Species differences in auditory processing dynamics in songbird auditory telencephalon

The caudomedial nidopallium (NCM) of songbirds is a telencephalic area involved in the auditory processing and memorization of complex vocal communication signals. We used pure tone stimuli and multiunit electrophysiological recordings in awake birds to investigate whether the basic properties of song-responding circuits in NCM differ between canaries and zebra finches, two species whose songs are markedly different in their spectral and temporal organization. We found that the responses in zebra finch NCM are characterized by broad tuning and sustained responses that may facilitate the integration of zebra finch song syllables and call notes that are of long duration and have a broad harmonic structure. In contrast, we found that the responses in canary NCM show narrower tuning and less sustained responses over the time periods analyzed. These characteristics may contribute to enhanced processing of the narrow-band whistles, rapid trills, and steep frequency modulations that are prominent features of canary song. These species differences are much less pronounced in field L2, the direct thalamorecipient region that represents a preceding station in the central avian auditory pathway. NCM responses did not differ across sexes of either species, but field L2 did show wider tuning in zebra finch females relative to males. In sum, species differences in the response properties of NCM likely reflect selectivity for the acoustic elements of each species' vocal repertoire.     

Auditory topography and temporal response dynamics of canary caudal telencephalon

To map the encoding of auditory cues in songbirds, multiunit electrophysiological responses to pure tone stimuli (250-5000 Hz) were recorded at 373 sites throughout the avian analogue of the mammalian auditory cortex in the caudal telencephalon of awake, restrained canaries. We found that a dorso-ventral tonotopic gradient from low to high frequency stimuli extends from the rostral field L2 to caudal-most caudo-medial nidopallium (NCM), similar to the frequency-dependent patterns of ZENK gene expression in canary NCM and to electrophysiological responses in other songbird species. However, response characteristics differ across the region. In field L2, responses are vigorous, phasic, and do not habituate to repeated presentations of the same stimulus. In an important subset of field L2 sites, tuning width narrows over the course of the response, which then terminates rapidly at stimulus offset. These properties are associated with inhibition at many nonpreferred frequencies and poststimulus inhibition at responsive frequencies. In contrast, NCM sites habituate to repeated sine waves, have wider tuning and lower amplitude responses, and rarely show inhibitory effects. Tuning curves in NCM are also flatter than those of field L2, and are often multipeaked. In addition, tuning width increases as the response unfolds and poststimulus excitation is often sustained in NCM. In sum, specific parts of the canary caudo-medial telencephalon differ in their response properties, suggesting differential roles in auditory processing. NCM properties, in particular, may allow for response integration across multiple spectrally varying stimulus elements, such as those that occur during birdsong.     

HEARING IN THE RED-BILLED FIREFINCH LAGON O S TIC TA SENEGALA AND THE SPANISH TIMBRADO CANARY SERINUS CANARIA: THE INFLUENCE OF NATURAL AND ARTIFICIAL SELECTION ON AUDITORY ABILITIES AND VOCAL STRUCTURE

ABSTRACT

We tested the auditory sensitivity of red-billed firefinches Lagonosticta senegal0061 and Spanish timbrado canaries Serinus canaria. Both these species produce songs and calls that are narrowband and relatively high in frequency, with spectral energy falling predominantly in the region of 3–6 kHz. Hearing thresholds were measured in these two species and compared to the auditory sensitivity of closely related species: the well studied zebra finch Taeniopygia guttata, and other strains of canary bred for song. Auditory thresholds were similar in both groups of birds, with firefinches having an audiogram typical for that of small birds. Timbrado canaries exhibited an audiogram with its greatest sensitivity in the relatively high region of 4–6 kHz, corresponding to the peak frequency of its calls. Critical ratios measured over a range of several octaves increased in a monotonie fashion at a rate of 2–3 dB per octave for both firefinches and timbrado canaries. Critical ratios in these two species are similar to what has been found in most other small passerine species, suggesting spectral resolving abilities similar to most small birds tested to date.     

Increased bursting glutamatergic neurotransmission in an auditory forebrain area of the zebra finch (Taenopygia guttata) induced by auditory stimulation

The caudomedial nidopallium (NCM) is a telencephalic area involved in auditory processing and memorization in songbirds, but the synaptic mechanisms associated with auditory processing in NCM are largely unknown. To identify potential changes in synaptic transmission induced by auditory stimulation in NCM, we used a slice preparation for path-clamp recordings of synaptic currents in the NCM of adult zebra finches (Taenopygia guttata) sacrificed after sound isolation followed by exposure to conspecific song or silence. Although post-synaptic GABAergic and glutamatergic currents in the NCM of control and song-exposed birds did not present any differences regarding their frequency, amplitude and duration after song exposure, we observed a higher probability of generation of bursting glutamatergic currents after blockade of GABAergic transmission in song-exposed birds as compared to controls. Both song-exposed males and females presented an increase in the probability of the expression of bursting glutamatergic currents, however bursting was more commonly seen in males where they appeared even without blocking GABAergic transmission. Our data show that song exposure changes the excitability of the glutamatergic neuronal network, increasing the probability of the generation of bursts of glutamatergic currents, but does not affect basic parameters of glutamatergic and GABAergic synaptic currents.     

HVC lesions modify immediate early gene expression in auditory forebrain regions of femalesongbirds

It is well established that auditory forebrain regions of oscine birds are essential for the encoding of species‐typical songs and are, therefore, vital for recognition of song during sociosexual interactions. Regions such as the caudal medial nidopallium (NCM) and the caudal medial mesopallium (CMM) are involved in perceptual processing of song and the formation of auditory memories. There is an additional telencephalic nucleus, however, that has also been implicated in species recognition. This nucleus is HVC, a prominent nucleus that sits at the apex of the song system, and is well known for its critical role in song learning and song production in male songbirds. Here, we explore the functional relationship between auditory forebrain regions (i.e., NCM and CMM) and HVC in female canaries (Serinus canaria). We lesion HVC and examine immediate early gene responses to conspecific song presentation within CMM and NCM to explore whether HVC can modulate auditory responses within these forebrain regions. Our results reveal robust deficits in ZENK‐ir in CMM and NCM of HVC‐lesioned females when compared with control‐ and sham‐lesioned females, indicating that functional connections exists between HVC and NCM/CMM. Although these connected regions have been implicated in song learning and production in males, they likely serve distinct functions in female songbirds that face the task of song recognition rather than song production. Identifying functional connections between HVC and auditory regions involved in song perception is an essential step toward developing a comprehensive understanding of the neural basis of song recognition. © 2012 Wiley Periodicals, Inc. Develop Neurobiol, 2013     

Effects of Song Experience and Song Quality on Immediate Early Gene Expression in Female Canaries (Serinus canaria)

Female songbirds are thought to make mate choices based on aspects of male song quality. Male canaries (Serinus canaria) produce songs with “special” syllables that have been shown to be highly salient to female listeners – eliciting high rates of sexual displays and enhanced immediate early gene (IEG) expression. Immunohistochemistry for the IEG ZENK was used to examine the effects of experience with these syllables on activity in the caudal mesopallium (CMM) and nidocaudal mesopallium (NCM), two auditory areas important in processing conspecific song. Photostimulated female canaries were housed in sound attenuated chambers and played pseudosongs containing either three special syllables or three non‐special syllables, an intro, and an outro sequence. Females that heard special syllable pseudosongs exhibited higher ZENK expression in CMM. To assess the effects of experience, photostimulated females were pair housed and exposed to playback of song with or without special syllables for 14 days. After transfer to individual housing, birds were played one of the aforementioned stimuli or silence. ZENK expression in CMM and NCM was equivalent for song with and without special syllables, but significantly lower for silence. Females who experienced song with special syllables had lower plasma estradiol concentrations after final song playback. This study indicates that CMM exhibits an IEG response bias to special syllables in limited acoustic contexts, but not in full song, which may contain additional biologically relevant information. Furthermore, estradiol concentrations may mediate changes in song responses, serving as a mechanism for modulating mate choice in differing song environments.     

Testosterone regulates the activity and expression of aromatase in the canary neostriatum

The estrogen synthesizing enzyme, P450 aromatase, plays a critical role in the regulation of vertebrate sexual behavior. Songbirds differ from other avian species in the distribution and expression of aromatase in the telencephalon. The highest concentration of aromatase in the songbird brain is found in the caudomedial neostriatum (NCM). This area surrounds the only nucleus of the neural song system that contains estrogen receptors, the high vocal center (HVC). It has been suggested that estrogen produced in NCM via aromatization of circulating testosterone (T) is involved in song development and adult song plasticity. The modalities of regulation of aromatase in NCM are not well understood, and some studies suggest that in NCM, unlike in the preoptic-hypothalamic areas, aromatase is not regulated by androgen and/or estrogen. In this work, we studied whether the treatment of female canaries with T, which induces the development of malelike song and the masculinization of the song system, also induces an increase in the expression and activity of aromatase in NCM. Our results show that both the expression and activity of aromatase in NCM increase in female canaries following T treatment. This study provides the first direct evidence that T regulates telencephalic aromatase in songbirds, and suggests that an increase in estrogen production in NCM might be functional in neural and behavioral plasticity during phases of song organization.     

Immediate early gene (ZENK) responses to song in juvenile female and male zebra finches: effects of rearing environment

Accurate song perception is likely to be as important for female songbirds as it is for male songbirds. Male zebra finches (Taeniopygia guttata) show differential ZENK expression to conspecific and heterospecific songs by day 30 posthatch in auditory perceptual brain regions such as the caudomedial nidopallium (NCM) and the caudomedial mesopallium (CMM). The current study examined ZENK expression in response to songs of different qualities at day 45 posthatch in both sexes. Normally reared juvenile zebra finches showed higher densities of immunopositive nuclei in both the dorsal and ventral areas of NCM and CMM (formerly cmHV), but not HA, a visual area, in response to normal song over untutored song or silence. Male and female patterns of ZENK expression did not differ. We next compared responses of birds reared without exposure to normal song (untutored) to those of normally reared birds. Untutored birds did not show higher responses to normal song than to untutored song in the three song perception areas. Furthermore, untutored birds of both sexes showed lower densities of immunopositive nuclei in all four areas than did normally reared birds. In addition, ZENK expression was greater in untutored females than in males in the dorsal portion of NCM and in CMM. Our findings suggest that at least some neural mechanisms of song perception are in place in socially reared female and male finches at an early age. Furthermore, early exposure to song tutors affects responses to song stimuli.     

Transmission of avian pox from starlings to Rothchild's mynahs

Several wild species of birds, including starlings (Sturnus vulgaris), house sparrows (Passer domesticus) and pigeons (Columba livia) gained access to an aviary housing Rothchild's mynahs (Leucospar rothchildii) and over 100 additional birds representing a variety of species. Six of approximately 15 mynahs became infected with avian pox and all of them died. None of the other birds in the aviary developed lesions. Pox virus was isolated from mynah facial lesions on chicken chorioallantoic membrane and in duck embryo fibroblast cell culture. It did not produce lesions in white Leghorn chickens, but did produce lesions in 4 of 11 wild starlings captured outside the aviary. Results indicated the agent was an indigenous starling pox capable of infecting and producing disease in mynah birds. Destruction of the captive starlings and isolation of the remaining mynahs immediately stopped the mortality.     

Social competition and plasma testosterone profile in domesticated canaries: an experimental test of the challenge hypothesis

The challenge hypothesis predicts that plasma testosterone (T) concentration is high when male-male competitions are high and decreases when males are engaged in paternal care. In monogamous species, T concentration increases at the beginning of the breeding period and decreases after egg laying. According to the challenge hypothesis, increasing competition should also lead to T increase. The aim of our study was to test this hypothesis. In a first experiment, we measured the T profile of domesticated canaries housed with their mate in separated cages without competition. In a second one, we created a competition by housing male and female domestic canaries together (in an aviary) and emphasized this competition by limiting food access. We also studied social status effect. Our results showed no effect of social status in both sexes and no differences in female's T concentration. Concerning males, we obtained a clear monogamous T profile from the ones housed in a low competition situation and a polygamous profile from the others housed in high competition situation. Thus, our results support the hypothesis of the plasticity of the mechanisms controlling T concentration according to environmental conditions.     

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.     

Influence of physical activity on tibial bone material properties in laying hens

Laying hens develop a type of osteoporosis that arises from a loss of structural bone, resulting in high incidence of fractures. In this study, a comparison of bone material properties was made for lines of hens created by divergent selection to have high and low bone strength and housed in either individual cages, with restricted mobility, or in an aviary system, with opportunity for increased mobility. Improvement of bone biomechanics in the high line hens and in aviary housing was mainly due to increased bone mass, thicker cortical bone and more medullary bone. However, bone material properties such as cortical and medullary bone mineral composition and crystallinity as well as collagen maturity did not differ between lines. However, bone material properties of birds from the different type of housing were markedly different. The cortical bone in aviary birds had a lower degree of mineralization and bone mineral was less mature and less organized than in caged birds. These differences can be explained by increased bone turnover rates due to the higher physical activity of aviary birds that stimulates bone formation and bone remodeling. Multivariate statistical analyses shows that both cortical and medullary bone contribute to breaking strengthThe cortical thickness was the single most important contributor while its degree of mineralization and porosity had a smaller contribution. Bone properties had poorer correlations with mechanical properties in cage birds than in aviary birds presumably due to the greater number of structural defects of cortical bone in cage birds.     

Developmental experience alters information coding in auditory midbrain and forebrain neurons

In songbirds, species identity and developmental experience shape vocal behavior and behavioral responses to vocalizations. The interaction of species identity and developmental experience may also shape the coding properties of sensory neurons. We tested whether responses of auditory midbrain and forebrain neurons to songs differed between species and between groups of conspecific birds with different developmental exposure to song. We also compared responses of individual neurons to conspecific and heterospecific songs. Zebra and Bengalese finches that were raised and tutored by conspecific birds, and zebra finches that were cross‐tutored by Bengalese finches were studied. Single‐unit responses to zebra and Bengalese finch songs were recorded and analyzed by calculating mutual information (MI), response reliability, mean spike rate, fluctuations in time‐varying spike rate, distributions of time‐varying spike rates, and neural discrimination of individual songs. MI quantifies a response's capacity to encode information about a stimulus. In midbrain and forebrain neurons, MI was significantly higher in normal zebra finch neurons than in Bengalese finch and cross‐tutored zebra finch neurons, but not between Bengalese finch and cross‐tutored zebra finch neurons. Information rate differences were largely due to spike rate differences. MI did not differ between responses to conspecific and heterospecific songs. Therefore, neurons from normal zebra finches encoded more information about songs than did neurons from other birds, but conspecific and heterospecific songs were encoded equally. Neural discrimination of songs and MI were highly correlated. Results demonstrate that developmental exposure to vocalizations shapes the information coding properties of songbird auditory neurons. © 2009 Wiley Periodicals, Inc. Develop Neurobiol 70: 235–252, 2010.     

The hippocampus and caudomedial neostriatum show selective responsiveness to conspecific song in the female zebra finch

The perception of song is vital to the reproductive success of both male and female songbirds. Several neural structures underlying this perception have been identified by examining expression of immediate early genes (IEGs) following the presentation of conspecific or heterospecific song. In the few avian species investigated, areas outside of the circuit for song production contain neurons that are active following song presentation, specifically the caudal hyperstriatum ventrale (cHV) and caudomedial neostriatum (NCM). While studied in detail in the male zebra finch, IEG responses in these neural substrates involved in song perception have not been quantified in females. Therefore, adult female zebra finches were presented with zebra finch song, nonzebra finch song, randomly generated tones, or silence for 30 min. One hour later they were sacrificed, and their brains removed, sectioned, and immunocytochemically processed for FOS expression. Animals exposed to zebra finch song had a significantly higher density of FOS-immunoreactive cells in the NCM than those presented with other songs, tones, or silence. Neuronal activation in the cHV was equivalent in birds that heard zebra finch and non-zebra finch song, expression that was higher than that observed in the groups that heard no song. Interestingly, the hippocampus (HP) and adjacent parahippocampal area (AHP) were activated in a manner comparable to the NCM. These results suggest a general role for the cHV in song perception and a more specific role for the NCM and HP/AHP in facilitating recognition of and responsiveness to species-specific song in female zebra finches.     

Observations on Giardia of Budgerigars

ABSTRACT. Sick budgerigars from a local aviary were found to be infected with Giardia. The trophozoites were of the Giardia duodenalis type as defined by Filice with elongate median bodies pointed on one or both ends and more or less perpendicular to the long axis of the body. Using three fixation-staining methods, and material from three birds, the length ranged from 10 to 18 μm and the width from 4.5 to 11 μm with a mean length to width ratio of 2. Attempts to culture the trophozoites in vitro from intestinal scrapings were unsuccessful. Also attempts to transmit the infection by fecal cysts to canaries and mice failed. It is proposed that the budgerigar form be called Giardia duodenalis , race psittaci .     

Species differences in the identification of acoustic stimuli by birds

The perceptual organization of auditory stimuli can reveal a great deal about how the brain naturally groups events. The current study uses identification techniques to investigate the abilities of two species of birds in identifying zebra finch song as well as synthetically generated speech stimuli. Budgerigars (Melopsittacus undulatus) and zebra finches (Taeniopygia guttata) were trained to differentially peck keys in response to the presentation of various complex stimuli. Although there were no clear differences in performance during the training paradigm between the two species, budgerigars were far more adept at learning to identify both sets of complex stimuli than were zebra finches, requiring far less trials to reach criterion. The non-singing but vocally plastic budgerigars vastly outperformed zebra finches at identifying both zebra finch song and synthetically designed human speech despite known similarities in auditory sensitivities between the two species and seemingly equivalent learning capacity. The flexibility that budgerigars seem to have at identifying various stimuli is highlighted by their enhanced performance in these tasks. These results are discussed in the context of what is known about both general and specialized processes which may contribute to any differences or similarities in performance.     

The effect of prior residence and pair bond on scrounging choices in flocks of zebra finches, Taenopygia guttata

In groups, animals can use the producer tactic to locate food patches and the scrounger tactic to join the food discoveries of other companions. At equilibrium, models predict a mixture of the two tactics with equal payoffs. Several factors may constrain the use of tactics and lead to biases in scrounging choices. I explored the effect of prior residence and pair bond as potential constraints on scrounging choices in flocks of zebra finches (Taenopygia guttata). Experimental flocks contained two birds already established in an aviary (prior residents) and two birds recently released in the aviary for the first time (new residents). All birds were previously trained to find food on a foraging grid. In the aviary, new residents followed prior residents from perches to the grid and relied heavily on prior residents to locate food patches. Low initial success by new residents probably favoured heavy reliance on the scrounger tactic. New residents that formed pair bonds with prior residents foraged closer to their mates and scrounged selectively from their mates in some cases. Prior residence, and pair bond to a lesser extent, influenced scrounging choices in zebra finches and could lead to deviation from the expected use of foraging tactics.     

Tactile contact is required for early estrogen treatment to alter the sexual partner preference of female zebra finches

Sex steroid actions during early development appear to play a role in the development of sex differences in sexual partner preference (SPP, preference for males vs. females) in several species of mammals and in the socially monogamous pair bonding zebra finch (Taeniopygia guttata). Female finches treated with estrogen as nestlings exhibit varying degrees of masculinized SPP as adults, but only if they have been housed in all-female groups during the juvenile and young adult period, suggesting that the estrogen effect may involve social experience and possibly sexual imprinting. Because tactile contact is important for consolidation of imprinted preferences in this species, it was predicted that early estrogen treatment would alter preferences of females only if they were allowed to have tactile contact with other females. Subjects were injected with estradiol benzoate or with oil (normal controls) daily for the first 2 weeks post-hatching. At age 45 days, they were housed in a mixed sex aviary (normal controls), in an all-female aviary allowing tactile contact (group EB-TC), or in an all-female aviary with no tactile contact (group EB-NTC). At 100+ days, birds were given two-choice SPP tests followed by aviary tests of SPP. EB-TC females did not show the sex-typical preference for male stimuli, and differed significantly from the controls on several measures. EB-NTC females preferred males and never differed significantly from controls. These results show that tactile contact after age 45 days is essential for an EB effect on SPP, supporting the hypothesis that hormones and sexual imprinting together contribute to SPP.