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Roles of photoperiod and testosterone in seasonal plasticity of the avian song control system.

The song control nuclei of songbirds undergo pronounced seasonal changes in size and neuronal attributes. The mechanisms by which seasonal changes in environmental variables such as photoperiod mediate seasonal changes in these brain regions are not known. Manipulations of photoperiod and/or testosterone in captive songbirds induce seasonal changes in the size of song nuclei comparable to those observed in wild songbirds. It is unclear, however, whether the effects of photoperiod on the song nuclei are mediated by testosterone or by steroid-independent mechanisms. We independently manipulated photoperiod and testosterone in castrated male Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii) to determine the contributions of steroid-dependent and -independent actions of photoperiod to seasonal changes in the size and neuronal attributes of song nuclei. Testosterone implants increased the size of several song nuclei, regardless of photoperiod. Photoperiod exerted small but significant steroid-independent effects on the volume of the higher vocal center and the size of neurons in the robust nucleus of the archistriatum. Photoperiod also modulated the effect of testosterone on the size of area X; testosterone treatment had a more pronounced effect on the size of area X on short days than on long days. These results suggest that although testosterone is the primary factor mediating seasonal changes in neural attributes of the song nuclei, photoperiod may act via mechanisms that are independent of steroid levels to supplement or modulate the actions of testosterone.

Animals↗

Lesions of the anterior forebrain song control pathway in female canaries affect song perception in an operant task.

We tested whether the avian anterior forebrain pathway functions in song perception in female canaries, and whether it is specialized for conspecific song perception or functions more generally in auditory perception. Using operant conditioning methods, we trained female canaries to discriminate among synthetic sound stimuli, canary songs, and song sparrow songs. We also trained each bird to discriminate among visual stimuli to test for general effects of lesions on performance. When canaries had learned the discrimination tasks, bilateral electrolytic lesions of the lateral portion of the magnocellular nucleus of the anterior neostriatum (lMAN) were made. The lesioned birds were then tested on the previously learned discrimination tasks. Lesions that destroyed most or all of lMAN decreased the ability of female canaries to discriminate between previously learned pairs of acoustic stimuli of all types, while visual discrimination was unaffected. These results suggest that the female canary anterior forebrain pathway contributes to the perception of acoustic stimuli, with this contribution including heterospecific song and other acoustic stimuli as well as canary song.

Acoustic Stimulation↗

Topography and morphology of retinal ganglion cells in Falconiforms: a study on predatory and carrion-eating birds.

The topographic distribution of retinal ganglion cells and their cell body size have been studied in five Falconiform species, including predatory (chilean eagle Buteo fuscenses australis, and sparrow hawk Falco sparverius) and carrion-eating (chimango caracara Milvago chimango; condor Vultur gryphus, and black vulture Coragyps atratus) birds. All these species had a well defined nasal fovea and a horizontal streak. Instead of a temporal fovea as in eagles and hawks, an afoveate temporal area is present in chimango, condor, and vulture. The highest ganglion cell density was found in the nasal fovea of Falco and Buteo with 65,000 and 62,000 cells/mm2, respectively. A negative correlation between ganglion cell density and cell body size was found in all the species studied. The specializations of the temporal retina showed a rather homogenous population of medium sized neurons, while the nasal foveas showed a homogeneous population of smaller ganglion cells. Finally, the peripheral retina showed a heterogeneous population of large, medium, and small ganglion cells. Predatory behavior appears to be closely related to foveal specializations, and is best exemplified in the eagle and hawk and to a lesser extent in the chimango.

Animals↗

Chemoarchitectonic subdivisions of the songbird septum and a comparative overview of septum chemical anatomy in jawed vertebrates.

Available data demonstrate that the avian septal region shares a number of social behavior functions and neurochemical features in common with mammals. However, the structural and functional subdivisions of the avian septum remain largely unexplored. In order to delineate chemoarchitectural zones of the avian septum, we prepared a large dataset of double-, triple-, and quadruple-labeled material in a variety of songbird species (finches and waxbills of the family Estrildidae and a limited number of emberizid sparrows) using antibodies against 10 neuropeptides and enzymes. Ten septal zones were identified that were placed into lateral, medial, caudocentral, and septohippocampal divisions, with the lateral and medial divisions each containing multiple zones. The distributions of numerous immunoreactive substances in the lateral septum closely match those of mammals (i.e., distributions of met-enkephalin, vasotocin, galanin, calcitonin gene-related peptide, tyrosine hydroxylase, vasoactive intestinal polypeptide, substance P, corticotropin-releasing factor, and neuropeptide Y), enabling detailed comparisons with numerous chemoarchitectonic zones of the mammalian lateral septum. Our septohippocampal and caudocentral divisions are topographically comparable to the mammalian septohippocampal and septofimbrial nuclei, respectively, although additional data will be required to establish homology. The present data also demonstrate the presence of a medial septal nucleus that is histochemically comparable to the medial septum of mammals. The avian medial septum is clearly defined by peptidergic markers and choline acetyltransferase immunoreactivity. These findings should provide a useful framework for functional and comparative studies, as they suggest that many features of the septum are highly conserved across vertebrate taxa.

Animals↗

Immunohistochemical localization of neuropeptides in the vocal control regions of two songbird species.

Immunohistochemistry was used to map the distribution of four neuropeptides in song control regions of two songbird species, the European starling (Sturnus vulgaris) and the song sparrow (Melospiza melodia). We searched for positively stained cell bodies or apparent terminals containing vasoactive intestinal peptide (VIP), methionine-enkephalin (MET), cholecystokinin (CCK), and substance P (SUB P). Intraventricular colchicine pretreatment was administered to enhance the visualization of peptide-containing cell bodies. Four areas implicated in the central control of song were examined. Three of these areas are sexually dimorphic telencephalic nuclei characteristic of songbirds: the caudal nucleus of the ventral hyperstriatum (HVc), the robust nucleus of the archistriatum (RA), and the magnocellular nucleus of the anterior neostriatum (MAN). The fourth region is the mesencephalic nucleus intercollicullaris (ICo), common to all birds, which contains the dorsomedial nucleus (DM) that appears to be specifically involved in the motor control of song. The pattern of neuropeptide localization was similar between the two species. However, the neuropeptides were heterogeneously dispersed among the four areas. VIP and MET were the most widely distributed, whereas CCK and SUB P were seen only in DM. MAN and HVc revealed remarkably similar patterns of staining for both MET and VIP. Fine varicosities immunolabeled for both these peptides appear to encircle nonreactive somata. In both these nuclei positively stained somata were observed for MET but not for VIP. In RA there was a dense accumulation of MET-positive multipolar cell bodies. VIP-containing neurons were seen in the surrounding archistriatum and caudal neostriatum but not in RA itself. Cell bodies and fibers for all four peptides were observed in DM; in no case were they limited to this subregion, but rather seemed to encompass the surrounding intercollicular area as well. The widespread distribution of VIP and MET strongly suggests a role for these peptides in the acquisition or production of passerine song.

Afferent Pathways↗

Muscarinic cholinergic receptors in the songbird and quail brain: a quantitative autoradiographic study.

In order to clarify the neuroanatomical basis for postulated muscarinic cholinergic control of a wide array of physiological processes in birds, the distribution of muscarinic cholinergic receptors in the brain of three avian species was investigated by quantitative autoradiography. The species consisted of two passerines (songbirds), the European starling (Sturnus vulgaris) and the song sparrow (Melospiza melodia), and one galliform, the Japanese quail (Coturnix coturnix japonica). [3H]N-methyl scopolamine (NMS), a muscarinic cholinergic antagonist was used as the ligand to label the receptors. Initial experiments demonstrated that the binding of this ligand in the three species is saturable in the nanomolar range and has a high affinity (Kd = +/- 0.6 nM). Displacement experiments revealed that three muscarinic ligands competed in an order of potency characteristic of the mammalian muscarinic receptor (i.e., atropine greater than oxotremorine greater than carbachol) for NMS binding in the avian brain. In all three species, portions of the basal ganglia, such as the parolfactory lobe and the paleostriatum augmentatum, exhibited the highest density of binding. On the other hand, the paleostriatum primitivum, the avian homologue of the mammalian globus pallidus, contained very few binding sites. Other telencephalic sites, such as the ventral and dorsal hyperstriatum, also revealed relatively high receptor density. However, the neostriatum and especially the ectostriatum showed much lower levels. In the hypothalamus, in all three species, specific binding could be observed in the ventromedial nucleus and adjacent areas. The paraventricular nucleus also showed moderate levels of binding density, especially in the two songbird taxa. At a more rostral level, the preoptic area showed low levels of binding. In the quail, the sexually dimorphic nucleus of the preoptic area was clearly outlined in the autoradiograms by the low level of binding sites compared to the surrounding areas. In the two passerine species, nuclei of the song system were identified by either high or low levels of NMS binding. High binding defined area X and the mesencephalic nucleus, intercollicularis (ICo). In contrast, the robust nucleus of the archistriatum and the magnocellular nucleus of the anterior neostriatum showed low levels of binding in comparison with the surrounding tissue. None of these nuclei were visible in the quail autoradiograms except for ICo, which appeared as in the passerines as a heavily labelled area surrounding the lightly labelled nucleus mesencephalicus lateralis pars dorsalis. In all three species, the hippocampal complex was devoid of NMS binding except for two lateral dark bands that were present along the entire rostral to caudal extent of the hippocampus.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

Developmental overproduction and selective attrition: new processes in the epigenesis of birdsong.

All phases of song development from infancy to adulthood were studied intensively in a group of laboratory-reared birds. Male swamp sparrows, Melospiza georgiana, trained with tape-recorded songs in infancy, developed song some 8 months later, averaging 2.2 song types per bird. Analysis of the intermediate stage of plastic song revealed that the birds generated 4 to 5 times more song material than was needed for the species-specific song repertoire. The excess was discarded at the time of full song crystallization. Indications that the attrition process is selective include tendencies to retain imitated rather than nonimitated elements, and the rejection of heterospecific elements. Attrition may also be influenced by vocal stimulation at the time of song crystallization, providing an opportunity for behavioral adjustment even though new themes can no longer be learned. Attrition has been described in the transition in human infants from babbling to speech.

Animals↗

Chromosomal aberrations and delays in cell progression induced by X-rays in Tradescantia clone 02 meristems.

In root meristems of Tradescantia clone 02 (developed by Sparrow and his colleagues for mutation studies), X-rays interfere with the progression of cells through the cell cycle and induce chromosomal aberrations in a dose-dependent manner consistent with linear-quadratic kinetics. Sequential mitotic cell accumulations after irradiation indicate that sensitivity to aberration induction is probably greatest in cells from late S to early G2, with chromatid interchanges the most frequent aberration type and all aberrations consistent with initiation from the interaction between two lesions. The ratio of the coefficients in the linear (alpha) and the quadratic (beta) terms (alpha/beta) is equal to the dose average of specific energy produced by individual particles in the site where interaction takes place. The ratio alpha/beta for chromosomal aberrations is similar to that previously found for X-ray-induced mutation in Tradescantia stamen hairs, supporting the proposal that radiation-induced mutational events are due to chromosomal aberrations with interaction distances of about 1 micron. Abrahamson and co-workers have noted that both alpha/beta ratios appear to be related to nuclear target size and are similar for chromosomal and mutational endpoints in the same organism. These findings support this concept; however, it is apparent that any situation which diminishes yield at high doses (eg, mitotic delay) will primarily affect the beta component, resulting in low assessments of interaction site diameters.

Cell Cycle↗

Circadian organization and the role of the pineal in birds.

All organisms exhibit significant daily rhythms in a myriad of functions from molecular levels to the level of the whole organism. Significantly, most of these rhythms will persist under constant conditions, showing that they are driven by an internal circadian clock. In birds the circadian system is composed of several interacting sites, each of which may contain a circadian clock. These sites include the pineal organ, the suprachiasmatic nucleus (SCN) of the hypothalamus, and, in some species, the eyes. Light is the most powerful entraining stimulus for circadian rhythms and, in birds, light can affect the system via three different pathways: the eyes, the pineal, and extraretinal photoreceptors located in the deep brain. Circadian pacemakers in the pineal and in the eyes of some avian species communicate with the hypothalamic pacemakers via the rhythmic synthesis and release of the hormone melatonin. Often the hypothalamic pacemakers are unable to sustain persistent rhythmicity in constant conditions in the absence of periodic melatonin input from the pineal (or eyes). It has also been proposed that pineal pacemakers may be unable to sustain rhythmicity in constant conditions without periodic neural input from the SCN. Significant variation can occur among birds in the relative roles that the pineal, the SCN, and the eyes play within the circadian system; for example, in the house sparrow pacemakers in the pineal play the predominant role, in the pigeon circadian pacemakers in both the pineal and eyes play a significant role, and in Japanese quail ocular pacemakers play the predominant role.

Animals↗

Spontaneous continuous release of spermatozoa and its predawn surge in male passerine birds.

Spontaneous, continuous release of morphologically normal spermatozoa occurs in males of species of passerine (order Passeriformes) birds that were examined. It was demonstrated and studied quantitatively in temporarily captive and isolated house sparrows and house finches by means of repetitive cloacal lavages and extraction of excreta. It is suggested that this phenomenon could be exploited to facilitate comparative and quantitative evaluations of release of spermatozoa in relation to diverse environmental, physiological, and social factors.

Animals↗

Testosterone treatment increases the metabolic capacity of adult avian song control nuclei.

In songbirds, the size of brain nuclei that control song learning and production change seasonally. These changes are mainly controlled by seasonal changes in plasma testosterone (T) concentration. One hypothesis to explain why it may be adaptive for these areas to regress in the fall is that this would decrease the metabolic demand of maintaining a large song system when singing is reduced or absent. We used a marker for cellular metabolism to examine birds with regressed song nuclei and compared them to birds whose song nuclei were induced to grow by administration of exogenous T. Photorefractory male Gambel's white-crowned sparrows were captured during their autumnal migration and kept in outdoor aviaries on a natural photoperiod. We implanted birds with Silastic capsules containing T or with empty implants. Three weeks later the birds were sacrificed. We assayed the brains for cytochrome oxidase (CO) activity and measured the volume of four song nuclei: HVc, RA, 1MAN, and area X. All four nuclei increased in volume in response to T treatment. T treatment increased the metabolic capacity of area X, HVc, and RA relative to surrounding tissue but had no effect on the metabolic capacity of 1MAN. These results support the hypothesis that song nuclei are more metabolically active under the influence of T than they are when plasma T levels are low.

Animals↗

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.

Action Potentials↗

Cellular interactions determine neuronal phenotypes in rodent retinal cultures.

Progenitor cells isolated from early rat embryo retinas differentiate into phenotypes normally generated early in retinal development (e.g., ganglion cells), whereas progenitors isolated from postnatal retinas differentiate into later-generated retinal cell types (e.g., rod photoreceptors; Reh and Kljavin, J. Neurosci. 9:4179-4189; 1989; Adler and Hatlee, 1989; Science 243:391-393; Sparrow, Hicks, and Barnstable, 1990, Dev. Brain Res. 51:69-84). To determine whether this change in committment is intrinsic to the progenitor cells, or alternatively can be modified by interactions with their developing environment, I co-cultured mouse and rat retinal cells, from different developmental stages, and identified the resulting phenotypes with species-specific and cell class-specific antibodies. I found that the phenotypes into which mouse neuroepithelial cells differentiate depends on the phenotypes of the rat cells that surround them. Retinal precursor cells from embryonic day (E) 10-12 will adopt the rod photoreceptor phenotype only when close to cells expressing this phenotype. By contrast, when the E10-12 retinal progenitor cells are cultured with cells from the cerebral cortex, they differentiate primarily into large multipolar neurons, similar in their morphology and antigen expression to retinal ganglion cells. These results indicate that interactions among the cells of the developing retina are important in the determination of cell fate.

Animals↗

The timing of song memorization differs in males and females: a new assay for avian vocal learning

We describe a new assay for measuring the acquisition phase of song learning in birds and compare it with the standard method of comparing a pupil's imitation to his tutor's song. Juvenile male and female white-crowned sparrows, Zonotrichia leucophrysgive call notes in response to playback of species-typical song. After 10-day periods of tape tutoring conducted in the first 50 days of life, subjects gave significantly more calls in response to tutor songs than to novel songs. An identical procedure conducted at a later age yielded a different result. Birds did not distinguish tutor from novel songs in winter, after the sensitive phase for song acquisition. Males gave significantly more calls to those tutor songs that they subsequently sang the next spring than to tutor songs they did not reproduce. Assuming that the call assay correlates with long-term storage of songs in females as it does in males, these results also indicate that the sensitive phase for song acquisition is shorter in females than in males of this species.1997The Association for the Study of Animal Behaviour

Journal Article↗

Combined aromatase inhibitor and antiandrogen treatment decreases territorial aggression in a wild songbird during the nonbreeding season.

Male song sparrows (Melospiza melodia morphna) defend territories throughout the year in western Washington State. In the nonbreeding season (autumn and winter), aggression and song are robustly expressed but plasma testosterone (T) levels are basal. Also, castration does not decrease nonbreeding territoriality. In this field experiment, we asked whether nonbreeding aggression is independent of T. T can act via androgen receptors or T can be aromatized to 17beta-estradiol (E(2)) and act via estrogen receptors. We treated free-living nonbreeding birds with an aromatase inhibitor (ATD) and an androgen receptor antagonist (flutamide) in combination. We then challenged subjects with a live decoy and playback of tape-recorded songs. ATD+flutamide treatment decreased several aggressive behaviors. However, ATD+flutamide treatment did not affect body condition, suggesting that subjects were healthy and that foraging behavior was not reduced. As expected, ATD+flutamide treatment increased plasma T, probably by blocking negative feedback on luteinizing hormone. Surprisingly, ATD+flutamide treatment increased plasma E(2). Most other studies using aromatase inhibitors have not measured plasma E(2). However, it is possible that ATD+flutamide treatment decreased local E(2) levels in the brain but not in plasma. Finally, ATD+flutamide treatment increased plasma corticosterone, perhaps in response to increased plasma T or E(2). To our knowledge, these are the first data to suggest that nonbreeding territoriality is regulated by endogenous steroid hormones. Nongonadal production of sex steroids may support aggression in the nonbreeding season.

Aggression↗

Neurally active stress peptide inhibits territorial defense in wild birds.

It is unclear whether the behavioral effects of peptides in laboratory studies always reflect natural conditions. Here we test whether we can detect measurable behavioral changes after rapidly injecting peptides into the brains of wild birds. We used a modified stereotaxic-like technique to inject corticotrophin-releasing factor (CRF) and arginine vasotocin (AVT, the nonmammalian form of arginine vasopressin), two hormones important in the stress response, into the brains of wild, freely behaving, male white-crowned sparrows (Zonotrichia leucophrys). We then monitored subsequent territorial behavior to determine whether CRF or AVT altered this behavior. Surprisingly, the potent stressors of capture and surgery did not eliminate territorial behavior, with many birds resuming territorial defense within 60-90 min after surgery. Centrally acting CRF, however, significantly reduced territorial defense whereas centrally acting AVT had no effect. These results indicate that the behavioral affects of peptides can be studied under natural conditions.

Animals↗

Stimulatory effects on the reproductive axis in female songbirds by conspecific and heterospecific male song.

Courtship vocalizations of male songbirds can profoundly enhance the reproductive physiology and behavior of conspecific females. However, no study has fully investigated the selectivity of conspecific song effects on reproductive development in birds. We studied the effects of conspecific and heterospecific song on reproductive development in domesticated (canaries) and wild songbirds (song sparrows). As expected, conspecific song enhanced follicular development. Unexpectedly, however, birds exposed to heterospecific song also underwent enhanced follicular development (compared to birds exposed to no song); conspecific and heterospecific songs were equally effective in enhancing ovarian development. In canaries exposed to 18L:6D, conspecific song induced oviposition earlier and at a greater frequency than in heterospecific and no song groups, with the fewest eggs being laid in the no song group. These results indicate that conspecific and heterospecific male song can enhance reproductive activity in female songbirds. Whether or not activation of the reproductive axis in female songbirds by heterospecific song occurs in the wild remains unclear. It is also unclear as to whether the ability of the reproductive axis to respond to heterospecific song performs a specific function, or whether it is simply a consequence of greater selection pressure acting upon behavioral responses to song.

Animals↗

A molecular phylogeny of warbling-finches (Poospiza): paraphyly in a neotropical Emberizid genus.

We investigated the phylogenetic relationships of 12 species within a single genus of neotropical passerine (Poospiza) using 849 bp (283 codons) of the cytochrome b mitochondrial gene. We further explored evolutionary affinities of these taxa using sequence from an additional 47 thraupine (tanagers) and 7 emberizine (sparrows and buntings) genera, members of the predominantly New World family Emberizidae. Poospiza have traditionally been considered part of the emberizine radiation. However, our analyses suggest that members of this genus are more closely related to some thraupine lineages than they are to the other neotropical emberizine genera included in our study (Atlapetes, Embernagra, Melopyrrha, Phrygilus, Saltatricula, Tiaris). Although member taxa are closely related, the genus Poospiza appears to be paraphyletic with representatives of 6 thraupine genera (Cnemoscopus, Cypsnagra, Hemispingus, Nephelornis, Pyrrhocoma, Thylpopsis) interspersed among four well-supported Poospiza clades. The majority of species within this Poospiza-thraupine clade have geographic ranges that are exclusive to, or partially overlap with, the Andes Mountains. It is probable that these mountains have played an important role in driving cladogenesis within this group. Sequence divergence (transversions only; mean 4.7+/-1.3%) within the clade suggests that much of this diversification occurred within the late Miocene and Pliocene, a period coincident with major orogenic activity in central-western South America.

Animals↗