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

Satoshi Kojima; Allison J. Doupe

doi:10.1152/jn.00916.2006

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

Journal of Neurophysiology ◽

10.1152/jn.00916.2006 ◽

2007 ◽

Vol 98 (4) ◽

pp. 2099-2109 ◽

Cited By ~ 22

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.

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Intrinsic and Synaptic Properties of Neurons in an Avian Thalamic Nucleus During Song Learning

Journal of Neurophysiology ◽

10.1152/jn.2002.88.4.1903 ◽

2002 ◽

Vol 88 (4) ◽

pp. 1903-1914 ◽

Cited By ~ 20

Author(s):

Minmin Luo ◽

David J. Perkel

Keyword(s):

Basal Ganglia ◽

Reversal Potential ◽

Song Learning ◽

Equilibrium Potential ◽

Sensorimotor Learning ◽

Acid Decarboxylase ◽

Inhibitory Input ◽

Zebra Finches ◽

Intrinsic Properties ◽

Area X

The anterior forebrain pathway (AFP) of the avian song system is a circuit essential for song learning but not for song production. This pathway consists of a loop serially connecting area X in the basal ganglia, the medial portion of the dorsolateral nucleus of thalamus (DLM), and the pallial lateral magnocellular nucleus of the anterior neostriatum (lMAN). The majority of DLM neurons in adult male zebra finches closely resemble mammalian thalamocortical neurons in both their intrinsic properties and the strong GABAergic inhibitory input they receive from the basal ganglia. These observations support the hypothesis that the AFP and the mammalian basal ganglia-thalamocortical pathway use similar information-processing mechanisms during sensorimotor learning. Our goal was to determine whether the cellular properties of DLM neurons are already established in juvenile birds in the sensorimotor phase of song learning when the AFP is essential. Current- and voltage-clamp recording in DLM of juvenile male zebra finches showed that juvenile DLM has two distinct cell types with intrinsic properties largely similar to those of their respective adult counterparts. Immunostaining for glutamic acid decarboxylase (GAD) in juvenile zebra finches revealed that, as in adults, most area X somata are large and strongly GAD+ and that their terminals in DLM form dense GAD+ baskets around somata. GAD immunoreactivity in DLM was depleted by lesions of area X, indicating that a strong GABAergic projection from area X to DLM is already established in juveniles. Some of the DLM neurons exhibited large, spontaneous GABAergic synaptic events. Stimulation of the afferent pathway evoked an inhibitory postsynaptic potential or current that was blocked by the GABAA receptor antagonist bicuculline methiodide. The decay of the GABAAreceptor-mediated currents was slower in juvenile neurons than in adults. In addition, the reversal potential for these currents in juveniles was significantly more depolarized both than that in adults and than the Cl− equilibrium potential; yet the reversal potential was still well below the firing threshold and thus inhibitory in the slice preparation. Our findings suggest that the signal-processing role of DLM during sensorimotor learning is generally similar to that in adulthood but that quantitative changes in synaptic transmission accompany the development of stereotyped song.

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A subcortical circuit linking the cerebellum to the basal ganglia engaged in vocal learning

10.1101/198317 ◽

2017 ◽

Cited By ~ 1

Author(s):

Ludivine Pidoux ◽

Pascale Leblanc ◽

Arthur Leblois

Keyword(s):

Basal Ganglia ◽

Vocal Learning ◽

Song Learning ◽

Sensorimotor Learning ◽

Zebra Finches ◽

Subcortical Structures ◽

Song Production ◽

Cerebellar Lesions ◽

Avian Song

AbstractSpeech is a complex sensorimotor skill, and vocal learning involves both the basal ganglia and the cerebellum. These subcortical structures interact indirectly through their respective loops with thalamo-cortical and brainstem networks, and directly via subcortical pathways, but the role of their interaction during sensorimotor learning remains undetermined. While songbirds and their song-dedicated basal ganglia-thalamo-cortical circuitry offer a unique opportunity to study subcortical circuits involved in vocal learning, the cerebellar contribution to avian song learning remains unknown. We demonstrate that the cerebellum provides a strong input to the song-related basal ganglia nucleus in zebra finches. Cerebellar signals are transmitted to the basal ganglia via a disynaptic connection through the thalamus and then conveyed to their cortical target and to the premotor nucleus controlling song production. Finally, cerebellar lesions impair juvenile song learning, opening new opportunities to investigate how subcortical interactions between the cerebellum and basal ganglia contribute to sensorimotor learning.

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A subcortical circuit linking the cerebellum to the basal ganglia engaged in vocal learning

eLife ◽

10.7554/elife.32167 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 13

Author(s):

Ludivine Pidoux ◽

Pascale Le Blanc ◽

Carole Levenes ◽

Arthur Leblois

Keyword(s):

Basal Ganglia ◽

Vocal Learning ◽

Song Learning ◽

Sensorimotor Learning ◽

Zebra Finches ◽

Subcortical Structures ◽

Song Production ◽

Cerebellar Lesions ◽

Avian Song

Speech is a complex sensorimotor skill, and vocal learning involves both the basal ganglia and the cerebellum. These subcortical structures interact indirectly through their respective loops with thalamo-cortical and brainstem networks, and directly via subcortical pathways, but the role of their interaction during sensorimotor learning remains undetermined. While songbirds and their song-dedicated basal ganglia-thalamo-cortical circuitry offer a unique opportunity to study subcortical circuits involved in vocal learning, the cerebellar contribution to avian song learning remains unknown. We demonstrate that the cerebellum provides a strong input to the song-related basal ganglia nucleus in zebra finches. Cerebellar signals are transmitted to the basal ganglia via a disynaptic connection through the thalamus and then conveyed to their cortical target and to the premotor nucleus controlling song production. Finally, cerebellar lesions impair juvenile song learning, opening new opportunities to investigate how subcortical interactions between the cerebellum and basal ganglia contribute to sensorimotor learning.

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

Neural Plasticity ◽

10.1155/2020/6647389 ◽

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.

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Properties of Dopamine Release and Uptake in the Songbird Basal Ganglia

Journal of Neurophysiology ◽

10.1152/jn.01053.2004 ◽

2005 ◽

Vol 93 (4) ◽

pp. 1871-1879 ◽

Cited By ~ 28

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.

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Endocannabinoids mediate synaptic plasticity at glutamatergic synapses on spiny neurons within a basal ganglia nucleus necessary for song learning

Journal of Neurophysiology ◽

10.1152/jn.00676.2010 ◽

2011 ◽

Vol 105 (3) ◽

pp. 1159-1169 ◽

Cited By ~ 9

Author(s):

John A. Thompson ◽

David J. Perkel

Keyword(s):

Synaptic Plasticity ◽

Basal Ganglia ◽

Motor Learning ◽

Metabotropic Glutamate Receptors ◽

Song Learning ◽

Vocal Development ◽

Epsc Amplitude ◽

Spiny Neurons ◽

Group I ◽

Area X

Activation of type 1 cannabinoid receptors (CB1R) in many central nervous system structures induces both short- and long-term changes in synaptic transmission. Within mammalian striatum, endocannabinoids (eCB) are one of several mechanisms that induce synaptic plasticity at glutamatergic terminals onto medium spiny neurons. Striatal synaptic plasticity may contribute a critical component of adaptive motor coordination and procedural learning. Songbirds are advantageous for studying the neural mechanisms of motor learning because they possess a neural pathway necessary for song learning and adult song plasticity that includes a striato-pallidal nucleus, area X (homologous to a portion of mammalian basal ganglia). Recent findings suggest that eCBs contribute to vocal development. For example, dense CB1R expression in song control nuclei peaks around the closure of the sensori-motor integration phase of song development. Also, systemic administration of a CB1R agonist during vocal development impairs song learning. Here we test whether activation of CB1R alters excitatory synaptic input on spiny neurons in area X of adult male zebra finches. Application of the CB1R agonist WIN55212–2 decreased excitatory postsynaptic current (EPSC) amplitude; that decrease was blocked by the CB1R antagonist AM251. Guided by eCB experiments in mammalian striatum, we tested and verified that at least two mechanisms indirectly activate CB1Rs through eCBs in area X. First, activation of group I metabotropic glutamate receptors with the agonist 3,5-dihydroxyphenylglycine (DHPG) induced a CB1R-mediated reduction in EPSC amplitude. Second, we observed that a 10 s postsynaptic depolarization induced a calcium-mediated, eCB-dependent decrease in synaptic strength that resisted rescue with late CB1R blockade. Together, these results show that eCB modulation occurs at inputs to area X spiny neurons and could influence motor learning and production.

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Social context differentially modulates activity of two interneuron populations in an avian basal ganglia nucleus

Journal of Neurophysiology ◽

10.1152/jn.00622.2016 ◽

2016 ◽

Vol 116 (6) ◽

pp. 2831-2840 ◽

Cited By ~ 3

Author(s):

Sarah C. Woolley

Keyword(s):

Basal Ganglia ◽

Cell Types ◽

Behavioral State ◽

Zebra Finches ◽

Multiple Cell ◽

Fast Spiking ◽

Behavioral Transition ◽

Area X ◽

Spontaneous Singing

Basal ganglia circuits are critical for the modulation of motor performance across behavioral states. In zebra finches, a cortical-basal ganglia circuit dedicated to singing is necessary for males to adjust their song performance and transition between spontaneous singing, when they are alone (“undirected” song), and a performance state, when they sing to a female (“female-directed” song). However, we know little about the role of different basal ganglia cell types in this behavioral transition or the degree to which behavioral context modulates the activity of different neuron classes. To investigate whether interneurons in the songbird basal ganglia encode information about behavioral state, I recorded from two interneuron types, fast-spiking interneurons (FSI) and external pallidal (GPe) neurons, in the songbird basal ganglia nucleus area X during both female-directed and undirected singing. Both cell types exhibited higher firing rates, more frequent bursting, and greater trial-by-trial variability in firing when male zebra finches produced undirected songs compared with when they produced female-directed songs. However, the magnitude and direction of changes to the firing rate, bursting, and variability of spiking between when birds sat silently and when they sang undirected and female-directed song varied between FSI and GPe neurons. These data indicate that social modulation of activity important for eliciting changes in behavioral state is present in multiple cell types within area X and suggests that social interactions may adjust circuit dynamics during singing at multiple points within the circuit.

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

Journal of Neurophysiology ◽

10.1152/jn.00584.2012 ◽

2014 ◽

Vol 111 (2) ◽

pp. 248-257 ◽

Cited By ~ 9

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.”

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