scholarly journals Corticobasal ganglia projecting neurons are required for juvenile vocal learning but not for adult vocal plasticity in songbirds

2019 ◽  
Vol 116 (45) ◽  
pp. 22833-22843 ◽  
Author(s):  
Miguel Sánchez-Valpuesta ◽  
Yumeno Suzuki ◽  
Yukino Shibata ◽  
Noriyuki Toji ◽  
Yu Ji ◽  
...  
Keyword(s):  
Basal Ganglia ◽  
Vocal Learning ◽  
Skill Learning ◽  
Projection Neurons ◽  
Neural Function ◽  
Vocal Plasticity ◽  
Song Structure ◽  
Acoustic Fluctuations ◽  
Temporal Aspects ◽  
Area X

Birdsong, like human speech, consists of a sequence of temporally precise movements acquired through vocal learning. The learning of such sequential vocalizations depends on the neural function of the motor cortex and basal ganglia. However, it is unknown how the connections between cortical and basal ganglia components contribute to vocal motor skill learning, as mammalian motor cortices serve multiple types of motor action and most experimentally tractable animals do not exhibit vocal learning. Here, we leveraged the zebra finch, a songbird, as an animal model to explore the function of the connectivity between cortex-like (HVC) and basal ganglia (area X), connected by HVC(X) projection neurons with temporally precise firing during singing. By specifically ablating HVC(X) neurons, juvenile zebra finches failed to copy tutored syllable acoustics and developed temporally unstable songs with less sequence consistency. In contrast, HVC(X)-ablated adults did not alter their learned song structure, but generated acoustic fluctuations and responded to auditory feedback disruption by the introduction of song deterioration, as did normal adults. These results indicate that the corticobasal ganglia input is important for learning the acoustic and temporal aspects of song structure, but not for generating vocal fluctuations that contribute to the maintenance of an already learned vocal pattern.

Sleep-Related Neural Activity in a Premotor and a Basal-Ganglia Pathway of the Songbird

2006 ◽  
Vol 96 (2) ◽  
pp. 794-812 ◽  
Author(s):  
Richard H. R. Hahnloser ◽  
Alexay A. Kozhevnikov ◽  
Michale S. Fee
Keyword(s):  
Basal Ganglia ◽  
Vocal Learning ◽  
Spike Trains ◽  
Projection Neurons ◽  
Time Lags ◽  
Reversible Inactivation ◽  
Magnocellular Nucleus ◽  
Area X ◽  
Temporal Sequences ◽  
Spike Patterns

During singing, neurons in premotor nucleus RA (robust nucleus of the arcopallium) of the zebra finch produce complex temporal sequences of bursts that are recapitulated during sleep. RA receives input from nucleus HVC via the premotor pathway, and also from the lateral magnocellular nucleus of the anterior nidopallium (LMAN), part of a basal ganglia-related circuit essential for vocal learning. We explore the propagation of sleep-related spike patterns in these two pathways and their influences on RA activity. We promote sleep in head-fixed birds by injections of melatonin and make single-neuron recordings from the three major classes of neurons in HVC: RA-projecting neurons, Area X-projecting neurons, and interneurons. We also record LMAN neurons that project to RA. In paired recordings, spike trains from identified HVC neuron types are strongly coherent with spike trains in RA neurons, whereas LMAN projection neurons on average exhibit only a weak coherency with neurons in HVC and RA. We further examine the relative roles of HVC and LMAN in generating RA burst sequences with reversible inactivation. Lidocaine inactivation of HVC completely abolishes bursting in RA, whereas inactivation of LMAN has no effect on burst rates in RA. In combination, our data suggest that in adult birds, RA burst sequences in sleep are driven via the premotor pathway from HVC. We present a simple generative model of spike trains in HVC, RA, and LMAN neurons that is able to qualitatively reproduce observed coherency functions. We propose that commonly observed coherency peaks at positive and negative time lags are caused by sequentially correlated HVC activity.

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.

Phasic basal ganglia activity associated with high-gamma oscillation during sleep in a songbird

2012 ◽  
Vol 107 (1) ◽  
pp. 424-432 ◽  
Author(s):  
Shin Yanagihara ◽  
Neal A. Hessler
Keyword(s):  
Basal Ganglia ◽  
Phase Locking ◽  
Critical Role ◽  
Field Potential ◽  
Vocal Plasticity ◽  
Song System ◽  
Gamma Frequency ◽  
High Gamma ◽  
Area X

The basal ganglia is thought to be critical for motor control and learning in mammals. In specific basal ganglia regions, gamma frequency oscillations occur during various behavioral states, including sleeping periods. Given the critical role of sleep in regulating vocal plasticity of songbirds, we examined the presence of such oscillations in the basal ganglia. In the song system nucleus Area X, epochs of high-gamma frequency (80–160 Hz) oscillation of local field potential during sleep were associated with phasic increases of neural activity. While birds were awake, activity of the same neurons increased specifically when birds were singing. Furthermore, during sleep there was a clear tendency for phase locking of spikes to these oscillations. Such patterned activity in the sleeping songbird basal ganglia could play a role in off-line processing of song system motor networks.

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 A Basal Ganglia Circuit Sufficient To Guide Birdsong Learning

2017 ◽  
Author(s):  
Lei Xiao ◽  
Gaurav Chattree ◽  
Francisco Garcia Oscos ◽  
Mou Cao ◽  
Matthew J. Wanat ◽  
...  
Keyword(s):  
Performance Evaluation ◽  
Basal Ganglia ◽  
Negative Reinforcement ◽  
Vocal Learning ◽  
Optical Excitation ◽  
Performance Outcomes ◽  
Axon Terminals ◽  
Area X ◽  
Candidate Performance ◽  
The Brain

SUMMARYLearning complex vocal behaviors, like speech and birdsong, is thought to rely on continued performance evaluation. Whether candidate performance evaluation circuits in the brain are sufficient to guide vocal learning is not known. Here, we test the sufficiency of VTA projections to the vocal basal ganglia (Area X) in singing zebra finches, a songbird species that learns to produce a complex and stereotyped multi-syllabic courtship song during development. We optogenetically manipulate VTA axon terminals in singing birds contingent on how the pitch of individual song syllables are naturally performed. We find that optical excitation and inhibition of VTA terminals have opponent effects on future performances of targeted song syllables and are each sufficient to reliably guide learned changes in song, consistent with positive and negative reinforcement of performance outcomes. These findings define a central role for reinforcement mechanisms in learning vocalizations and provide the first demonstration of minimal circuit elements for learning vocal behaviors.

scholarly journals Vocal babbling in songbirds requires the basal ganglia-recipient motor thalamus but not the basal ganglia

2011 ◽  
Vol 105 (6) ◽  
pp. 2729-2739 ◽  
Author(s):  
Jesse H. Goldberg ◽  
Michale S. Fee
Keyword(s):  
Basal Ganglia ◽  
Thalamic Nucleus ◽  
Vocal Learning ◽  
Trial And Error ◽  
Bilateral Lesions ◽  
Motor Thalamus ◽  
Area X

Young songbirds produce vocal “babbling,” and the variability of their songs is thought to underlie a process of trial-and-error vocal learning. It is known that this exploratory variability requires the “cortical” component of a basal ganglia (BG) thalamocortical loop, but less understood is the role of the BG and thalamic components in this behavior. We found that large bilateral lesions to the songbird BG homolog Area X had little or no effect on song variability during vocal babbling. In contrast, lesions to the BG-recipient thalamic nucleus DLM (medial portion of the dorsolateral thalamus) largely abolished normal vocal babbling in young birds and caused a dramatic increase in song stereotypy. These findings support the idea that the motor thalamus plays a key role in the expression of exploratory juvenile behaviors during learning.

scholarly journals Differential contributions of basal ganglia and thalamus to song initiation, tempo, and structure

2014 ◽  
Vol 111 (2) ◽  
pp. 248-257 ◽  
Author(s):  
J. R. Chen ◽  
L. Stepanek ◽  
A. J. Doupe
Keyword(s):  
Basal Ganglia ◽  
Motor Behavior ◽  
Acoustic Structure ◽  
Vocal Plasticity ◽  
Structure Changes ◽  
Cortical Nucleus ◽  
Anterior Forebrain ◽  
Song Production ◽  
Circuit Function ◽  
Area X

Basal ganglia-thalamocortical circuits are multistage loops critical to motor behavior, but the contributions of individual components to overall circuit function remain unclear. We addressed these issues in a songbird basal ganglia-thalamocortical circuit (the anterior forebrain pathway, AFP) specialized for singing and critical for vocal plasticity. The major known afferent to the AFP is the premotor cortical nucleus, HVC. Surprisingly, previous studies found that lesions of HVC alter song but do not eliminate the ability of the AFP to drive song production. We therefore used this AFP-driven song to investigate the role of basal ganglia and thalamus in vocal structure, tempo, and initiation. We found that lesions of the striatopallidal component (Area X) slowed song and simplified its acoustic structure. Elimination of the thalamic component (DLM) further simplified the acoustic structure of song and regularized its rhythm but also dramatically reduced song production. The acoustic structure changes imply that sequential stages of the AFP each add complexity to song, but the effects of DLM lesions on song initiation suggest that thalamus is a locus of additional inputs important to initiation. Together, our results highlight the cumulative contribution of stages of a basal ganglia-thalamocortical circuit to motor output along with distinct involvement of thalamus in song initiation or “gating.”

Singing-Related Activity of Identified HVC Neurons in the Zebra Finch

2007 ◽  
Vol 97 (6) ◽  
pp. 4271-4283 ◽  
Author(s):  
Alexay A. Kozhevnikov ◽  
Michale S. Fee
Keyword(s):  
Vocal Learning ◽  
Primary Source ◽  
Projection Neurons ◽  
Related Activity ◽  
Population Activity ◽  
Antidromic Activation ◽  
Firing Patterns ◽  
Anterior Forebrain ◽  
Song Production ◽  
Area X

High vocal center (HVC) is part of the premotor pathway necessary for song production and is also a primary source of input to the anterior forebrain pathway (AFP), a basal ganglia-related circuit essential for vocal learning. We have examined the activity of identified HVC neurons of zebra finches during singing. Antidromic activation was used to identify three classes of HVC cells: neurons projecting to the premotor nucleus RA, neurons projecting to area X in the AFP, and putative HVC interneurons. HVC interneurons are active throughout the song and display tonic patterns of activity. Projection neurons exhibit highly phasic stereotyped firing patterns. X-projecting (HVC(X)) neurons burst zero to four times per motif, whereas RA-projecting neurons burst extremely sparsely—at most once per motif. The bursts of HVC projection neurons are tightly locked to the song and typically have a jitter of <1 ms. Population activity of interneurons, but not projection neurons, was significantly correlated with syllable patterns. Consistent with the idea that HVC codes for the temporal order in the song rather than for sound, the vocal dynamics and neural dynamics in HVC occur on different and uncorrelated time scales. We test whether HVC(X) neurons are auditory sensitive during singing. We recorded the activity of these neurons in juvenile birds during singing and found that firing patterns of these neurons are not altered by distorted auditory feedback, which is known to disrupt learning or to cause degradation of song already learned.

scholarly journals Thalamostriatal and cerebellothalamic pathways in a songbird, the Bengalese finch

2017 ◽  
Author(s):  
David A. Nicholson ◽  
Todd Roberts ◽  
Samuel J. Sober
Keyword(s):  
Basal Ganglia ◽  
Viral Vector ◽  
Vocal Learning ◽  
Cerebellar Nuclei ◽  
Mammalian Brain ◽  
Neural Basis ◽  
Dorsal Thalamus ◽  
Intralaminar Nuclei ◽  
Song System ◽  
Area X

AbstractThe thalamostriatal system is a major network in the mammalian brain, originating principally from the intralaminar nuclei of thalamus. Functions of the thalamostriatal system remain unclear, but a subset of these projections provides a pathway through which the cerebellum communicates with the basal ganglia. Both the cerebellum and basal ganglia play crucial roles in motor control. Although songbirds have yielded key insights into the neural basis of vocal learning, it is unknown whether a thalamostriatal system exists in the songbird brain. Thalamic nucleus DLM is an important part of the song system, the network of nuclei required for learning and producing song. DLM receives output from song system basal ganglia nucleus Area X and sits within dorsal thalamus, the proposed avian homolog of the mammalian intralaminar nuclei that also receives projections from the cerebellar nuclei. Using a viral vector that specifically labels presynaptic axon segments, we show in Bengalese finches that dorsal thalamus projects to Area X, the basal ganglia nucleus of the song system, and to surrounding medial striatum. To identify the sources of thalamic input to Area X, we map DLM and cerebellar-recipient dorsal thalamus (DTCbN). Surprisingly, we find both DLM and immediately-adjacent subregions of DTCbN project to Area X. In contrast, a medial-ventral subregion of DTCbN projects to medial striatum outside Area X. Our results suggest the basal ganglia in the song system, like the mammalian basal ganglia, integrate feedback from the thalamic region to which they project as well as thalamic regions that receive cerebellar output.

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