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.”

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 The Adjustment of Anterior Forebrain Pathway (AFP) to Birdsong Is Phased during Song Learning and Maintenance

2020 ◽  
Vol 2020 ◽  
pp. 1-17
Author(s):  
Jie Zang ◽  
Shenquan Liu
Keyword(s):  
Basal Ganglia ◽  
Auditory Feedback ◽  
Specific Effect ◽  
Song Learning ◽  
Exact Role ◽  
Anterior Forebrain Pathway ◽  
Anterior Forebrain ◽  
Song Production ◽  
Two Phases

Anterior forebrain pathway (AFP), a basal ganglia-dorsal forebrain circuit, significantly impacts birdsong, specifically in juvenile or deaf birds. Despite many physiological experiments supporting AFP’s role in song production, the mechanism underlying it remains poorly understood. Using a computational model of the anterior forebrain pathway and song premotor pathway, we examined the dynamic process and exact role of AFP during song learning and distorted auditory feedback (DAF). Our simulation suggests that AFP can adjust the premotor pathway structure and syllables based on its delayed input to the robust nucleus of the archistriatum (RA). It is also indicated that the adjustment to the synaptic conductance in the song premotor pathway has two phases: normal phases where the adjustment decreases with an increasing number of trials and abnormal phases where the adjustment remains stable or even increases. These two phases alternate and impel a specific effect on birdsong based on AFP’s specific structures, which may be associated with auditory feedback. Furthermore, our model captured some characteristics shown in birdsong experiments, such as similarities in pitch, intensity, and duration to real birds and the highly abnormal features of syllables during DAF.

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.

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.

scholarly journals Song Selectivity in the Pallial-Basal Ganglia Song Circuit of Zebra Finches Raised Without Tutor Song Exposure

2007 ◽  
Vol 98 (4) ◽  
pp. 2099-2109 ◽  
Author(s):  
Satoshi Kojima ◽  
Allison J. Doupe
Keyword(s):  
Basal Ganglia ◽  
Song Learning ◽  
Sensorimotor Learning ◽  
Zebra Finches ◽  
Auditory Neurons ◽  
Sensory Learning ◽  
Anterior Forebrain ◽  
Acoustic Experience ◽  
Area X ◽  
Insight Into

Acoustic experience critically influences auditory cortical development as well as emergence of highly selective auditory neurons in the songbird sensorimotor circuit. In adult zebra finches, these “song-selective” neurons respond better to the bird's own song (BOS) than to songs of other conspecifics. Birds learn their songs by memorizing a tutor's song and then matching auditory feedback of their voice to the tutor song memory. Song-selective neurons in the pallial-basal ganglia circuit called the anterior forebrain pathway (AFP) reflect the development of BOS. However, during learning, they also respond strongly to tutor song and are compromised in their adult selectivity when birds are prevented from matching BOS to tutor, suggesting that selectivity depends on tutor song learning as well as sensorimotor matching of BOS feedback to the tutor song memory. We examined the contribution of sensory learning of tutor song to song selectivity by recording from AFP neurons in birds reared without exposure to adult conspecifics. We found that AFP neurons in these “isolate” birds had highly tuned responses to isolate BOS. The selectivity was as high, and in the striato-pallidal nucleus Area X, even higher than that in normal birds, due to abnormally weak responsiveness to conspecific song. These results demonstrate that sensory learning of tutor song is not necessary for BOS tuning of AFP neurons. Because isolate birds develop their song via sensorimotor learning, our data further illustrate the importance of individual sensorimotor learning for song selectivity and provide insight into possible functions of song-selective neurons.

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 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.

Development of a Selective Response To an Adult Vocalization in Nestling Black-Capped Chickadees

Behaviour ◽  
1995 ◽  
Vol 132 (1-2) ◽  
pp. 1-20 ◽  
Author(s):  
Janine R. Clemmons
Keyword(s):  
Experimental Evidence ◽  
Auditory Sensitivity ◽  
Field Observations ◽  
Parus Atricapillus ◽  
Acoustic Structure ◽  
Nesting Site ◽  
Song Production

AbstractThere are many studies on how songbirds develop song production, but few on how songbirds develop appropriate responses to conspecific vocalizations. The black-capped chickadee, Parus atricapillus, produces a vocalization, the 'squawk', that stimulates gaping in nestlings during feeding. To determine whether nestlings gape selectively at the squawk, playbacks of several conspecific vocalizations plus a heterospecific vocalization were presented to nestlings within natural nests. A preference for the squawk did not appear until day 2-3 and then steadily increased, until by day 11-13, nestlings gaped only at the squawk. To determine whether there are constraints on which vocalization can develop as the gaping stimulus, newly-hatched nestlings were reinforced with food for gaping either at the squawk or the faint feebee, the two most common adult vocalizations at the nesting site. Regardless of reinforcement, nestlings gaped most frequently at the squawk. In addition, after the first few days posthatch, nestlings became as responsive to a third, unreinforced, heterospecific vocalization as to the squawk. The responsiveness to the heterospecific vocalization coincided with the expanding range of auditory sensitivity that occurs at the same age during passerine development. Thus, while field observations show that nestlings gape mostly to the squawk relative to other parental vocalizations, experimental evidence indicates that there is not an exclusive link between the signal (squawk) and its response (gaping), especially during the first week posthatch when parents use the signal most frequently. Rather, an effectively selective response may be achieved redundantly by a variety of factors. Possible factors that are discussed include matching acoustic structure to nestling perceptual biases and the behavior

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