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

ABSTRACT: 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 neuromodulation by neuroestrogens concerns the acute regulation of sensory coding by the auditory cortex as demonstrated by electrophysiological 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.SIGNIFICANCE STATEMENT Neuroestrogens can acutely modulate sensory processing in a manner similar to neuromodulators. We report that acute estrogen depletion rapidly disrupts auditory processing in large areas of the male starling brain. Effects were larger in March than in December or May/June, lateralized to the left hemisphere and specific to behaviorally relevant stimuli. These findings confirm and extend previous data that identified an acute regulation of auditory neurons in zebra finches by (1) delineating the extent of the brain region affected, (2) confirming its lateralization, and (3) demonstrating that a large part of the auditory brain regions are acutely affected by estrogens. These findings provide a very powerful tool to investigate auditory responsiveness in songbirds and its fast modulation by sex steroids.

SUBMITTER: De Groof G

PROVIDER: S-EPMC6596569 | biostudies-literature | 2017 Apr

REPOSITORIES: biostudies-literature

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

De Groof Geert G Balthazart Jacques J Cornil Charlotte A CA Van der Linden Annemie A

The Journal of neuroscience : the official journal of the Society for Neuroscience 20170317 16

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 neuromodulation by neuroestrogens concerns the acute regulation of sensory coding by the auditory cortex as demonstrated by electrophysiological studies of selected neurons in zebra finches. Yet, the spatial extent of such modulation by n ...[more]

PMID: 28314822

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Project description:BackgroundLateralized processing of speech is a well studied phenomenon in humans. Both anatomical and neurophysiological studies support the view that nonhuman primates and other animal species also reveal hemispheric differences in areas involved in sound processing. In recent years, an increasing number of studies on a range of taxa have employed an orienting paradigm to investigate lateralized acoustic processing. In this paradigm, sounds are played directly from behind and the direction of turn is recorded. This assay rests on the assumption that a hemispheric asymmetry in processing is coupled to an orienting bias towards the contralateral side. To examine this largely untested assumption, speech stimuli as well as artificial sounds were presented to 224 right-handed human subjects shopping in supermarkets in Germany and in the UK. To verify the lateralized processing of the speech stimuli, we additionally assessed the brain activation in response to presentation of the different stimuli using functional magnetic resonance imaging (fMRI).ResultsIn the naturalistic behavioural experiments, there was no difference in orienting behaviour in relation to the stimulus material (speech, artificial sounds). Contrary to our predictions, subjects revealed a significant left bias, irrespective of the sound category. This left bias was slightly but not significantly stronger in German subjects. The fMRI experiments confirmed that the speech stimuli evoked a significant left lateralized activation in BA44 compared to the artificial sounds.ConclusionThese findings suggest that in adult humans, orienting biases are not necessarily coupled with lateralized processing of acoustic stimuli. Our results -- as well as the inconsistent orienting biases found in different animal species -- suggest that the orienting assay should be used with caution. Apparently, attention biases, experience, and experimental conditions may all affect head turning responses. Because of the complexity of the interaction of factors, the use of the orienting assay to determine lateralized processing of sound stimuli is discouraged.

Dataset Information

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

Publications

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

Similar Datasets

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