Literature DB >> 24075977

The basal ganglia is necessary for learning spectral, but not temporal, features of birdsong.

Timothy M Otchy1,2, Cengiz Pehlevan1,3, Farhan Ali4,1, Antoniu L Fantana4,1, Yoram Burak1,3, Bence P Ölveczky4,1.   

Abstract

Executing a motor skill requires the brain to control which muscles to activate at what times. How these aspects of control-motor implementation and timing-are acquired, and whether the learning processes underlying them differ, is not well understood. To address this, we used a reinforcement learning paradigm to independently manipulate both spectral and temporal features of birdsong, a complex learned motor sequence, while recording and perturbing activity in underlying circuits. Our results uncovered a striking dissociation in how neural circuits underlie learning in the two domains. The basal ganglia was required for modifying spectral, but not temporal, structure. This functional dissociation extended to the descending motor pathway, where recordings from a premotor cortex analog nucleus reflected changes to temporal, but not spectral, structure. Our results reveal a strategy in which the nervous system employs different and largely independent circuits to learn distinct aspects of a motor skill.
Copyright © 2013 Elsevier Inc. All rights reserved.

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Year:  2013        PMID: 24075977      PMCID: PMC3929499          DOI: 10.1016/j.neuron.2013.07.049

Source DB:  PubMed          Journal:  Neuron        ISSN: 0896-6273            Impact factor:   17.173


  65 in total

1.  Performance variability enables adaptive plasticity of 'crystallized' adult birdsong.

Authors:  Evren C Tumer; Michael S Brainard
Journal:  Nature       Date:  2007-12-20       Impact factor: 49.962

2.  Model of birdsong learning based on gradient estimation by dynamic perturbation of neural conductances.

Authors:  Ila R Fiete; Michale S Fee; H Sebastian Seung
Journal:  J Neurophysiol       Date:  2007-07-25       Impact factor: 2.714

3.  Neurons in a forebrain nucleus required for vocal plasticity rapidly switch between precise firing and variable bursting depending on social context.

Authors:  Mimi H Kao; Brian D Wright; Allison J Doupe
Journal:  J Neurosci       Date:  2008-12-03       Impact factor: 6.167

Review 4.  Contributions of the basal ganglia and functionally related brain structures to motor learning.

Authors:  Julien Doyon; Pierre Bellec; Rhonda Amsel; Virginia Penhune; Oury Monchi; Julie Carrier; Stéphane Lehéricy; Habib Benali
Journal:  Behav Brain Res       Date:  2008-11-17       Impact factor: 3.332

5.  Organization of the songbird basal ganglia, including area X.

Authors:  Abigail L Person; Samuel D Gale; Michael A Farries; David J Perkel
Journal:  J Comp Neurol       Date:  2008-06-10       Impact factor: 3.215

6.  Telencephalic neurons monosynaptically link brainstem and forebrain premotor networks necessary for song.

Authors:  Todd F Roberts; Marguerita E Klein; M Fabiana Kubke; J Martin Wild; Richard Mooney
Journal:  J Neurosci       Date:  2008-03-26       Impact factor: 6.167

7.  Using temperature to analyse temporal dynamics in the songbird motor pathway.

Authors:  Michael A Long; Michale S Fee
Journal:  Nature       Date:  2008-11-13       Impact factor: 49.962

8.  Central contributions to acoustic variation in birdsong.

Authors:  Samuel J Sober; Melville J Wohlgemuth; Michael S Brainard
Journal:  J Neurosci       Date:  2008-10-08       Impact factor: 6.167

9.  Activity propagation in an avian basal ganglia-thalamocortical circuit essential for vocal learning.

Authors:  Satoshi Kojima; Allison J Doupe
Journal:  J Neurosci       Date:  2009-04-15       Impact factor: 6.167

10.  Adult birdsong is actively maintained by error correction.

Authors:  Samuel J Sober; Michael S Brainard
Journal:  Nat Neurosci       Date:  2009-06-14       Impact factor: 24.884

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  58 in total

1.  Predicting plasticity: acute context-dependent changes to vocal performance predict long-term age-dependent changes.

Authors:  Logan S James; Jon T Sakata
Journal:  J Neurophysiol       Date:  2015-08-26       Impact factor: 2.714

2.  Acute off-target effects of neural circuit manipulations.

Authors:  Timothy M Otchy; Steffen B E Wolff; Juliana Y Rhee; Cengiz Pehlevan; Risa Kawai; Alexandre Kempf; Sharon M H Gobes; Bence P Ölveczky
Journal:  Nature       Date:  2015-12-09       Impact factor: 49.962

Review 3.  Two tales of how expectation of reward modulates behavior.

Authors:  Long Ding; David J Perkel
Journal:  Curr Opin Neurobiol       Date:  2014-07-23       Impact factor: 6.627

4.  Motor origin of precise synaptic inputs onto forebrain neurons driving a skilled behavior.

Authors:  Daniela Vallentin; Michael A Long
Journal:  J Neurosci       Date:  2015-01-07       Impact factor: 6.167

5.  Variation in sequence dynamics improves maintenance of stereotyped behavior in an example from bird song.

Authors:  Alison Duffy; Elliott Abe; David J Perkel; Adrienne L Fairhall
Journal:  Proc Natl Acad Sci U S A       Date:  2019-04-23       Impact factor: 11.205

Review 6.  Advantages of comparative studies in songbirds to understand the neural basis of sensorimotor integration.

Authors:  Karagh Murphy; Logan S James; Jon T Sakata; Jonathan F Prather
Journal:  J Neurophysiol       Date:  2017-03-22       Impact factor: 2.714

7.  A Basal Ganglia Circuit Sufficient to Guide Birdsong Learning.

Authors:  Lei Xiao; Gaurav Chattree; Francisco Garcia Oscos; Mou Cao; Matthew J Wanat; Todd F Roberts
Journal:  Neuron       Date:  2018-03-15       Impact factor: 17.173

8.  A neural circuit mechanism for regulating vocal variability during song learning in zebra finches.

Authors:  Jonathan Garst-Orozco; Baktash Babadi; Bence P Ölveczky
Journal:  Elife       Date:  2014-12-15       Impact factor: 8.140

9.  Focal expression of mutant huntingtin in the songbird basal ganglia disrupts cortico-basal ganglia networks and vocal sequences.

Authors:  Masashi Tanaka; Jonnathan Singh Alvarado; Malavika Murugan; Richard Mooney
Journal:  Proc Natl Acad Sci U S A       Date:  2016-03-07       Impact factor: 11.205

10.  Dopamine neurons encode performance error in singing birds.

Authors:  Vikram Gadagkar; Pavel A Puzerey; Ruidong Chen; Eliza Baird-Daniel; Alexander R Farhang; Jesse H Goldberg
Journal:  Science       Date:  2016-12-08       Impact factor: 47.728

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