Neural Correlates of Behavioural Olfactory Sensitivity Changes Seasonally in European Starlings

Possibly due to the small size of the olfactory bulb (OB) as compared to rodents, it was generally believed that songbirds lack a well-developed sense of smell. This belief was recently revised by several studies showing that various bird species, including passerines, use olfaction in many respects of life. During courtship and nest building, male European starlings (Sturnus vulgaris) incorporate aromatic herbs that are rich in volatile compounds (e.g., milfoil, Achillea millefolium) into the nests and they use olfactory cues to identify these plants. Interestingly, European starlings show seasonal differences in their ability to respond to odour cues: odour sensitivity peaks during nest-building in the spring, but is almost non-existent during the non-breeding season.This study used repeated in vivo Manganese-enhanced MRI to quantify for the first time possible seasonal changes in the anatomy and activity of the OB in starling brains. We demonstrated that the OB of the starling exhibits a functional seasonal plasticity of certain plant odour specificity and that the OB is only able to detect milfoil odour during the breeding season. Volumetric analysis showed that this seasonal change in activity is not linked to a change in OB volume. By subsequently experimentally elevating testosterone (T) in half of the males during the non-breeding season we showed that the OB volume was increased compared to controls.By investigating the neural substrate of seasonal olfactory sensitivity changes we show that the starlings' OB loses its ability during the non-breeding season to detect a natural odour of a plant preferred as green nest material by male starlings. We found that testosterone, applied during the non-breeding season, does not restore the discriminatory ability of the OB but has an influence on its size

Own Song Selectivity in the Songbird Auditory Pathway: Suppression by Norepinephrine

Like human speech, birdsong is a learned behavior that supports species and individual recognition. Norepinephrine is a catecholamine suspected to play a role in song learning. The goal of this study was to investigate the role of norepinephrine in bird's own song selectivity, a property thought to be important for auditory feedback processes required for song learning and maintenance.Using functional magnetic resonance imaging, we show that injection of DSP-4, a specific noradrenergic toxin, unmasks own song selectivity in the dorsal part of NCM, a secondary auditory region.The level of norepinephrine throughout the telencephalon is known to be high in alert birds and low in sleeping birds. Our results suggest that norepinephrine activity can be further decreased, giving rise to a strong own song selective signal in dorsal NCM. This latent own song selective signal, which is only revealed under conditions of very low noradrenergic activity, might play a role in the auditory feedback and/or the integration of this feedback with the motor circuitry for vocal learning and maintenance

Topography and Lateralized Effect of Acute Aromatase Inhibition on Auditory Processing in a Seasonal Songbird

It is increasingly recognized that brain-derived estrogens (neuroestrogens) can regulate brain physiology and behavior much faster than what was previously known from the transcriptional action of estrogens on nuclear receptors. One of the best examples of such neuro- modulation by neuroestrogens concerns the acute regulation of sensory coding by the auditory cortex as demonstrated by electrophys- iological studies of selected neurons in zebra finches. Yet, the spatial extent of such modulation by neuroestrogens is not known. Using functional magnetic resonance imaging, we demonstrate here that acute estrogen depletion alters within minutes auditory processing in male European starlings. These effects are confined to very specific but large areas of the auditory cortex. They are also specifically lateralized to the left hemisphere. Interestingly, the modulation of auditory responses by estrogens was much larger (both in amplitude and in topography) in March than in December or May/June. This effect was presumably independent from changes in circulating testosterone concentrations since levels of the steroid were controlled by subcutaneous implants, thus suggesting actions related to other aspects of the seasonal cycle or photoperiodic manipulations. Finally, we also show that estrogen production specifically modulates selectivity for behaviorally relevant vocalizations in a specific part of the caudomedial nidopallium. These findings confirm and extend previous conclusions that had been obtained by electrophysiological techniques. This approach provides a new very powerful tool to investigate auditory responsiveness in songbirds and its fast modulation by sex steroids

The starling auditory brain shows selectivity for songs used in individual recognition

Prix du meilleur posterInternational audience[No abstract

Functional changes between seasons in the male songbird auditory forebrain

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.International audienceSongbirds are an excellent model for investigating the perception of learned complex acoustic communication signals. Male European starlings (Sturnus vulgaris) sing throughout the year distinct types of song that bear either social or individual information. Although the relative importance of social and individual information changes seasonally, evidence of functional seasonal changes in neural response to these songs remains elusive. We thus decided to use in vivo functional magnetic resonance imaging (fMRI) to examine auditory responses of male starlings that were exposed to songs that convey different levels of information (species-specific and group identity or individual identity), both during (when mate recognition is particularly important) and outside the breeding season (when group recognition is particularly important). We report three main findings: (1) the auditory area caudomedial nidopallium (NCM), an auditory region that is analogous to the mammalian auditory cortex, is clearly involved in the processing/categorization of conspecific songs; (2) season-related change in differential song processing is limited to a caudal part of NCM; in the more rostral parts, songs bearing individual information induce higher BOLD responses than songs bearing species and group information, regardless of the season; (3) the differentiation between songs bearing species and group information and songs bearing individual information seems to be biased toward the right hemisphere. This study provides evidence that auditory processing of behaviorally-relevant (conspecific) communication signals changes seasonally, even when the spectro-temporal properties of these signals do not change

Seasonal changes in selectivity for individual male song in a female songbird basal ganglia nucleus

International audienceIn seasonally breeding songbirds, such as European starlings (Sturnus vulgaris), male song plays a direct role in immediate mate attraction during, but not outside of, the breeding season. The present experiment was designed to explore whether female starlings would display differential neural responses to male song during and outside of the breeding season. Starlings are highly social songbirds whose songs show different levels of variations that reflect not only species-specific but also individual-specific identity. Taking advantage of the whole-brain approach allowed by functional Magnetic Resonance Imaging (fMRI), we measured the neural responses to these songs in medetomidine-anesthetized adult female starlings (N=11) in both the breeding (spring) and the non-breeding (fall) seasons. Subjects were exposed to synthetic pure tones and to two types of male starling song: species-specific songs (used in species and population recognition) and individual conspecific songs (used in individual recognition). The direct comparison of the neural activation elicited by songs used in individual recognition, as compared to species-specific songs, revealed that perception of individual male songs induced a greater activity in the regions analogous to the auditory cortex of mammals (Field L and caudomedial nidopallium (NCM)) and in a basal ganglia homolog called Area X. There were however differences within these regions according to the season. Whereas the dorso-caudal part of NCM showed the same selectivity for individual male songs in both seasons (unlike male starlings), Area X showed this selectivity only during the breeding season. In the non-breeding season, selectivity for individual male songs was not present anymore in Area X. Responses to synthetic pure tone stimuli remained unchanged between the seasons, indicating that this seasonal change in selectivity for individual stimuli in Area X was not due to a change in auditory perception as a whole. Finally, the data seems to suggest lateralization of selectivity for individual songs towards the left basal ganglia. These results suggest that seasons impact auditory processing and that a differential representation of sounds with distinct biological significance is thus observed between seasons. This opens questions about a potential neural substrate for the extraction of biologically relevant information used in vocal communication