Developmental Regulation of Basal Ganglia Circuitry during the Sensitive Period for Vocal Learning in Songbirds

2004 ◽  
Vol 1016 (1) ◽  
pp. 395-415 ◽  
Author(s):  
SARAH W. BOTTJER
Keyword(s):  
Basal Ganglia ◽  
Developmental Regulation ◽  
Vocal Learning ◽  
Sensitive Period

scholarly journals Auditory experience refines cortico-basal ganglia inputs to motor cortex via remapping of single axons during vocal learning in zebra finches

2012 ◽  
Vol 107 (4) ◽  
pp. 1142-1156 ◽  
Author(s):  
Vanessa C. Miller-Sims ◽  
Sarah W. Bottjer
Keyword(s):  
Basal Ganglia ◽  
Motor Cortex ◽  
Vocal Learning ◽  
Song Learning ◽  
Sensitive Period ◽  
Cortical Region ◽  
Topographic Organization ◽  
Magnocellular Nucleus ◽  
Auditory Experience ◽  
Dependent Processes

Experience-dependent changes in neural connectivity underlie developmental learning and result in life-long changes in behavior. In songbirds axons from the cortical region LMANcore (core region of lateral magnocellular nucleus of anterior nidopallium) convey the output of a basal ganglia circuit necessary for song learning to vocal motor cortex [robust nucleus of the arcopallium (RA)]. This axonal projection undergoes remodeling during the sensitive period for learning to achieve topographic organization. To examine how auditory experience instructs the development of connectivity in this pathway, we compared the morphology of individual LMANcore→RA axon arbors in normal juvenile songbirds to those raised in white noise. The spatial extent of axon arbors decreased during the first week of vocal learning, even in the absence of normal auditory experience. During the second week of vocal learning axon arbors of normal birds showed a loss of branches and varicosities; in contrast, experience-deprived birds showed no reduction in branches or varicosities and maintained some arbors in the wrong topographic location. Thus both experience-independent and experience-dependent processes are necessary to establish topographic organization in juvenile birds, which may allow birds to modify their vocal output in a directed manner and match their vocalizations to a tutor song. Many LMANcore axons of juvenile birds, but not adults, extended branches into dorsal arcopallium (Ad), a region adjacent to RA that is part of a parallel basal ganglia pathway also necessary for vocal learning. This transient projection provides a point of integration between the two basal ganglia pathways, suggesting that these branches convey corollary discharge signals as birds are actively engaged in 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 Development of neural responsivity to vocal sounds in higher level auditory cortex of songbirds

2014 ◽  
Vol 112 (1) ◽  
pp. 81-94 ◽  
Author(s):  
Vanessa C. Miller-Sims ◽  
Sarah W. Bottjer
Keyword(s):  
Auditory Cortex ◽  
Vocal Learning ◽  
Response Strength ◽  
Neural Mechanisms ◽  
Sensitive Period ◽  
Unexpected Result ◽  
Salient Stimulus ◽  
Evoked Activity ◽  
High Level ◽  
Persistent Response

Like humans, songbirds learn vocal sounds from “tutors” during a sensitive period of development. Vocal learning in songbirds therefore provides a powerful model system for investigating neural mechanisms by which memories of learned vocal sounds are stored. This study examined whether NCM (caudo-medial nidopallium), a region of higher level auditory cortex in songbirds, serves as a locus where a neural memory of tutor sounds is acquired during early stages of vocal learning. NCM neurons respond well to complex auditory stimuli, and evoked activity in many NCM neurons habituates such that the response to a stimulus that is heard repeatedly decreases to approximately one-half its original level (stimulus-specific adaptation). The rate of neural habituation serves as an index of familiarity, being low for familiar sounds, but high for novel sounds. We found that response strength across different song stimuli was higher in NCM neurons of adult zebra finches than in juveniles, and that only adult NCM responded selectively to tutor song. The rate of habituation across both tutor song and novel conspecific songs was lower in adult than in juvenile NCM, indicating higher familiarity and a more persistent response to song stimuli in adults. In juvenile birds that have memorized tutor vocal sounds, neural habituation was higher for tutor song than for a familiar conspecific song. This unexpected result suggests that the response to tutor song in NCM at this age may be subject to top-down influences that maintain the tutor song as a salient stimulus, despite its high level of familiarity.

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

Silent Synapses in a Thalamo-Cortical Circuit Necessary for Song Learning in Zebra Finches

2005 ◽  
Vol 94 (6) ◽  
pp. 3698-3707 ◽  
Author(s):  
Sarah W. Bottjer
Keyword(s):  
Failure Rate ◽  
Behavioral Plasticity ◽  
Vocal Learning ◽  
Relative Number ◽  
Song Learning ◽  
Sensitive Period ◽  
Vocal Behavior ◽  
Adult Males ◽  
Silent Synapses

Developmental changes in synaptic properties may act to limit neural and behavioral plasticity associated with sensitive periods. This study characterized synaptic maturation in a glutamatergic thalamo-cortical pathway that is necessary for vocal learning in songbirds. Lesions of the projection from medial dorsolateral nucleus of the thalamus (DLM) to the cortical nucleus lateral magnocellular nucleus of the anterior nidopallium (LMAN) greatly disrupt song behavior in juvenile birds during early stages of vocal learning. However, such lesions lose the ability to disrupt vocal behavior in normal birds at 60–70 days of age, around the time that selective auditory tuning for each bird’s own song (BOS) emerges in LMAN neurons. This pattern has suggested that LMAN is involved in processing song-related information and evaluating the degree to which vocal motor output matches the tutor song to be learned. Analysis of reversed excitatory postsynaptic currents at DLM→LMAN synapses in in vitro slice preparations revealed a pronounced N-methyl-d-aspartate receptor (NMDAR)-mediated component in both juvenile and adult cells with no developmental decrease in the relative contribution of NMDARs to synaptic transmission. However, the synaptic failure rate at DLM→LMAN synapses in juvenile males during the sensitive period for song learning was significantly lower at depolarized potentials than at hyperpolarized potentials. In contrast, the failure rate at DLM→LMAN synapses did not differ at hyper- versus depolarized holding potentials in adult males that had completed the acquisition of a stereotyped song. This pattern indicates that juvenile cells have a higher incidence of silent (NMDAR-only) synapses, which are postsynaptically silent at hyperpolarized potentials due to the voltage-dependent gating of NMDARs. Thus the decreased involvement of the LMAN pathway in vocal behavior is mirrored by a decline in the incidence of silent synapses but not by changes in the relative number of NMDA and AMPA receptors at DLM→LMAN synapses. These findings suggest that a developmental decrease in silent synapses within LMAN may represent a neural correlate of behavioral plasticity during song learning.

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.

scholarly journals Song preferences predict the quality of vocal learning in zebra finches

2021 ◽  
Author(s):  
Carlos A. Rodriguez-Saltos ◽  
Aditya Bhise ◽  
Prasanna Karur ◽  
Ramsha Nabihah Khan ◽  
Sumin Lee ◽  
...  
Keyword(s):  
Reinforcement Schedule ◽  
Social Process ◽  
Vocal Learning ◽  
Song Learning ◽  
Sensitive Period ◽  
Social Reward ◽  
Zebra Finches ◽  
Vocal Development ◽  
Song Preferences

In songbirds, learning to sing is a highly social process that likely involves social reward. Here, we hypothesized that the degree to which a juvenile songbird learns a song depends on the degree to which it finds that song rewarding to hear during vocal development. We tested this hypothesis by measuring song preferences in young birds during song learning and then analyzing their adult songs. Song preferences were measured in an operant key-pressing assay. Juvenile male zebra finches (Taeniopygia guttata) had access to two keys, each of which was associated with a higher likelihood of playing the song of their father or that of another familiar adult ("neighbor"). To minimize the effects of exposure on learning, we implemented a reinforcement schedule that allowed us to detect preferences while balancing exposure to each song. On average, the juveniles significantly preferred the father's song early during song learning, before they were themselves singing. At around post-hatch day 60, their preference shifted to the neighbor's song. At the end of the song learning period, we recorded the juveniles' songs and compared them to the father's and the neighbor's song. All of the birds copied father's song. The accuracy with which the father's song was imitated was positively correlated with the peak strength of the preference for the father's song during the sensitive period. Our results show that preference for a social stimulus, in this case a vocalization, predicted social learning during development.

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