Eliot A. Brenowitz

Seasonal plasticity in the adult brain

Seasonal plasticity of structure and function is a fundamental feature of nervous systems in a wide variety of animals that occupy seasonal environments. Excellent examples of seasonal brain changes are found in the avian song control system, which has become a leading model of morphological and functional plasticity in the adult CNS. The volumes of entire brain regions that control song increase dramatically in anticipation of the breeding season. These volumetric changes are induced primarily by vernal increases in circulating sex steroids and are accompanied by increases in neuronal size, number and spacing. In several species, these structural changes in the song control circuitry are associated with seasonal changes in song production and learning. Songbirds provide important insights into the mechanisms and behavioral consequences of plasticity in the adult brain.

Comparative approaches to the avian song system

There is extensive diversity among the 4000 species of songbirds in different aspects of song behavior, including the timing of vocal learning, sex patterns of song production, number of songs that are learned (i.e., repertoire size), and seasonality of song behavior. This diversity provides unparalleled opportunities for comparative studies of the relationship between the structure and function of brain regions and song behavior. The comparative approach has been used in two contexts: (a) to test hypotheses about mechanisms of song control, and (b) to study the evolution of the control system in different groups of birds. In the first context, I review studies in which a comparative approach has been used to investigate sex differences in the song system, the relationship between the number of song types a bird sings and the size of the song nuclei, and seasonal plasticity of the song control circuits. In the second context, I discuss whether the vocal control systems of parrots and songbirds were inherited from a common ancestor or independently evolved. I also consider at what stage in the phylogeny of songbirds the hormone-sensitive forebrain circuit found in modern birds first evolved. I conclude by identifying directions for future research in which a comparative approach would be productive.

Song learning in birds: diversity and plasticity, opportunities and challenges

A common trend in neuroscience is convergence on selected model systems. Underlying this approach is an often implicit assumption that mechanisms observed in one species are characteristic of all related species. Although the model system approach has been extremely productive, it might not account for all of the mechanistic differences between species that differ behaviourally. Using the neural system that regulates song learning in songbirds as an example, we demonstrate how integrating model system and comparative approaches can lead to a more complete picture of neural mechanisms, and can resolve issues raised by a focus on selected species.

Plasticity of the adult avian song control system

Abstract: There is extensive plasticity of the song behavior of birds and the neuroendocrine circuit that regulates this behavior in adulthood. One of the most pronounced examples of plasticity, found in every species of seasonally breeding bird examined, is the occurrence of large seasonal changes in the size of song control nuclei and in their cellular attributes. This seasonal plasticity of the song circuits is primarily regulated by changes in the secretion and metabolism of gonadal testosterone (T). Both androgenic and estrogenic sex steroids contribute to seasonal growth of the song system. These steroids act directly on the forebrain song nucleus HVC, which then stimulates growth of its efferent target nuclei transsynaptically. Seasonal growth and regression of the song circuits occur rapidly and sequentially following changes in circulating T and its metabolites. As the neural song circuits change across seasons, there are changes in different aspects of song behavior, including the structural stereotypy of songs, their duration, and the rate of production. The burden of evidence supports a model in which changes in song behavior are a consequence rather than a cause of the changes in the song circuits of the brain. Seasonal plasticity of the song system may have evolved as an adaptation to reduce the energetic demands imposed by these regions of the brain outside the breeding season, when the use of song for mate attraction and territorial defense is reduced or absent. The synaptic plasticity that accompanies seasonal changes in the song system may have acted as a preadaptation that enabled the evolution of adult song learning in some species of birds.

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 Gambels 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.

Dehydroepiandrosterone (DHEA) increases territorial song and the size of an associated brain region in a male songbird.

In many species, male territorial aggression is tightly coupled with gonadal secretion of testosterone (T). In contrast, in song sparrows (Melospiza melodia morphna), males are highly aggressive during the breeding (spring) and nonbreeding (autumn and early winter) seasons, but not during molt (late summer). In aggressive nonbreeding song sparrows, plasma T levels are basal (< or = 0.10 ng/ml), and castration has no effect on aggression. However, aromatase inhibitors reduce nonbreeding aggression, indicating a role for estrogen in wintering males. In the nonbreeding season, the substrate for brain aromatase is unclear, because plasma T and androstenedione levels are basal. Aromatizable androgen may be derived from plasma dehydroepiandrosterone (DHEA), an androgen precursor. DHEA circulates at elevated levels in wintering males (approximately 0.8 ng/ml) and might be locally converted to T in the brain. Moreover, plasma DHEA is reduced during molt, as is aggression. Here, we experimentally increased DHEA in wild nonbreeding male song sparrows and examined territorial behaviors (e.g., singing) and discrete neural regions controlling the production of song. A physiological dose of DHEA for 15 days increased singing in response to simulated territorial intrusions. In addition, DHEA treatment increased the volume of a telencephalic brain region (the HVc) controlling song, indicating that DHEA can have large-scale neuroanatomical effects in adult animals. The DHEA treatment also caused a slight increase in plasma T. Exogenous DHEA may have been metabolized to sex steroids within the brain to exert these behavioral and neural effects, and it is also possible that peripheral metabolism contributed to these effects. These are the first results to suggest that exogenous DHEA increases male-male aggression and the size of an entire brain region in adults. The data are consistent with the hypothesis that DHEA regulates territorial behavior, especially in the nonbreeding season, when plasma T is basal.

Seasonal changes in androgen receptor immunoreactivity in the song nucleus HVc of a wild bird.

In seasonally breeding songbirds, song behavior and neural morphology change seasonally. Song control nuclei are larger during the breeding season, as determined by multiple cytological labels. Seasonal changes in song nuclei are regulated by testosterone (T), and several song nuclei contain intracellular androgen receptors (AR). Changes in AR levels may interact with changes in plasma T levels to regulate song nuclei morphology.

SEASONAL PLASTICITY AND SEXUAL DIMORPHISM IN THE AVIAN SONG CONTROL SYSTEM: STEREOLOGICAL MEASUREMENT OF NEURON DENSITY AND NUMBER

Differences in neuron density and number are associated with seasonal plasticity and sexual dimorphism in the avian song control system. In previous studies, neuron density and number in this system have been quantified primarily through nonstereological approaches in thick tissue sections by using the nucleolus as the unit of count. The reported differences between seasons and sexes may be inaccurate due to biases introduced by neuron splitting during sectioning. We used the unbiased optical disector technique on tissue from three previous studies (two investigations of seasonal plasticity and one investigation of sexual dimorphism in avian song nuclei) to assess seasonal and sex differences in neuron density and number. In two song nuclei, HVc and the robust nucleus of the archistriatum (RA), the optical disector yielded intergroup differences in neuron density and number that coincided well with the three previous reports.

A field study of seasonal neuronal incorporation into the song control system of a songbird that lacks adult song learning

Adult songbirds can incorporate new neurons into HVc, a telencephalic song control nucleus. Neuronal incorporation into HVc is greater in the fall than in the spring in adult canaries (open-ended song learners) and is temporally related to seasonal song modification. We used the western song sparrow, a species that does not modify its adult song, to test the hypothesis that neuronal incorporation into adult HVc is not seasonally variable in age-limited song learners. Wild song sparrows were captured during the fall and the spring, implanted with osmotic pumps containing [3H]thymidine, released onto their territories, and recaptured after 30 days. The density, proportion, and number of new HVc neurons were all significantly greater in the fall than in the spring. There was also a seasonal change in the incorporation of new neurons into the adjacent neostriatum that was less pronounced than the change in HVc. This is the first study of neuronal recruitment into the song control system of freely ranging wild songbirds. These results indicate that seasonal changes in HVc neuronal incorporation are not restricted to open-ended song learners. The functional significance of neuronal recruitment into HVc therefore remains elusive.

Acoustic communication in spring peepers - Call characteristics and neurophysiological aspects

SummarySpectral and amplitude features of the advertisement call of male spring peeper tree frogs (Hyla crucifer) were analyzed and compared to the physiological characteristics of the peripheral auditory system in both males and females determined by single unit electrophysiological recording in the VIIIth cranial nerve. The call is a very simple, nearly tonal signal with a single spectral peak (mean for the population = 2,895 Hz) and little or no harmonic or internal temporal structure. The electrophysiological results show two populations of auditory fibers in the VIIIth nerve with characteristics similar to those in other anurans. One population, presumably from the amphibian papilla, contains units tuned below 1,200 Hz. A second, high frequency population is also present, and presumably arises from the basilar papilla (BP). A sexual dimorphism is apparent in the tuning of BP units. Female BPs are tuned between 2,100 and 3,700 Hz (X= 2,939 Hz) while male BPs are tuned between 3,350 and 4,000 Hz (X= 3,580). Thus in this species the advertisement call is detected only by the basilar papilla. The BP of females is tuned to the call while the male BP is mismatched. Males can still detect the call with the lower flanks of their BP tuning curves, however, but the detection threshold will be much higher than in the females. Therefore the male advertisement call will be far more audible to females than to males.