of male zebra finches in four stages of the song learning process: pre‐subsong (25 days posthatch; dph), subsong (45 dph), plastic song (60 dph), and crystallized song (130 dph). Nts expression in LMAN during the subsong stage was lower compared to other time points. Ntsr1 expression was highest in HVC, Area X, and RA during the pre‐subsong stage. Opposite and complementary expression patterns for the two genes in song nuclei and across the whole brain suggest distinct roles for regions that produce and receive Nts. The expression changes at crucial time points for song development are similar to changes observed in dopamine studies and suggest Nts may be involved in the process of vocal learning. © 2018 Wiley Periodicals, Inc. Develop Neurobiol 78: 671–686, 2018     

Birth,migration, incorporation,and death of vocal control neurons in adult songbirds

Neurogenesis continues in the brain of adult birds. These cells are born in the ventricular zone of the lateral ventricles. Young neurons then migrate long distances guided, in part, by radial cell processes and become incorporated throughout most of the telencephalon. In songbirds, the high vocal center (HVC), which is important for the production of learned song, receives many of its neurons after hatching. HVC neurons which project to the robust nucleus of the archistriatum to form part of the efferent pathway for song production, and HVC interneurons continue to be added throughout life. In contrast, Area X-projecting HVC cells, thought to be part of a circuit necessary for song learning but not essential for adult song production, are only born in the embryo. New neurons in HVC of juvenile and adult birds replace older cells that die. There is a correlation between seasonal cell turnover rates (addition and loss) and testosterone levels in adult male canaries. Available evidence suggests that steroid hormones control the recruitment and/or survival of new HVC neurons, but not their production. The functions of neuronal replacement in adult birds remain unclear. However, rates of HVC neuron turnover are highest at times of year when canaries modify their songs. Replaceable HVC neurons may participate in the modification of perceptual memories or motor programs for song production. In contrast, permanent HVC neurons could hold long-lasting song-related information. The unexpected large-scale production of neurons in the adult brain holds important clues about brain function and, in particular, about the neural control of a learned behavior—birdsong. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 585–601, 1997     

Melatonin Binding in the House Sparrow Song Control System: Sexual Dimorphism and the Effect of Photoperiod

Avian song is a sexually dimorphic behavior which is regulated seasonally. This regulation involves the construction and growth of song control structures: the high vocal center (HVC),nucleus robustus archistrialis(RA),nucleus magnocellularis anterior(MAN), and Area X. Song behavior and its neural correlates are controlled by steroid-dependent and independent processes. The avian circadian system is known to be involved in both daily processes and seasonal reproduction. A major part of this system is the circadian secretion of melatonin by the pineal gland. To determine possible interactions of the circadian and song control systems, the distribution and density of 2-[¹²⁵I]iodomelatonin (IMEL) binding, an indicator of melatonin sensitivity, were determined in male and female house sparrow brains. Specific binding was found in visual system centers of both genders, but binding in HVC, RA, and Area X was present only in males. Binding in MAN was present in both sexes. Although the effects of short and long photoperiods on male house sparrow IMEL binding in song structures revealed no systematic changes, there were significant differences in binding under different photoperiods in HVC and RA. IMEL binding in the tectofugalnucleus rotundus,however, was consistently highest under short day conditions. IMEL binding in song control nuclei was independent of testicular influence, since castration did not affect it significantly. The data point to a role for the circadian system of house sparrows in song control, but a specific role for melatonin in the daily or seasonal regulation of the song control system in birds, could not be determined.     

Seasonal‐like plasticity of spontaneous firing rate in a songbird pre‐motor nucleus

Many animals exhibit seasonal changes in behavior and its underlying neural substrates. In seasonally breeding songbirds, the brain nuclei that control song learning and production undergo substantial structural changes at the onset of each breeding season, in association with changes in song behavior. These changes are largely mediated by photoperiod‐dependent changes in circulating concentrations of gonadal steroid hormones. Little is known, however, about whether changes in the electrophysiological activity of neurons accompany the dramatic morphological changes in the song nuclei. Here we induced seasonal‐like changes in the song systems of adult white‐crowned sparrows and used extracellular recording in acute brain slices from those individuals to study physiological properties of neurons in the robust nucleus of the arcopallium (RA), a pre‐motor nucleus necessary for song production. We report that: RA neurons from birds in breeding condition show a more than twofold increase in spontaneous firing rate compared to those from nonbreeding condition; this change appears to require both androgenic and estrogenic actions; and this change is intrinsic to the RA neurons. Thus, neurons in the song circuit exhibit both morphological and physiological adult seasonal plasticity. © 2005 Wiley Periodicals, Inc. J Neurobiol, 2005     

Perineuronal nets and vocal plasticity in songbirds: A proposed mechanism to explain the difference between closed‐ended and open‐ended learning

Perineuronal nets (PNN) are aggregations of chondroitin sulfate proteoglycans surrounding the soma and proximal processes of neurons, mostly GABAergic interneurons expressing parvalbumin. They limit the plasticity of their afferent synaptic connections. In zebra finches PNN develop in an experience‐dependent manner in the song control nuclei HVC and RA (nucleus robustus arcopallialis) when young birds crystallize their song. Because songbird species that are open‐ended learners tend to recapitulate each year the different phases of song learning until their song crystallizes at the beginning of the breeding season, we tested whether seasonal changes in PNN expression would be found in the song control nuclei of a seasonally breeding species such as the European starling. Only minimal changes in PNN densities and total number of cells surrounded by PNN were detected. However, comparison of the density of PNN and of PNN surrounding parvalbumin‐positive cells revealed that these structures are far less numerous in starlings that show extensive adult vocal plasticity, including learning of new songs throughout the year, than in the closed‐ended learner zebra finches. Canaries that also display some vocal plasticity across season but were never formally shown to learn new songs in adulthood were intermediate in this respect. Together these data suggest that establishment of PNN around parvalbumin‐positive neurons in song control nuclei has diverged during evolution to control the different learning capacities observed in songbird species. This differential expression of PNN in different songbird species could represent a key cellular mechanism mediating species variation between closed‐ended and open‐ended learning strategies. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 77: 975–994, 2017     

Acetylcholinesterase in central vocal control nuclei of the zebra finch (<Emphasis Type="Italic">Taeniopygia guttata</Emphasis>)

The distribution of acetylcholinesterase (AChE) in the central vocal control nuclei of the zebra finch was studied using enzyme histochemistry. AChE fibres and cells are intensely labelled in the forebrain nucleus area X, strongly labelled in high vocal centre (HVC) perikarya, and moderately to lightly labelled in the somata and neuropil of vocal control nuclei robust nucleus of arcopallium (RA), medial magnocellular nucleus of the anterior nidopallium (MMAN) and lateral magnocellular nucleus of the anterior nidopallium (LMAN). The identified sites of cholinergic and/or cholinoceptive neurons are similar to the cholinergic presence in vocal control regions of other songbirds such as the song sparrow, starling and another genus of the zebra finch (Poephila guttata), and to a certain extent in parallel vocal control regions in vocalizing birds such as the budgerigar. AChE presence in the vocal control system suggests innervation by either afferent projecting cholinergic systems and/or local circuit cholinergic neurons. Co-occurrence with choline acetyltransferase (ChAT) indicates efferent cholinergic projections. The cholinergic presence in parts of the zebra finch vocal control system, such as the area X, that is also intricately wired with parts of the basal ganglia, the descending fibre tracts and brain stem nuclei could underlie this circuitry’s involvement in sensory processing and motor control of song.     

HVC microlesions do not destabilize the vocal patterns of adult male zebra finches with prior ablation of LMAN

The songs of adult male zebra finches (Taeniopygia guttata) arise by an integration of activity from two neural pathways that emanate from the telencephalic nucleus HVC (proper name). One pathway descends directly from HVC to the vocal premotor nucleus RA (the robust nucleus of the arcopallium) whereas a second pathway descends from HVC into a basal ganglia circuit (the anterior forebrain pathway, AFP) that also terminates in RA. Although HVC neurons that project directly to RA outnumber those that contribute to the AFP, both populations are distributed throughout HVC. Thus, partial ablation (microlesion) of HVC should damage both pathways in a proportional manner. We report here that bilateral HVC microlesions in adult male zebra finches produce an immediate loss of song stereotypy from which birds recover, in some cases within 3 days. The contribution of the AFP to the onset of song destabilization was tested by ablating the output nucleus of this circuit (LMAN, the lateral magnocellular nucleus of the anterior nidopallium) prior to bilateral HVC microlesions. Song stereotypy was largely unaffected. Together, our findings suggest that adult vocal production involves nonproportional integration of two streams of neural activity with opposing effects on song--HVC's direct projection to RA underlies production of stereotyped song whereas the AFP seems to facilitate vocal variation. However, the rapid recovery of song in birds with HVC microlesions alone suggests the presence of dynamic corrective mechanisms that favor vocal stereotypy.     

白腰文鸟发声行为的神经发育

本文研究了 5～ 15 0日龄雄性白腰文鸟 (Lonchurastriataswinhoei)不同年龄段的声谱变化以及这种变化的神经调制机制。结果如下 :(1)HVC、RA和AreaX三个发声核团的神经联系基本接近成年鸟的水平后 ,幼鸟才开始学习鸣叫 (约 45日龄 ) ;(2 )HVC、RA和AreaX达到成年核团体积时 (约 80日龄 ) ,幼鸟才具有成年雄鸟的鸣叫模式 ;(3)发声控制核团的发育与核团间的神经支配有关 ,而基本不受鸣唱行为的影响 ,HVC、RA和AreaX的最快增长时间段各不相同 ,三个核团随年龄增长而呈现体积增长的显著变化 (one wayANOVA ,P <0 0 5 ) ,但各核团在任意两个时间段的体积差异并不都显著。结果提示 :发声行为产生的时间和发展与发声控制核团的发育、核团间的神经联系有关 ,最终的体积发育程度受内在遗传力的作用 ,同时可能还受神经核团建立正常神经联系时间的影响