Adult Male White-crowned Sparrows Research Articles

Adult Neurogenesis Leads to the Functional Reconstruction of a Telencephalic Neural Circuit.

Seasonally breeding songbirds exhibit pronounced annual changes in song behavior, and in the morphology and physiology of the telencephalic neural circuit underlying production of learned song. Each breeding season, new adult-born neurons are added to the pallial nucleus HVC in response to seasonal changes in steroid hormone levels, and send long axonal projections to their target nucleus, the robust nucleus of the arcopallium (RA). We investigated the role that adult neurogenesis plays in the seasonal reconstruction of this circuit. We labeled newborn HVC neurons with BrdU, and RA-projecting HVC neurons (HVCRA) with retrograde tracer injected in RA of adult male white-crowned sparrows (Zonotrichia leucophrys gambelii) in breeding or nonbreeding conditions. We found that there were many more HVCRA neurons in breeding than nonbreeding birds. Furthermore, we observed that more newborn HVC neurons were back-filled by the tracer in breeding animals. Behaviorally, song structure degraded as the HVC-RA circuit degenerated, and recovered as the circuit regenerated, in close correlation with the number of new HVCRA neurons. These results support the hypothesis that the HVC-RA circuit degenerates in nonbreeding birds, and that newborn neurons reconstruct the circuit in breeding birds, leading to functional recovery of song behavior. We investigated the role that adult neurogenesis plays in the seasonal reconstruction of a telencephalic neural circuit that controls song behavior in white-crowned sparrows. We showed that nonbreeding birds had a 36%-49% reduction in the number of projection neurons compared with breeding birds, and the regeneration of the circuit in the breeding season is due to the integration of adult-born projection neurons. Additionally, song structure degraded as the circuit degenerated and recovered as the circuit regenerated, in close correlation with new projection neuron number. This study demonstrates that steroid hormones can help reestablish functional neuronal circuits following degeneration in the adult brain and shows non-injury-induced degeneration and reconstruction of a neural circuit critical for producing a learned behavior.

The Role of Neurotrophins in the Seasonal-Like Growth of the Avian Song Control System

The avian song control system undergoes pronounced seasonal plasticity in response to photoperiod and hormonal cues. The action of testosterone (T) and its metabolites in the song nucleus HVC is both necessary and sufficient to promote breeding season-like growth of its efferent nuclei RA (robust nucleus of the arcopallium) and Area X, suggesting that HVC may release a trophic factor such as brain-derived neurotrophic factor (BDNF) into RA and X. BDNF is involved in many forms of adult neural plasticity in other systems and is present in the avian song system. We used a combination of in situ hybridization and intracerebral infusions to test whether BDNF plays a role in the seasonal-like growth of the song system in adult male white-crowned sparrows. BDNF mRNA levels increased in HVC in response to breeding conditions, and BDNF infusion into RA was sufficient to promote breeding-like changes in somatic area and neuronal density. Expression of the mRNA for the Trk B receptor of BDNF, however, did not vary with seasonal conditions in either HVC or RA. Local blockade of BDNF activity in RA via infusion of Trk-Fc fusion proteins inhibited the response to breeding conditions. Our results indicate that BDNF is sufficient to promote the seasonal plasticity in somatic area and cell density in RA, although NT-3 may also contribute to this process, and suggest that HVC may be a presynaptic source of increased levels of BDNF in RA of breeding-condition birds.

Neurogenesis in an Adult Avian Song Nucleus Is Reduced by Decreasing Caspase-Mediated Apoptosis

Neuron death and replacement are fundamental components of brain plasticity. Much remains unknown, however, about the mechanistic interaction between neuron death and neurogenesis in adult vertebrates. In seasonally breeding adult male white-crowned sparrows, the song system nucleus HVC loses approximately 26% of its neurons via caspase-dependent apoptosis within 4 d after a transition to nonbreeding physiological conditions. To determine whether neuronal death is necessary for the recruitment of new neurons, we infused caspase inhibitors into HVC in vivo and suppressed neurodegeneration for at least 20 d after the transition to nonbreeding conditions. The blockade of HVC neuron death reduced the number and density of new neurons recruited to the ipsilateral HVC by 48 and 29%, respectively, compared with contralateral HVC. Our results are the first to show that reducing neuronal death in the adult brain decreases the recruitment of new neurons.

Rapid seasonal-like regression of the adult avian song control system

We analyzed how rapidly avian song control nuclei regress after testosterone (T) withdrawal. Regression of neuronal attributes resulting from T withdrawal has been observed in several animal models. The time course over which regression occurs is not known, however. To address this issue, we castrated adult male white-crowned sparrows and rapidly shifted them to short-day photoperiods after being held under breeding conditions (long-day photoperiod and systemic T exposure) for 3 weeks. We found that the volume of one song nucleus, HVC, regressed 22% within 12 h after T withdrawal. Changes in HVC neuron density after T withdrawal were dynamic; density increased at 12 h and then decreased by 4 days. HVC neuron number was reduced by 26% by 4 days. The volumes of Area X and the robust nucleus of the arcopallium (RA) were significantly regressed by 7 and 20 days, respectively. RA somatic area and neuronal spacing were significantly reduced by 2 days. The rapidity of HVC regression is unprecedented among vertebrate models of hormone-sensitive neural circuits. These results reveal that the rapid regression of the song control system provides a model for the important role sex steroid hormones play in mediating adult neural plasticity and in neuroprotection.

Androgens and estrogens induce seasonal-like growth of song nuclei in the adult songbird brain.

In seasonally breeding songbirds, the brain regions that control song behavior undergo dramatic structural changes at the onset of each annual breeding season. As spring approaches and days get longer, gonadal testosterone (T) secretion increases and triggers the growth of several song control nuclei. T can be converted to androgenic and estrogenic metabolites by enzymes expressed in the brain. This opens the possibility that the effects of T may be mediated via the androgen receptor, the estrogen receptor, or both. To test this hypothesis, we examined the effects of two bioactive T metabolites on song nucleus growth and song behavior in adult male white-crowned sparrows. Castrated sparrows with regressed song control nuclei were implanted with silastic capsules containing either crystalline T, 5alpha-dihydrotestosterone (DHT), estradiol (E(2)), or a combination of DHT+E(2). Control animals received empty implants. Song production was highly variable within treatment groups. Only one of seven birds treated with E(2) alone was observed singing, whereas a majority of birds with T or DHT sang. After 37 days of exposure to sex steroids, we measured the volumes of the forebrain song nucleus HVc, the robust nucleus of the archistriatum (RA), and a basal ganglia homolog (area X). All three steroid treatments increased the volumes of these three song nuclei when compared to blank-implanted controls. These data demonstrate that androgen and estrogen receptor binding are sufficient to trigger seasonal song nucleus growth. These data also suggest that T's effects on seasonal song nucleus growth may depend, in part, upon enzymatic conversion of T to bioactive metabolites.

Act locally and think globally: intracerebral testosterone implants induce seasonal-like growth of adult avian song control circuits.

There is pronounced seasonal plasticity in the morphology of the neural circuits that regulate song behavior in adult songbirds, primarily in response to changes in plasma testosterone (T) levels. Most song nuclei have androgen receptors. Afferent input from the telencephalic nucleus HVc (also known as the "high vocal center") is necessary for seasonal growth of the direct efferent target nuclei RA and area X. We asked here whether T-stimulated growth of HVc is sufficient to induce growth of its efferent nuclei. Intracerebral T implants were placed unilaterally near HVc or RA in photosensitive adult male white-crowned sparrows for one month. The T implant near HVc produced significant growth of the ipsilateral (but not contralateral) HVc, RA, and area X, and increased neuronal number in the ipsilateral HVc. The T implant near RA did not produce selective growth of ipsilateral RA, HVc, or area X. Intracerebral T implants did not elevate plasma T levels, nor did they stimulate growth of two peripheral androgen sensitive targets, the syrinx and the cloacal protuberance. These results suggest that seasonal growth of the adult song circuits results from T acting directly on HVc, which then stimulates the growth of RA and area X transynaptically.

Breeding Conditions Induce Rapid and Sequential Growth in Adult Avian Song Control Circuits: A Model of Seasonal Plasticity in the Brain

In adult songbirds, seasonal changes in photoperiod and circulating testosterone (T) stimulate structural changes within the neural song control circuitry. The mechanisms that control this natural plasticity are poorly understood. To determine how quickly and in what sequence the song nuclei respond to changing daylength and circulating T, we captured 18 adult male white-crowned sparrows and kept them on short days for 12 weeks. We killed five of these birds and exposed the rest to long days (LD) and elevated T. We killed these birds either 7 or 20 d after LD + T exposure. We measured song nuclei volumes and cellular attributes, the mass of the vocal production organ (the syrinx), and song behavior. The neostriatal song control nucleus HVC (also known as "high vocal center"), added 50,000 neurons and increased in size within 7 d of exposure to LD + T. Efferent targets of HVC, the robust nucleus of the archistriatum (RA), and area X of the parolfactory lobe grew more slowly and were not significantly larger until day 20 of the study. The tracheosyringeal portion of the hypoglossal nucleus (nXIIts), which receives projections from RA and normally grows in response to seasonal cues, did not grow over the time course of this study. Syringeal mass increased within 7 d of LD + T treatment. The anatomical changes in the brain were accompanied by behavioral changes in song production. On day 7 when the song circuitry was incompletely developed, male sparrows sang less stereotyped songs than males at day 20 with more completely developed song circuits. These results suggest that the song circuitry responds rapidly and sequentially to breeding-typical conditions (long days and elevated T), and that song stereotypy increases as nuclei within this circuitry grow.

Anterior forebrain pathway is needed for stable song expression in adult male white-crowned sparrows ( Zonotrichia leucophrys)

The anterior forebrain pathway of the avian song system is involved in juvenile song learning, but its function in adult song behavior is not known. This report uses lesions to study the role of a particular forebrain nucleus, lMAN, in the seasonal regeneration of song in adult white-crowned sparrows ( Zonotrichia leucophrys oriantha). White-crowned sparrows, even when acoustically isolated as juveniles, crystallize a single song which they maintain throughout adulthood. The lateral portion of the magnocellular nucleus of the anterior neostriatum (lMAN) was lesioned bilaterally in adult males maintained on short days (8 h of light). Daylength was increased to 16 h following the surgeries, and all birds were recorded in the post-lesion singing season. Lesioned birds showed a large decrease in song note frequency following the lesions, significantly larger than did intact, age-matched controls. Further changes were seen in the post-lesion songs of seven of 11 successfully lesioned males. These changes included variability in song pattern, loss of frequency control and addition of new notes, some of which had been practiced during juvenile song development. These changes seemed especially large in birds that had either been acoustically isolated or had not fully copied a tape-tutor song during juvenile song development. These results are the first to indicate that the motor memories for song elements that had been practiced and discarded early in life are retained, and they suggest that lMAN affects seasonal song expression by selectively reinforcing a particular song pattern.

Social Tutoring of Adult Male White-Crowned Sparrows

Journal Article Social Tutoring of Adult Male White-Crowned Sparrows Get access Richard M. Casey, Richard M. Casey Department of Biology, Colorado State University, Ft. Collins, CO 80523 Search for other works by this author on: Oxford Academic Google Scholar Myron C. Baker Myron C. Baker Department of Biology, Colorado State University, Ft. Collins, CO 80523 Search for other works by this author on: Oxford Academic Google Scholar The Condor, Volume 95, Issue 3, 1 August 1993, Pages 718–723, https://doi.org/10.2307/1369617 Published: 01 August 1993 Article history Received: 09 November 1992 Accepted: 23 February 1993 Published: 01 August 1993

Evidence for androgen independence of male mounting behavior in white-crowned sparrows ( Zonotrichia leucophrys gambelii)

Previous experiments have shown that expression of mounting behavior in sexually inexperienced, adult male white-crowned sparrows does not require elevated plasma levels of androgen; adult males maintained on nonstimulatory short days mount sexually receptive females. The experiments reported here demonstrate that (1) sexually inexperienced, prepubertal males maintained on nonstimulatory short days show very low mounting rates in response to female sexual displays; (2) these males exhibit high mounting rates when exposed to stimulatory long days but androgen treatment on short days is ineffective in stimulating high mounting rates; and (3) prepubertal castration has no effect on the expression of mounting behavior by photostimulated adult males. Thus, there is no evidence that mounting behavior of adult male white-crowned sparrows depends on androgen.

Responses of Photosensitive and Photorefractory Male White-crowned Sparrows (Zonotrichia leucophrys gambelii) to Synthetic Mammalian Luteinizing Hormone Releasing Hormone (Syn-LHRH)

To assess a possible role of the adenohypophysis in photorefractoriness, photosensitive and photorefractory adult male white-crowned sparrows (Zonotrichia leucophrys) were treated with single intravenous injections of 0, 0.5, 5, 20, 35, 50 or 500 ng of synthetic luteinizing hormone releasing hormone (Syn-LHRH) in 0.9% saline solution. Serial samples of plasma were taken immediately before and at 5, 20 and 60 min after injection. The plasma level of immunoreactive luteinizing hormone (irLH) was not altered by the injection of saline solution alone, or by 0.5 or 5 ng Syn-LHRH in either photosensitive or photorefractory birds. Treatment with 20, 35, 50 or 500 ng Syn-LHRH, however, elicited significant and approximately equal increases in plasma levels of irLH in both groups 5 min after injection. These responses are consistent with the hypothesis that the site of photorefractoriness is at a level higher than the adenohypophysis.

Formation of secondary neurohemal organs in the median eminence of the White-crowned Sparrow and Japanese quail

Midline electrolytic or radio frequency lesions were placed in the basal hypothalamus of adult male White-crowned Sparrows and Japanese quail. In White-crowned Sparrows, destruction of the neurohemal organs of the stainable hypothalamo-hypophysial neurosecretory system in the neural lobe (NL) and/or palisade layer of the anterior division of the median eminence (AME) resulted in the formation of large aggregations of stainable neurosecretory material (NSM) surrounding hypertrophied capillaries. Very few of these occurred in quail. These structures, herein referred to as secondary neurohemal organs, were located in the AME dorsal to that region in which NSM is usually found. In normal birds, this region was relatively devoid of capillaries. Interruption of fibers of the supraopticohypophysial tract dorsal to the median eminence was not conducive to formation of these structures. Damage to the stainable neurosecretory system of quail was apparently permanent, as practically no indication of repair was seen. It is suggested that secondary neurohemal organs in the White-crowned Sparrow may represent neurovascular organs of the NL and/or AME, and may function accordingly.