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1.  Blocking estradiol synthesis affects memory for songs in auditory forebrain of male zebra finches 
Neuroreport  2012;23(16):922-926.
Estradiol (E2) has recently been shown to modulate sensory processing in an auditory area of the songbird forebrain, the caudomedial nidopallium (NCM). When a bird hears conspecific song, E2 increases locally in NCM, where neurons express both the aromatase enzyme that synthesizes E2 from precursors and estrogen receptors. Auditory responses in NCM show a form of neuronal memory: repeated playback of the unique learned vocalizations of conspecific individuals induces long-lasting stimulus specific adaptation (SSA) of neural responses to each vocalization. In order to test the role of E2 in this auditory memory, we treated adult male zebra finches (n=16) with either the aromatase inhibitor Fadrozole (FAD) or saline for 8 days. We then exposed them to “training” songs and, 6h later, recorded multiunit auditory responses with an array of 16 microelectrodes in NCM. Adaptation rates (a measure of SSA) to playbacks of training and novel songs were computed, using established methods, to provide a measure of neuronal memory. Recordings from FAD-treated birds showed significantly reduced memory for the training songs compared to saline-treated controls, while auditory processing for novel songs did not differ between treatment groups. In addition, FAD did not change the response bias in favor of conspecific over heterospecific song stimuli. Our results show that E2 depletion affects the neuronal memory for vocalizations in songbird NCM, and suggest that E2 plays a necessary role in auditory processing and memory for communication signals.
doi:10.1097/WNR.0b013e3283588b61
PMCID: PMC4322868  PMID: 22955141
songbirds; NCM; auditory processing; estradiol; memory; stimulus specific adaptation; animal vocalization; species specificity
2.  Hemispheric Asymmetry in New Neurons in Adulthood Is Associated with Vocal Learning and Auditory Memory 
PLoS ONE  2014;9(9):e108929.
Many brain regions exhibit lateral differences in structure and function, and also incorporate new neurons in adulthood, thought to function in learning and in the formation of new memories. However, the contribution of new neurons to hemispheric differences in processing is unknown. The present study combines cellular, behavioral, and physiological methods to address whether 1) new neuron incorporation differs between the brain hemispheres, and 2) the degree to which hemispheric lateralization of new neurons correlates with behavioral and physiological measures of learning and memory. The songbird provides a model system for assessing the contribution of new neurons to hemispheric specialization because songbird brain areas for vocal processing are functionally lateralized and receive a continuous influx of new neurons in adulthood. In adult male zebra finches, we quantified new neurons in the caudomedial nidopallium (NCM), a forebrain area involved in discrimination and memory for the complex vocalizations of individual conspecifics. We assessed song learning and recorded neural responses to song in NCM. We found significantly more new neurons labeled in left than in right NCM; moreover, the degree of asymmetry in new neuron numbers was correlated with the quality of song learning and strength of neuronal memory for recently heard songs. In birds with experimentally impaired song quality, the hemispheric difference in new neurons was diminished. These results suggest that new neurons may contribute to an allocation of function between the hemispheres that underlies the learning and processing of complex signals.
doi:10.1371/journal.pone.0108929
PMCID: PMC4177556  PMID: 25251077
3.  To Modulate and Be Modulated: Estrogenic Influences on Auditory Processing of Communication Signals within a Socio-Neuro-Endocrine Framework 
Behavioral Neuroscience  2011;126(1):17-28.
Gonadal hormones modulate behavioral responses to sexual stimuli, and communication signals can also modulate circulating hormone levels. In several species, these combined effects appear to underlie a two-way interaction between circulating gonadal hormones and behavioral responses to socially salient stimuli. Recent work in songbirds has shown that manipulating local estradiol levels in the auditory forebrain produces physiological changes that affect discrimination of conspecific vocalizations and can affect behavior. These studies provide new evidence that estrogens can directly alter auditory processing and indirectly alter the behavioral response to a stimulus. These studies show that: 1. Local estradiol action within an auditory area is necessary for socially-relevant sounds to induce normal physiological responses in the brains of both sexes; 2. These physiological effects occur much more quickly than predicted by the classical time-frame for genomic effects; 3. Estradiol action within the auditory forebrain enables behavioral discrimination among socially-relevant sounds in males; and 4. Estradiol is produced locally in the male brain during exposure to particular social interactions. The accumulating evidence suggests a socio-neuro-endocrinology framework in which estradiol is essential to auditory processing, is increased by a socially relevant stimulus, acts rapidly to shape perception of subsequent stimuli experienced during social interactions, and modulates behavioral responses to these stimuli. Brain estrogens are likely to function similarly in both songbird sexes because aromatase and estrogen receptors are present in both male and female forebrain. Estrogenic modulation of perception in songbirds and perhaps other animals could fine-tune male advertising signals and female ability to discriminate them, facilitating mate selection by modulating behaviors. Keywords: Estrogens, Songbird, Social Context, Auditory Perception
doi:10.1037/a0026673
PMCID: PMC3272484  PMID: 22201281
4.  Noradrenergic Control of Gene Expression and Long-Term Neuronal Adaptation Evoked by Learned Vocalizations in Songbirds 
PLoS ONE  2012;7(5):e36276.
Norepinephrine (NE) is thought to play important roles in the consolidation and retrieval of long-term memories, but its role in the processing and memorization of complex acoustic signals used for vocal communication has yet to be determined. We have used a combination of gene expression analysis, electrophysiological recordings and pharmacological manipulations in zebra finches to examine the role of noradrenergic transmission in the brain’s response to birdsong, a learned vocal behavior that shares important features with human speech. We show that noradrenergic transmission is required for both the expression of activity-dependent genes and the long-term maintenance of stimulus-specific electrophysiological adaptation that are induced in central auditory neurons by stimulation with birdsong. Specifically, we show that the caudomedial nidopallium (NCM), an area directly involved in the auditory processing and memorization of birdsong, receives strong noradrenergic innervation. Song-responsive neurons in this area express α-adrenergic receptors and are in close proximity to noradrenergic terminals. We further show that local α-adrenergic antagonism interferes with song-induced gene expression, without affecting spontaneous or evoked electrophysiological activity, thus dissociating the molecular and electrophysiological responses to song. Moreover, α-adrenergic antagonism disrupts the maintenance but not the acquisition of the adapted physiological state. We suggest that the noradrenergic system regulates long-term changes in song-responsive neurons by modulating the gene expression response that is associated with the electrophysiological activation triggered by song. We also suggest that this mechanism may be an important contributor to long-term auditory memories of learned vocalizations.
doi:10.1371/journal.pone.0036276
PMCID: PMC3344865  PMID: 22574146
5.  Response Properties of the Auditory Telencephalon in Songbirds Change with Recent Experience and Season 
PLoS ONE  2008;3(8):e2854.
The caudomedial nidopallium (NCM) is a telencephalic auditory area that is selectively activated by conspecific vocalizations in zebra finches and canaries. We recently demonstrated that temporal and spectral dynamics of auditory tuning in NCM differ between these species [1]. In order to determine whether these differences reflect recent experience, we exposed separate groups of each species and sex to different housing conditions. Adult birds were housed either in an aviary with conspecifics (NORM), with heterospecifics (canary subjects in a zebra finch aviary, and vice versa: (CROSS)), or in isolation (ISO) for 9 days prior to testing. We then recorded extracellular multi-unit electrophysiological responses to simple pure tone stimuli (250–5000 Hz) in awake birds from each group and analyzed auditory tuning width using methods from our earlier studies. Relative to NORM birds, tuning was narrower in CROSS birds, and wider in ISO birds. The trend was greater in canaries, especially females. The date of recording was also included as a covariate in ANCOVAs that analyzed a larger set of the canary data, including data from birds tested outside of the breeding season, and treated housing condition and sex as independent variables. These tests show that tuning width was narrower early in the year and broader later. This effect was most pronounced in CROSS males. The degree of the short-term neural plasticity described here differs across sexes and species, and may reflect differences in NCM's anatomical and functional organization related to species differences in song characteristics, adult plasticity and/or social factors. More generally, NCM tuning is labile and may be modulated by recent experience to reflect the auditory processing required for behavioral adaptation to the current acoustic, social or seasonal context.
doi:10.1371/journal.pone.0002854
PMCID: PMC2475665  PMID: 18682724

Results 1-5 (5)