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Decrystallization of Adult Birdsong by Perturbation of Auditory Feedback Anthony Leonardo & Masakazu Konishi (1999)

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Decrystallization of Adult Birdsong by Perturbation of Auditory Feedback Anthony Leonardo & Masakazu Konishi (1999) 12/28/2011 The Study of Birdsong • Began in 1950’s with Thorpe introducing tools for recording and analyzing bird sounds (spectrogram) • Thorpe (1958) showed that chaffinches selectively learn the song of their own species • Also late in the 1950’s, Marler began his work distinguishing the ecological function of chaffinch calls • Konishi’s work in the 1960’s (under Marler) elucidated role of template song and auditory feedback in song development • Nordeen & Nordeen (1992): ―continued auditory input is necessary to maintain the patterns of neural organization supporting learned song in zebra finches‖ Anatomy of the song system Decrystallization of Adult Birdsong by Perturbation of Auditory Feedback Anthony Leonardo & Masakazu Konishi (1999) Presentation by Graham Baum ―Are there fundamental Authors principles that govern how Authors (cont’d) neurons solve behavioral Anthony Leonardo problems?" Masakazu (Mark) Konishi • Undergrad: Carnegie Melon, Class of 1994 (B.S. in Cognitive Science) • B.S. and M.S. at Hokkaido University, Japan • Ph. D at Cal-Tech under Mark Konishi • PhD under Peter Marler at UC Berkeley (1963) • • Finished dissertation in 2002: ―Neural dynamics Post-doc work at University of Tübingen, Germany and at the Division of Experimental Neurophysiology, Max-Planck Institute, Munich underlying complex behavior in songbird‖ (1963-1965) • Post-doc work under Markus Meister (Harvard University) • Currently runs the Konishi lab at Caltech • Currently a Group Leader at Janelia Farm (Research Campus of HHMI) Honors/Awards: Honors: - Member of National Academy of Sciences (1985) - Lindsley Prize in Behavioral Neuroscience In 2003 (for PhD thesis) - President of International Society for Neuroethology (1986-1989) - Grass Fellowship (2007) - International Prize for Biology (1990) - Capranica Foundation Prize in Neuroethology (2008) - In 2004 Ralph W. Gerard Prize in Neuroscience, Lewis S. Rosenstiel Award, Karl Spencer Lashley Award (The American Philosophical Society) 1 12/28/2011 Journal: Nature Key Points of the Study • First Issue: November, 1869 • What is the role of auditory feedback in adult zebra finch • Impact Factor: 36.101 song maintenance? • How do differences in auditory feedback perturbation affect the gradual loss of song stereotypy? (What features characterize the process of decrystallization?) • To what extent (and over what time-frame) do zebra finches with decrystallized song recover full song stereotypy? Birdsong Organization Passerine Birds • Syllable – individual sound components separated by • 4000 species 1000 ―Suboscines‖ silent intervals 3000 ―Oscines‖ • Motif – sequence of syllables • Less complex songs • Complex song (usually) • Bout – sequence of motifs production • Can develop normal generated by songs without CPG which is auditory feedback modified by (CPG-controlled) auditory • Inability to imitate feedback song Bird Song Acquisition: Ontogeny and Auditory Feedback Perturbation Protocol Crystallization “Adaptive Protocol” (Brainard and Doupe, 2002) “Syllable-Triggered • Sub-song Plastic Song Crystallization Protocol” • Crystallization 2 12/28/2011 Decrystallization of Birdsong Adaptive Protocol • Decrystallization Adaptive Protocol Group (n=3 birds) • Increase in stuttering; increase in maximum song length • Syllable addition/deletion • Spectral distortion (―wobbling‖ of harmonic structure) – indicates loss of precise control over the syrinx • *Results paralleled previous studies with deafened birds Decrystallization: Syllable-Triggered Syllable-Triggered Protocol Baseline version of Syllable A After one week of protocol Syllable-Triggered Protocol (n=2 birds) • Harmonic stacking on targeted syllable • Apparent changes after one week of feedback exposure After one month of protocol Understanding Decrystallization Through Markov Chain Brainard & Doupe’s Model (2000) Statistical parameter for variability • The next state in the chain depends only on the current state and not on the sequence of events that preceded it • What significance does this have for birdsong? Question: Why did birdsongs decrystallize differently in the different auditory feedback conditions? 3 12/28/2011 Song Recovery (―Re-crystallization‖) Conclusions Adaptive Protocol Birds • ―We revealed that the songs were stable not because they had • Complete recovery (return to baseline song) after 2-4 months of become hardwired but because they are maintained removal from feedback condition dynamically‖ – Leonardo • ―This finding is not consistent with the classical depiction of Syllable-Triggered Bird song development in which a dynamic learning period in youth ends in a static maintenance period in adulthood‖ (p. 469) • Made ―partial recovery‖ by 8 months after cessation of feedback • Feedback-based evaluation is essential for maintenance of adult song stability • Differences in decrystallization due to variable levels of disturbed feedback and vocal output modification (more on this later) • Re-crystallization: Gradual return to stereotyped baseline song after normal auditory feedback References Observation 1: Songs become stable and stereotyped in adults Observation 2: Adult songs degrade when auditory feedback is altered 1. Brainard, M.S., & Doupe, A.J. (2002) What songbirds teach us about learning. Nature, 417, 351-358. 2. Konishi, M. (2010) From central pattern generator to sensory template in the 2 possible explanations: evolution of birdsong. Brain & Language 115, 18-20 3. Nordeen K, & Nordeen E. (1992) Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches. Behav. Neural Biol., 57, 58- 66 Synapses in the motor Active evaluation of pathway become stable auditory feedback is after the sensorimotor ongoing, but song stabilizes learning period, once because auditory input song crystallizes. matches the stored target. ✕ ? Interruption of a basal ganglia- The authors forebrain circuit prevents plasticity of learned vocalizations Michael Brainard Allison Doupe Michael Brainard and Allison Doupe (2000) Assistant Professor Professor Depts of Physiology Dept of Psychiatry, UCSF and Psychiatry, UCSF BA from Harvard, 1985, Biochemistry Editor for the Journal of Neuroscience and the PhD from Stanford, 1995, Neuroscience Journal of Neurobiology The Brainard lab: The Doupe lab: “how experience, particularly during early life, “how the nervous system mediates behavior, shapes the functioning of the nervous system” especially complex behaviors that must be learned” “a combination of behavioral and neurophysiological “we are studying how the different features of song techniques to investigate the mechanisms underlying are represented [in the AFP], how the animal's vocal learning in songbirds” auditory experience and vocal learning shape its 1 RA, 3 post-docs, 3 grad students neuronal properties, and what the crucial function of this pathway might be” Petra Deane 2 RAs, 7 post-docs, 2 grad students 4 12/28/2011 The journal Key points of the study Hypothesis Active evaluation of auditory feedback is ongoing, but song stabilizes because auditory input matches the stored target. • What are the potential neural mechanisms for ongoing, active, feedback-based evaluation? • What are the candidate brain regions/pathways involved? • Is there actually evidence? Proposed neural mechanism LEARNING JUVENILE \ \ \ vs. ⌥ ⌥ ⌥ \ \ \ ⌥ ⌥ ⌥ ⌥ ⌥ ⌥ adaptive modification Proposed neural mechanism Proposed neural mechanism ADULT DEAFENED ADULT \ \ \ vs. \ \ \ \ \ \ vs. no signal \ \ \ \ \ \ \ \ \ \ \ \ \ \ \ no signal What brain regions evaluate feedback and/or transmit this stable song instructive signal? non-adaptive modification 5 12/28/2011 Candidate brain regions/pathway responsible Candidate brain regions/pathway responsible Anterior Forebrain Pathway (AFP) • AFP is necessary for juvenile vocal learning, lesion studies prevent learning • Spatially well-placed to instructively alter the motor pathway at the level of RA • Neurons in the AFP respond preferentially to tutor song and a bird’s own song Selectivity to both tutor and self song would allow the AFP to evaluate the fit between incoming auditory signals and a memorized tutor model. Testing the proposed neural mechanism Methods DEAFENED & LESIONED ADULT \ \ \ vs. no signal Two aspects of song have been shown to be controlled independently: \ \ \ \ \ \ no signal 1. Changes to syllables (nucleus RA) 2. Changes to overall song structure, syllable order (nucleus HVC) So, in this study, they tested both independently: 1. Scored how well syllables from pre-treatment repertoire were preserved (RA) 2. Assessed changes in the syllable order, deviations from A B C D E (HVC) Lesion LMAN in the AFP Prediction: Confirmed this method by cutting tracheosyringeal nerve.. stable song Syllable structure deteriorated, order of syllables sung remained stable ✓ Results Results Lesions to LMAN prevent post-deafening deterioration in both syllables and song: Lesions to LMAN prevent post-deafening deterioration in both syllables and song: different same confirms role of AFP (LMAN) 6 12/28/2011 Conclusions Changes in song when auditory feedback is disrupted are due to an active process, not through passive changes in the motor pathway. AFP plays the same role in adults as it does in juveniles— adult songs are stable only because their auditory feedback matches the template. Understanding Decrystallization Through Brainard & Doupe’s Model (2000) Question: Why did birdsongs decrystallize differently in the different auditory feedback conditions? 7 .
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