Representation of Early Sensory Experience in the Adult Auditory Midbrain: Implications for Vocal Learning

PLOS ONE, Dec 2019

Vocal learning in songbirds and humans occurs by imitation of adult vocalizations. In both groups, vocal learning includes a perceptual phase during which juveniles birds and infants memorize adult vocalizations. Despite intensive research, the neural mechanisms supporting this auditory memory are still poorly understood. The present functional MRI study demonstrates that in adult zebra finches, the right auditory midbrain nucleus responds selectively to the copied vocalizations. The selective signal is distinct from selectivity for the bird's own song and does not simply reflect acoustic differences between the stimuli. Furthermore, the amplitude of the selective signal is positively correlated with the strength of vocal learning, measured by the amount of song that experimental birds copied from the adult model. These results indicate that early sensory experience can generate a long-lasting memory trace in the auditory midbrain of songbirds that may support song learning.

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Representation of Early Sensory Experience in the Adult Auditory Midbrain: Implications for Vocal Learning

Poirier C (2013) Representation of Early Sensory Experience in the Adult Auditory Midbrain: Implications for Vocal Learning. PLoS ONE 8(4): e61764. doi:10.1371/journal.pone.0061764 Representation of Early Sensory Experience in the Adult Auditory Midbrain: Implications for Vocal Learning Anne van der Kant 0 Se bastien Dere gnaucourt 0 Manfred Gahr 0 Annemie Van der Linden 0 Colline Poirier 0 Todd W. Troyer, University of Texas at San Antonio, United States of America 0 1 Bio-Imaging Lab, University of Antwerp, Antwerp, Belgium, 2 Department of Behavioural Neurobiology, Max Planck Institute for Ornithology , Seewiesen , Germany Vocal learning in songbirds and humans occurs by imitation of adult vocalizations. In both groups, vocal learning includes a perceptual phase during which juveniles birds and infants memorize adult vocalizations. Despite intensive research, the neural mechanisms supporting this auditory memory are still poorly understood. The present functional MRI study demonstrates that in adult zebra finches, the right auditory midbrain nucleus responds selectively to the copied vocalizations. The selective signal is distinct from selectivity for the bird's own song and does not simply reflect acoustic differences between the stimuli. Furthermore, the amplitude of the selective signal is positively correlated with the strength of vocal learning, measured by the amount of song that experimental birds copied from the adult model. These results indicate that early sensory experience can generate a long-lasting memory trace in the auditory midbrain of songbirds that may support song learning. - Funding: This research was supported by grants from the Research Foundation - Flanders (FWO, www.fwo.be, project Nr G.0420.02), Concerted Research Actions (GOA funding) from the University of Antwerp (www. ua.ac.be), and partly sponsored by EC FP6 project DiMI, LSHB-CT-2005-512146, EC FP6 project EMIL LSHC-CT-2004-503569 and the Max Planck Society (www.mpg.de). C.P. is a Postdoctoral Fellow of the Research Foundation - Flanders (FWO). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Songbirds share with humans the ability to learn their vocalizations [13]. Like human babies need to be exposed to adult speech to develop a normal vocal repertoire, juvenile songbirds need to be exposed to adult conspecific vocalizations to develop a normal song (sensory phase). Then, during a subsequent sensori-motor phase, they use auditory feedback to progressively match their own developing vocalizations to the memorized adult model (called tutor song) [4]. Learning by imitation requires first to compare the motor performance with the object of imitation and then to correct for potential errors. It has long been hypothesized that the anterior forebrain pathway of songbirds, a circuit driving vocal variability in juveniles and adults [57], participates in both vocal error detection and error correction [8]. While the role of the anterior forebrain pathway in generating a corrective premotor bias has been recently confirmed [9], a growing number of studies point to the ascending auditory pathway as the main neural substrate of tutor song memory [10 15] and feedback-dependent error detection [16,17]. However, if the auditory system supports the comparison between the birds own song and a memory trace of the tutor song in order to detect vocal errors, one would expect to find birds own song and tutor song selective signals in some of the auditory nuclei [18]. While significant birds own song selective responses have been recently found in the auditory midbrain [19] and the auditory thalamus [17], evidence for tutor song selective responses in the ascending auditory pathway is still missing. The goal of this study was thus to look for tutor song selectivity in the auditory system, using blood oxygen level-dependent (BOLD) functional MRI (fMRI), a technique commonly used on humans and recently adapted to songbirds [20]. Such selectivity was found in the right auditory midbrain. Materials and Methods Ethical Statement All experimental procedures were performed in accordance with the Belgian laws on the protection and welfare of animals and were approved by the ethical committee of the University of Antwerp, Belgium (EC nr 2009/21). All fMRI recordings were performed under isoflurane anesthesia and all efforts were made to minimize suffering and anxiety. Subjects Twenty adult male (mean age 24 months, range 1041 months) zebra finches (Taeniopygia guttata) recruited from the breeding colony of the Max Planck Institute for Ornithology (Seewiesen, Germany) were used in this experiment. Birds were raised by their parents from 0 to 7 days post hatching (DPH), by their mother from 8 to 34 DPH and were kept alone from 35 to 42 DPH. The birds were then housed singly with one a (...truncated)


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Anne van der Kant, Sébastien Derégnaucourt, Manfred Gahr, Annemie Van der Linden, Colline Poirier. Representation of Early Sensory Experience in the Adult Auditory Midbrain: Implications for Vocal Learning, PLOS ONE, 2013, 4, DOI: 10.1371/journal.pone.0061764