A novel basal ganglia pathway forms a loop linking a vocal learning circuit with its dopaminergic input

2008 ◽  
Vol 508 (5) ◽  
pp. 824-839 ◽  
Author(s):  
Samuel D. Gale ◽  
Abigail L. Person ◽  
David J. Perkel
Keyword(s):  
Basal Ganglia ◽  
Vocal Learning

scholarly journals Shared mechanisms of auditory and non-auditory vocal learning in the songbird brain

2021 ◽  
Author(s):  
James McGregor ◽  
Abigail Grassler ◽  
Paul I. Jaffe ◽  
Amanda Louise Jacob ◽  
Michael Brainard ◽  
...  
Keyword(s):  
Reinforcement Learning ◽  
Basal Ganglia ◽  
General Principle ◽  
Auditory Feedback ◽  
Sensory Feedback ◽  
Vocal Learning ◽  
Neural Systems ◽  
Auditory Information ◽  
Vocal Plasticity

Songbirds and humans share the ability to adaptively modify their vocalizations based on sensory feedback. Prior studies have focused primarily on the role that auditory feedback plays in shaping vocal output throughout life. In contrast, it is unclear whether and how non-auditory information drives vocal plasticity. Here, we first used a reinforcement learning paradigm to establish that non-auditory feedback can drive vocal learning in adult songbirds. We then assessed the role of a songbird basal ganglia-thalamocortical pathway critical to auditory vocal learning in this novel form of vocal plasticity. We found that both this circuit and its dopaminergic inputs are necessary for non-auditory vocal learning, demonstrating that this pathway is not specialized exclusively for auditory-driven vocal learning. The ability of this circuit to use both auditory and non-auditory information to guide vocal learning may reflect a general principle for the neural systems that support vocal plasticity across species.

scholarly journals miR-9 regulates basal ganglia-dependent developmental vocal learning and adult vocal performance in songbirds

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Zhimin Shi ◽  
Zoe Piccus ◽  
Xiaofang Zhang ◽  
Huidi Yang ◽  
Hannah Jarrell ◽  
...  
Keyword(s):  
Basal Ganglia ◽  
Vocal Communication ◽  
Vocal Learning ◽  
Vital Role ◽  
Language Impairments ◽  
Vocal Performance ◽  
Behavioral Deficits ◽  
Expression Of Genes ◽  
Dopamine Signaling ◽  
Area X

miR-9 is an evolutionarily conserved miRNA that is abundantly expressed in Area X, a basal ganglia nucleus required for vocal learning in songbirds. Here, we report that overexpression of miR-9 in Area X of juvenile zebra finches impairs developmental vocal learning, resulting in a song with syllable omission, reduced similarity to the tutor song, and altered acoustic features. miR-9 overexpression in juveniles also leads to more variable song performance in adulthood, and abolishes social context-dependent modulation of song variability. We further show that these behavioral deficits are accompanied by downregulation of FoxP1 and FoxP2, genes that are known to be associated with language impairments, as well as by disruption of dopamine signaling and widespread changes in the expression of genes that are important in circuit development and functions. These findings demonstrate a vital role for miR-9 in basal ganglia function and vocal communication, suggesting that dysregulation of miR-9 in humans may contribute to language impairments and related neurodevelopmental disorders.

scholarly journals Dopaminergic modulation of basal ganglia output through coupled excitation–inhibition

2017 ◽  
Vol 114 (22) ◽  
pp. 5713-5718 ◽  
Author(s):  
Agata Budzillo ◽  
Alison Duffy ◽  
Kimberly E. Miller ◽  
Adrienne L. Fairhall ◽  
David J. Perkel
Keyword(s):  
Basal Ganglia ◽  
Dynamic Change ◽  
Vocal Learning ◽  
Synaptic Connections ◽  
Biophysical Mechanism ◽  
Output Neurons ◽  
Neural Variability ◽  
Vocal Variability ◽  
Selection Of

Learning and maintenance of skilled movements require exploration of motor space and selection of appropriate actions. Vocal learning and social context-dependent plasticity in songbirds depend on a basal ganglia circuit, which actively generates vocal variability. Dopamine in the basal ganglia reduces trial-to-trial neural variability when the bird engages in courtship song. Here, we present evidence for a unique, tonically active, excitatory interneuron in the songbird basal ganglia that makes strong synaptic connections onto output pallidal neurons, often linked in time with inhibitory events. Dopamine receptor activity modulates the coupling of these excitatory and inhibitory events in vitro, which results in a dynamic change in the synchrony of a modeled population of basal ganglia output neurons receiving excitatory and inhibitory inputs. The excitatory interneuron thus serves as one biophysical mechanism for the introduction or modulation of neural variability in this circuit.

Properties of Dopamine Release and Uptake in the Songbird Basal Ganglia

2005 ◽  
Vol 93 (4) ◽  
pp. 1871-1879 ◽  
Author(s):  
Samuel D. Gale ◽  
David J. Perkel
Keyword(s):  
Basal Ganglia ◽  
Brain Slices ◽  
Vocal Learning ◽  
Monoamine Transporters ◽  
Anterior Forebrain ◽  
Song Production ◽  
Electrode Selectivity ◽  
Area X ◽  
Da Release

Vocal learning in songbirds requires a basal ganglia circuit termed the anterior forebrain pathway (AFP). The AFP is not required for song production, and its role in song learning is not well understood. Like the mammalian striatum, the striatal component of the AFP, Area X, receives dense dopaminergic innervation from the midbrain. Since dopamine (DA) clearly plays a crucial role in basal ganglia–mediated motor control and learning in mammals, it seems likely that DA signaling contributes importantly to the functions of Area X as well. In this study, we used voltammetric methods to detect subsecond changes in extracellular DA concentration to gain better understanding of the properties and regulation of DA release and uptake in Area X. We electrically stimulated Ca2+- and action potential–dependent release of an electroactive substance in Area X brain slices and identified the substance as DA by the voltammetric waveform, electrode selectivity, and neurochemical and pharmacological evidence. As in the mammalian striatum, DA release in Area X is depressed by autoinhibition, and the lifetime of extracellular DA is strongly constrained by monoamine transporters. These results add to the known physiological similarities of the mammalian and songbird striatum and support further use of voltammetry in songbirds to investigate the role of basal ganglia DA in motor learning.

scholarly journals Parallel pathways for vocal learning in basal ganglia of songbirds

2009 ◽  
Vol 13 (2) ◽  
pp. 153-155 ◽  
Author(s):  
Sarah W Bottjer ◽  
Brie Altenau
Keyword(s):  
Basal Ganglia ◽  
Vocal Learning ◽  
Parallel Pathways

scholarly journals Vocal learning, prosody, and basal ganglia: Don't underestimate their complexity

2014 ◽  
Vol 37 (6) ◽  
pp. 570-571 ◽  
Author(s):  
Andrea Ravignani ◽  
Mauricio Martins ◽  
W. Tecumseh Fitch
Keyword(s):  
Basal Ganglia ◽  
Emotional Expression ◽  
Vocal Learning ◽  
Nonhuman Animal ◽  
Linguistic Information ◽  
Target Article ◽  
Human Adults

AbstractAckermann et al.'s arguments in the target article need sharpening and rethinking at both mechanistic and evolutionary levels. First, the authors' evolutionary arguments are inconsistent with recent evidence concerning nonhuman animal rhythmic abilities. Second, prosodic intonation conveys much more complex linguistic information than mere emotional expression. Finally, human adults' basal ganglia have a considerably wider role in speech modulation than Ackermann et al. surmise.

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