Auditory-Dependent Vocal Recovery in Adult Male Zebra Finches Is Facilitated by Lesion of a Forebrain Pathway That Includes the Basal Ganglia

Thompson, John A.; Wu, Wei; Bertram, Richard; Johnson, Frank

doi:10.1523/jneurosci.2853-07.2007

Cited by 49 publications

(59 citation statements)

References 60 publications

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“…This is the first demonstration that LMAN contributes directly to the behavioral deterioration caused by deafening. However, LMAN lesions also rescue changes in song behavior caused by microlesions of HVC (Thompson et al, 2007), and while it is not clear whether the initial vocal deficits result from HVC damage, altered feedback, or both, questions concerning LMANЈs role in behavioral recovery are similar in the two cases. Specifically, Thompson et al argue that song degradation may reflect changes in how HVC and LMAN interact to influence vocal output.…”

Section: Discussionmentioning

confidence: 98%

“…LMAN could contribute directly to the expression of vocal changes seen after deafening since stimulating LMAN triggers immediate changes in song structure (Kao et al, 2005), and this region contributes to natural song variability in both young and adult birds (Kao et al, 2005;Olveczky et al, 2005;Kao and Brainard, 2006;Aronov et al, 2008). Also, LMAN lesions eliminate recently learned adjustments in song provoked by aversive feedback (Andalman and Fee, 2009) and rapidly reverse vocal change produced by microlesions of the descending VMP (Thompson et al, 2007). LMAN may also prompt or permit changes elsewhere.…”

Section: Introductionmentioning

confidence: 99%

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Deafening-Induced Vocal Deterioration in Adult Songbirds Is Reversed by Disrupting a Basal Ganglia-Forebrain Circuit

Nordeen

Nordeen²

2010

J. Neurosci.

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Motor exploration can be an adaptive strategy when behavior fails to achieve an expected outcome. For example, like humans, adult songbirds change their vocal output when auditory feedback is altered or absent. Here, we show that the output of an anterior forebrain pathway (AFP) through the avian basal ganglia directly contributes to the expression of deafening-induced vocal changes in adulthood. Lesioning the output nucleus of this circuit in adult male zebra finches reverses moderate changes in song structure and variability caused by deafening. Furthermore, the results indicate that more severe deafening-induced changes in vocal behavior likely reflect altered function outside the AFP (e.g., within the vocal motor pathway). AFP lesions do not promote recovery if songs are severely deteriorated at the time of lesion even though previous work shows that the AFP is required for such deterioration to emerge. Thus, in birds, as in mammals, the contribution of basal ganglia-thalamic-cortical circuits to motor control may change when feedback is absent or unexpected and includes both "active" and "permissive" roles.

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Section: Discussionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

Deafening-Induced Vocal Deterioration in Adult Songbirds Is Reversed by Disrupting a Basal Ganglia-Forebrain Circuit

Nordeen

Nordeen²

2010

J. Neurosci.

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“…Stereotaxic coordinates from the posterior branch of the midsaggital sinus were used to locate LMAN (rostral: 5.1-5.5 mm; lateral: 1.2-1.8 mm; depth: 1.7-2.1 mm). As in previous studies (Bottjer et al 1984;Brainard andDoupe 2000, 2001;Kao and Brainard 2006;Kittelberger and Mooney 1999;Scharff and Nottebohm 1991;Thompson and Johnson 2006;Thompson et al 2007), we removed LMAN by performing electrolytic lesions. Electrolytic lesions not only destroy the cell bodies of neurons in focal brain areas but can also damage fibers that pass through the area.…”

Section: Lman Lesionsmentioning

confidence: 99%

An Avian Basal Ganglia-Forebrain Circuit Contributes Differentially to Syllable Versus Sequence Variability of Adult Bengalese Finch Song

Hampton

Sakata

Brainard

2009

Journal of Neurophysiology

123

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Hampton CM, Sakata JT, Brainard MS. An avian basal ganglia-forebrain circuit contributes differentially to syllable versus sequence variability of adult Bengalese finch song. J Neurophysiol 101: 3235-3245, 2009. First published April 8, 2009 doi:10.1152/jn.91089.2008. Behavioral variability is important for motor skill learning but continues to be present and actively regulated even in well-learned behaviors. In adult songbirds, two types of song variability can persist and are modulated by social context: variability in syllable structure and variability in syllable sequencing. The degree to which the control of both types of adult variability is shared or distinct remains unknown. The output of a basal ganglia-forebrain circuit, LMAN (the lateral magnocellular nucleus of the anterior nidopallium), has been implicated in song variability. For example, in adult zebra finches, neurons in LMAN actively control the variability of syllable structure. It is unclear, however, whether LMAN contributes to variability in adult syllable sequencing because sequence variability in adult zebra finch song is minimal. In contrast, Bengalese finches retain variability in both syllable structure and syllable sequencing into adulthood. We analyzed the effects of LMAN lesions on the variability of syllable structure and sequencing and on the social modulation of these forms of variability in adult Bengalese finches. We found that lesions of LMAN significantly reduced the variability of syllable structure but not of syllable sequencing. We also found that LMAN lesions eliminated the social modulation of the variability of syllable structure but did not detect significant effects on the modulation of sequence variability. These results show that LMAN contributes differentially to syllable versus sequence variability of adult song and suggest that these forms of variability are regulated by distinct neural pathways.

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“…However, perturbations of auditory feedback (32,33), damage to nucleus HVC (11), deafening (34), or syringeal nerve damage (35) can reinstate song plasticity in adult birds. LMAN lesions before deafening prevent song degradation (35)(36)(37); however, lesions of LMAN do not induce recovery of song that has been allowed to completely degrade (38). It would therefore be interesting to determine whether the capacity for LTD in RA is reinstated in these birds or whether open-ended learners, such as canaries or mockingbirds, which continue to modify their song throughout their lives, show the capacity for LTD in RA during periods of adult song plasticity.…”

Section: Discussionmentioning

confidence: 99%

“…SAP data were exported to Excel. Scatterplots were created and data for each syllable was separated with the filter function of Excel using parameters set by referencing song files in SAP (37). The CV of pitch was calculated for each syllable individually and then averaged for each bird.…”

Section: Methodsmentioning

confidence: 99%

Premotor synaptic plasticity limited to the critical period for song learning

Sizemore

Perkel

2011

Proc. Natl. Acad. Sci. U.S.A.

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Synaptic plasticity has been hypothesized to underlie learning and memory. Understanding of how such plasticity might produce motor learning is limited, in part because of the paucity of model systems with a tractable learned behavior under control of a discrete neural circuit. Songbirds possess both of these traits, thereby providing an excellent model for studying vertebrate motor learning. We report unique evidence of long-term depression (LTD) in the juvenile songbird premotor robust nucleus of the arcopallium (RA). LTD induction at RA recurrent collateral synapses requires NMDA receptors, postsynaptic depolarization, and postsynaptic calcium, and can be reversed by high-frequency stimulation. In adult birds, which have exited the critical period for sensorimotor learning and cannot modify their song, we were no longer able to induce LTD at RA collateral synapses. Furthermore, testosterone-induced premature maturation of song in juveniles abolishes LTD. LTD in nucleus RA therefore makes an excellent candidate mechanism to mediate song learning during development and is well-suited to provide insight into other forms of vertebrate motor learning.L ong-lasting changes in synaptic strength, such as long-term potentiation (LTP) and long-term depression (LTD), have emerged as leading cellular models for the modification of neural circuitry during learning (1). In particular, associative learning induces LTP in the hippocampus (2). Skill learning can increase extracellular field potentials and partially occlude LTP at cortico-cortical synapses in the motor cortex (3), suggesting a similar role for cortical synaptic plasticity in motor learning. However, whether cortical synaptic plasticity underlies motor learning remains unclear, partly because of the distributed nature of cortical motor control and because of the paucity of behavioral paradigms controlled by sufficiently discrete cortical regions.Songbirds provide a highly advantageous model for studying the neural substrate of motor learning. Juvenile birds learn their songs during a critical period by first listening to an adult male tutor (sensory phase) and then practicing, and listening to themselves (sensorimotor phase), until they produce a stereotyped copy of the tutor's vocalization (4) (Fig. 1A). Early vocalizations are highly variable; after thousands of repetitions, however, the song is modified to match the tutor's song and becomes highly stereotyped, or "crystallized" (5).A discrete set of brain nuclei mediates song learning and production (6) (Fig. 1B). This song system can be divided into two functional pathways: the direct motor pathway, which is necessary for song production, and the anterior forebrain pathway (AFP), a cortical-basal ganglia pathway necessary for song learning and some forms of adult song plasticity, but not for the production of learned song (7-11). The premotor robust nucleus of the arcopallium (RA) occupies a crucial position in the song system as the final telencephalic nucleus in the direct motor pathway and the only motor...

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Auditory-Dependent Vocal Recovery in Adult Male Zebra Finches Is Facilitated by Lesion of a Forebrain Pathway That Includes the Basal Ganglia

Cited by 49 publications

References 60 publications

Deafening-Induced Vocal Deterioration in Adult Songbirds Is Reversed by Disrupting a Basal Ganglia-Forebrain Circuit

Deafening-Induced Vocal Deterioration in Adult Songbirds Is Reversed by Disrupting a Basal Ganglia-Forebrain Circuit

An Avian Basal Ganglia-Forebrain Circuit Contributes Differentially to Syllable Versus Sequence Variability of Adult Bengalese Finch Song

Premotor synaptic plasticity limited to the critical period for song learning

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