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Anatomical and Functional Organization of Inhibitory Circuits in the Songbird Auditory Forebrain
Jin Kwon Jeong, Liisa A. Tremere, Michael J. Ryave, Victor C. Vuong and Raphael Pinaud
Journal of Experimental Neuroscience , 2012,
Abstract: Recent studies on the anatomical and functional organization of GABAergic networks in central auditory circuits of the zebra finch have highlighted the strong impact of inhibitory mechanisms on both the central encoding and processing of acoustic information in a vocal learning species. Most of this work has focused on the caudomedial nidopallium (NCM), a forebrain area postulated to be the songbird analogue of the mammalian auditory association cortex. NCM houses neurons with selective responses to conspecific songs and is a site thought to house auditory memories required for vocal learning and, likely, individual identification. Here we review our recent work on the anatomical distribution of GABAergic cells in NCM, their engagement in response to song and the roles for inhibitory transmission in the physiology of NCM at rest and during the processing of natural communication signals. GABAergic cells are highly abundant in the songbird auditory forebrain and account for nearly half of the overall neuronal population in NCM with a large fraction of these neurons activated by song in freely-behaving animals. GABAergic synapses provide considerable local, tonic inhibition to NCM neurons at rest and, during sound processing, may contain the spread of excitation away from un-activated or quiescent parts of the network. Finally, we review our work showing that GABAA-mediated inhibition directly regulates the temporal organization of song-driven responses in awake songbirds, and appears to enhance the reliability of auditory encoding in NCM.
Altered Auditory BOLD Response to Conspecific Birdsong in Zebra Finches with Stuttered Syllables  [PDF]
Henning U. Voss,Delanthi Salgado-Commissariat,Santosh A. Helekar
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0014415
Abstract: How well a songbird learns a song appears to depend on the formation of a robust auditory template of its tutor's song. Using functional magnetic resonance neuroimaging we examine auditory responses in two groups of zebra finches that differ in the type of song they sing after being tutored by birds producing stuttering-like syllable repetitions in their songs. We find that birds that learn to produce the stuttered syntax show attenuated blood oxygenation level-dependent (BOLD) responses to tutor's song, and more pronounced responses to conspecific song primarily in the auditory area field L of the avian forebrain, when compared to birds that produce normal song. These findings are consistent with the presence of a sensory song template critical for song learning in auditory areas of the zebra finch forebrain. In addition, they suggest a relationship between an altered response related to familiarity and/or saliency of song stimuli and the production of variant songs with stuttered syllables.
Rapid Effects of Hearing Song on Catecholaminergic Activity in the Songbird Auditory Pathway  [PDF]
Lisa L. Matragrano, Micha?l Beaulieu, Jessica O. Phillip, Ali I. Rae, Sara E. Sanford, Keith W. Sockman, Donna L. Maney
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0039388
Abstract: Catecholaminergic (CA) neurons innervate sensory areas and affect the processing of sensory signals. For example, in birds, CA fibers innervate the auditory pathway at each level, including the midbrain, thalamus, and forebrain. We have shown previously that in female European starlings, CA activity in the auditory forebrain can be enhanced by exposure to attractive male song for one week. It is not known, however, whether hearing song can initiate that activity more rapidly. Here, we exposed estrogen-primed, female white-throated sparrows to conspecific male song and looked for evidence of rapid synthesis of catecholamines in auditory areas. In one hemisphere of the brain, we used immunohistochemistry to detect the phosphorylation of tyrosine hydroxylase (TH), a rate-limiting enzyme in the CA synthetic pathway. We found that immunoreactivity for TH phosphorylated at serine 40 increased dramatically in the auditory forebrain, but not the auditory thalamus and midbrain, after 15 min of song exposure. In the other hemisphere, we used high pressure liquid chromatography to measure catecholamines and their metabolites. We found that two dopamine metabolites, dihydroxyphenylacetic acid and homovanillic acid, increased in the auditory forebrain but not the auditory midbrain after 30 min of exposure to conspecific song. Our results are consistent with the hypothesis that exposure to a behaviorally relevant auditory stimulus rapidly induces CA activity, which may play a role in auditory responses.
Progress in Structure and Function of X Area in the Songbird''''s Forebrain

WANG Xiao-dong,XIAO Peng,LI Dong-feng,

动物学研究 , 2005,
Abstract: Like human speech, singing of songbirds is sensorimotor learning by tutor and auditory feedback. The development and crystallization of singing is depended on the integrity of the song system composed of vocal pathway and anterior forebrain pathway. X area in forebrain pathway plays an important role during learning and memory of singing. In this paper, we reviewed studies on the organization and the function in singing development and crystallization, the synaptic plasticity of X area. We also compared learning and memory function of X area to that of mammalian basal ganglia.
Song exposure regulates known and novel microRNAs in the zebra finch auditory forebrain
Preethi H Gunaratne, Ya-Chi Lin, Ashley L Benham, Jenny Drnevich, Cristian Coarfa, Jayantha B Tennakoon, Chad J Creighton, Jong H Kim, Aleksandar Milosavljevic, Michael Watson, Sam Griffiths-Jones, David F Clayton
BMC Genomics , 2011, DOI: 10.1186/1471-2164-12-277
Abstract: In the auditory forebrain, we identified 121 known miRNAs conserved in other vertebrates. We also identified 34 novel miRNAs that do not align to human or chicken genomes. Five conserved miRNAs showed significant and consistent changes in copy number after song exposure across three biological replications of the song-silence comparison, with two increasing (tgu-miR-25, tgu-miR-192) and three decreasing (tgu-miR-92, tgu-miR-124, tgu-miR-129-5p). We also detected a locus on the Z sex chromosome that produces three different novel miRNAs, with supporting evidence from Northern blot and TaqMan qPCR assays for differential expression in males and females and in response to song playbacks. One of these, tgu-miR-2954-3p, is predicted (by TargetScan) to regulate eight song-responsive mRNAs that all have functions in cellular proliferation and neuronal differentiation.The experience of hearing another bird singing alters the profile of miRNAs in the auditory forebrain of zebra finches. The response involves both known conserved miRNAs and novel miRNAs described so far only in the zebra finch, including a novel sex-linked, song-responsive miRNA. These results indicate that miRNAs are likely to contribute to the unique behavioural biology of learned song communication in songbirds.Songbirds are important models for exploring the neural and genomic mechanisms underlying vocal communication, social experience and learning (reviewed in [1]). Songbirds communicate using both innate calls and learned vocalizations (songs), and unique specializations of the brain evolved to support this behavior (reviewed in [2]). In the zebra finch, only the male produces songs, although both sexes process and discriminate specific songs [3-6]. The genome is actively engaged by song communication, as first shown in an early demonstration of how gene responses in the brain discriminate among different song stimuli [7]. The genomic response is not a simple correlate of neural activity and it can var
Own Song Selectivity in the Songbird Auditory Pathway: Suppression by Norepinephrine  [PDF]
Colline Poirier,Tiny Boumans,Michiel Vellema,Geert De Groof,Thierry D. Charlier,Marleen Verhoye,Annemie Van der Linden,Jacques Balthazart
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0020131
Abstract: 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.
Linking Social and Vocal Brains: Could Social Segregation Prevent a Proper Development of a Central Auditory Area in a Female Songbird?  [PDF]
Hugo Cousillas, Isabelle George, Laurence Henry, Jean-Pierre Richard, Martine Hausberger
PLOS ONE , 2008, DOI: 10.1371/journal.pone.0002194
Abstract: Direct social contact and social interaction affect speech development in human infants and are required in order to maintain perceptual abilities; however the processes involved are still poorly known. In the present study, we tested the hypothesis that social segregation during development would prevent the proper development of a central auditory area, using a “classical” animal model of vocal development, a songbird. Based on our knowledge of European starling, we raised young female starlings with peers and only adult male tutors. This ensured that female would show neither social bond with nor vocal copying from males. Electrophysiological recordings performed when these females were adult revealed perceptual abnormalities: they presented a larger auditory area, a lower proportion of specialized neurons and a larger proportion of generalist sites than wild-caught females, whereas these characteristics were similar to those observed in socially deprived (physically separated) females. These results confirmed and added to earlier results for males, suggesting that the degree of perceptual deficiency reflects the degree of social separation. To our knowledge, this report constitutes the first evidence that social segregation can, as much as physical separation, alter the development of a central auditory area.
Efficacy of the LiSN & Learn Auditory Training Software: randomized blinded controlled study  [cached]
Sharon Cameron,Helen Glyde,Harvey Dillon
Audiology Research , 2012, DOI: 10.4081/68
Abstract: Background: Children with a spatial processing disorder (SPD) require a more favorable signal-to-noise ratio in the classroom because they have difficulty perceiving sound source location cues. Previous research has shown that a novel training program - LiSN & Learn - employing spatialized sound, overcomes this deficit. Here we investigate whether improvements in spatial processing ability are specific to the LiSN & Learn training program. Materials and methods: Participants were ten children (aged between 6;0 [years;months] and 9;9) with normal peripheral hearing who were diagnosed as having SPD using the Listening in Spatialized Noise – Sentences Test (LISN-S). In a blinded controlled study, the participants were randomly allocated to train with either the LiSN & Learn or another auditory training program – Earobics - for approximately 15 minutes per day for twelve weeks. Results: There was a significant improvement post-training on the conditions of the LiSN-S that evaluate spatial processing ability for the LiSN & Learn group (p=0.03 to 0.0008, η2=0.75 to 0.95, n=5), but not for the Earobics group (p=0.5 to 0.7, η2=0.1 to 0.04, n=5). Results from questionnaires completed by the participants and their parents and teachers revealed improvements in real-world listening performance post-training were greater in the LiSN & Learn group than the Earobics group. Conclusions: LiSN & Learn training improved binaural processing ability in children with SPD, enhancing their ability to understand speech in noise. Exposure to non-spatialized auditory training does not produce similar outcomes, emphasizing the importance of deficit-specific remediation.
Functional MRI of Auditory Responses in the Zebra Finch Forebrain Reveals a Hierarchical Organisation Based on Signal Strength but Not Selectivity  [PDF]
Tiny Boumans, Sharon M. H. Gobes, Colline Poirier, Frederic E. Theunissen, Liesbeth Vandersmissen, Wouter Pintjens, Marleen Verhoye, Johan J. Bolhuis, Annemie Van der Linden
PLOS ONE , 2008, DOI: 10.1371/journal.pone.0003184
Abstract: Background Male songbirds learn their songs from an adult tutor when they are young. A network of brain nuclei known as the ‘song system’ is the likely neural substrate for sensorimotor learning and production of song, but the neural networks involved in processing the auditory feedback signals necessary for song learning and maintenance remain unknown. Determining which regions show preferential responsiveness to the bird's own song (BOS) is of great importance because neurons sensitive to self-generated vocalisations could mediate this auditory feedback process. Neurons in the song nuclei and in a secondary auditory area, the caudal medial mesopallium (CMM), show selective responses to the BOS. The aim of the present study is to investigate the emergence of BOS selectivity within the network of primary auditory sub-regions in the avian pallium. Methods and Findings Using blood oxygen level-dependent (BOLD) fMRI, we investigated neural responsiveness to natural and manipulated self-generated vocalisations and compared the selectivity for BOS and conspecific song in different sub-regions of the thalamo-recipient area Field L. Zebra finch males were exposed to conspecific song, BOS and to synthetic variations on BOS that differed in spectro-temporal and/or modulation phase structure. We found significant differences in the strength of BOLD responses between regions L2a, L2b and CMM, but no inter-stimuli differences within regions. In particular, we have shown that the overall signal strength to song and synthetic variations thereof was different within two sub-regions of Field L2: zone L2a was significantly more activated compared to the adjacent sub-region L2b. Conclusions Based on our results we suggest that unlike nuclei in the song system, sub-regions in the primary auditory pallium do not show selectivity for the BOS, but appear to show different levels of activity with exposure to any sound according to their place in the auditory processing stream.
Estradiol differentially affects auditory recognition and learning according to photoperiodic state in the adult male songbird, European starling (Sturnus vulgaris)  [PDF]
Rebecca M. Calisi,Daniel P. Knudsen,Jesse S. Krause,John C. Wingfield,Timothy Q. Gentner
PeerJ , 2015, DOI: 10.7717/peerj.150
Abstract: Changes in hormones can affect many types of learning in vertebrates. Adults experience fluctuations in a multitude of hormones over a temporal scale, from local, rapid action to more long-term, seasonal changes. Endocrine changes during development can affect behavioral outcomes in adulthood, but how learning is affected in adults by hormone fluctuations experienced during adulthood is less understood. Previous reports have implicated the sex steroid hormone estradiol (E2) in both male and female vertebrate cognitive functioning. Here, we examined the effects of E2 on auditory recognition and learning in male European starlings (Sturnus vulgaris). European starlings are photoperiodic, seasonally breeding songbirds that undergo different periods of reproductive activity according to annual changes in day length. We simulated these reproductive periods, specifically 1. photosensitivity, 2. photostimulation, and 3. photorefractoriness in captive birds by altering day length. During each period, we manipulated circulating E2 and examined multiple measures of learning. To manipulate circulating E2, we used subcutaneous implants containing either 17-β E2 and/or fadrozole (FAD), a highly specific aromatase inhibitor that suppresses E2 production in the body and the brain, and measured the latency for birds to learn and respond to short, male conspecific song segments (motifs). We report that photostimulated birds given E2 had higher response rates and responded with better accuracy than those given saline controls or FAD. Conversely, photosensitive, animals treated with E2 responded with less accuracy than those given FAD. These results demonstrate how circulating E2 and photoperiod can interact to shape auditory recognition and learning in adults, driving it in opposite directions in different states.
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