Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch

Sohrabji, Farida; Nordeen, Ernest J.; Nordeen, Kathy W.

doi:10.1016/0163-1047(90)90797-a

Cited by 401 publications

(350 citation statements)

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“…Just like intact birds and hearing birds with lesions of Area X (e.g., Fig. 2A, fourth group) (13,15), lesiondeaf birds continued to sing the same stereotyped sequence of syllables (motif), even eight wks after deafening. Effects of experimental manipulations on song were quantified using two measures that represent separately how well the spectral and The AFP of songbirds indirectly connects the motor nuclei HVC and RA, and consists of the basal ganglia (striato-pallidal) nucleus Area X (9, 10), the thalamic nucleus DLM, and the cortical nucleus LMAN.…”

Section: Resultsmentioning

confidence: 99%

“…1A for specific parallels to mammals; although these parallels are not complete (11,12), for simplicity we hereafter refer to LMAN as cortical]. As in mammals, the AFP is not required for the production of well-learned behaviors, but it is critically important for motor plasticity (13)(14)(15)(16)(17)(18). For example, in adult zebra finches, manipulations that distort or eliminate auditory feedback normally drive gradual changes in song structure (Figs.…”

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Task-related “cortical” bursting depends critically on basal ganglia input and is linked to vocal plasticity

Kojima

Kao

Doupe

2013

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

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Basal ganglia-thalamocortical circuits are critical for motor control and motor learning. Classically, basal ganglia nuclei are thought to regulate motor behavior by increasing or decreasing cortical firing rates, and basal ganglia diseases are assumed to reflect abnormal overall activity levels. More recent studies suggest instead that motor disorders derive from abnormal firing patterns, and have led to the hypothesis that surgical treatments, such as pallidotomy, act primarily by eliminating pathological firing patterns. Surprisingly little is known, however, about how the basal ganglia normally influence task-related cortical activity to regulate motor behavior, and how lesions of the basal ganglia influence cortical firing properties. Here, we investigated these questions in a songbird circuit that has striking homologies to mammalian basal ganglia-thalamocortical circuits but is specialized for singing. The “cortical” outflow nucleus of this circuit is required for song plasticity and normally exhibits increased firing during singing and song-locked burst firing. We found that lesions of the striato-pallidal nucleus in this circuit prevented hearing-dependent song changes. These basal ganglia lesions also stripped the cortical outflow neurons of their patterned burst firing during singing, without changing their spontaneous or singing-related firing rates. Taken together, these results suggest that the basal ganglia are essential not for normal cortical firing rates but for driving task-specific cortical firing patterns, including bursts. Moreover, such patterned bursting appears critical for motor plasticity. Our findings thus provide support for therapies that aim to treat basal ganglia movement disorders by normalizing firing patterns.

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Section: Resultsmentioning

confidence: 99%

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confidence: 99%

Task-related “cortical” bursting depends critically on basal ganglia input and is linked to vocal plasticity

Kojima

Kao

Doupe

2013

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

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“…Area X plays an integral role in male song learning and possibly song production in adulthood. For example, juvenile males with Area X ablated produce abnormal song in adulthood, although in adult males lesions of the nucleus have no detectable effect on song production or quality [26,31]. Interestingly, neurons in Area X show singing-related electrophysiological activity that declines slowly after song stops being produced [11], suggesting a function for the region outside of the sensitive period for song learning.…”

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confidence: 99%

“…While it is clear that Area X is important for song learning in juvenile males [31], the MSt outside of this region may serve functions likely to be more common in the two sexes. Alternatively, the ZENK response in d30 and d45 birds in the present study could result from a specialization of neurons within the MSt during the song-learning period that is not conserved into adulthood.…”

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confidence: 99%

Sexual dimorphism in song-induced ZENK expression in the medial striatum of juvenile zebra finches

Bailey

Wade

2006

Neuroscience Letters

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In the brains of male zebra finches (Taeniopygia guttata), the nuclei that direct song learning and production are larger than the corresponding regions in females, who do not sing. The dimorphism in Area X of the medial striatum (MSt), an area important for song learning, is even more dramatic in that it is identifiable in males but not females by Nissl stain. In the present study, conspecific song, but not other auditory stimuli, induced expression of the immediate early gene ZENK in the MSt surrounding but not within Area X in juvenile males (30 and 45 days post-hatch). ZENK immunoreactivity following conspecific songs was homogeneous throughout the MSt of females at the same ages. Little to no FOS immunoreactivity was observed in Area X or the rest of the MSt, and levels were not influenced by the type of auditory stimulus presented. Thus, the clear morphological difference in the lateral MSt (Area X) of males and females is mirrored by a specific functional one, and the data suggest a role for ZENK expression in the MSt outside of Area X in responding to relevant song stimuli. KeywordsSong perception; Immediate early gene; Area X; Basal ganglia; Song learning; Sex difference Nottebohm and Arnold [23] first described dramatic sexual dimorphisms in the brains of adult zebra finches and canaries wherein regions that control song learning and production are larger in males that sing than in females that do not. One of these regions, Area X of the medial striatum (MSt), is not identifiable via Nissl stains in females. Area X plays an integral role in male song learning and possibly song production in adulthood. For example, juvenile males with Area X ablated produce abnormal song in adulthood, although in adult males lesions of the nucleus have no detectable effect on song production or quality [26,31]. Interestingly, neurons in Area X show singing-related electrophysiological activity that declines slowly after song stops being produced [11], suggesting a function for the region outside of the sensitive period for song learning. Cells in this region in both juveniles and adults also display longterm potentiation [7]. In birds that hear song and sing in response, ZENK expression is increased in Area X compared to birds that hear song only or birds that hear no song [13][14][15]24]. Additionally, when the tracheosyringeal nerve is axotomized in developing males, the electrophysiological activity of some neurons within Area X is then tuned to the abnormal, axotomized bird's own song as well as the tutor's song, suggesting that neurons within Area X are important for vocal practice [32]. In males, the Nissl-defined volume of Area X increases between d10 and d40, when the adult volume is reached [20], and this change in volume is due in part to the addition of neurons during that period in males but not females [16,21].While it is clear that Area X is highly sexually dimorphic and important for the development of song in males, it was unknown whether the corresponding lateral region of MSt in females is resp...

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“…Notably, HVC X axons form synapses on other neurons in HVC and on striatopallidal neurons, but not on song premotor neurons in RA [30,66] (by analogy to mammalian cortical circuitry, HVC X cells resemble cortical pyramidal neurons that extend axons to the basal ganglia but not to the pyramidal tract). While lesions made downstream of HVC in the AFP of adult songbirds do not prevent singing, they can render the song less variable [67,68]. Therefore, while a prevailing view is that HVC X cells are not essential to song production, whether these cells may play a more nuanced role in singing has not been rigorously tested and remains plausible.…”

Section: Role In Productionmentioning

confidence: 99%

Auditory–vocal mirroring in songbirds

Mooney

2014

Phil. Trans. R. Soc. B

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Mirror neurons are theorized to serve as a neural substrate for spoken language in humans, but the existence and functions of auditory-vocal mirror neurons in the human brain remain largely matters of speculation. Songbirds resemble humans in their capacity for vocal learning and depend on their learned songs to facilitate courtship and individual recognition. Recent neurophysiological studies have detected putative auditory-vocal mirror neurons in a sensorimotor region of the songbird's brain that plays an important role in expressive and receptive aspects of vocal communication. This review discusses the auditory and motor-related properties of these cells, considers their potential role on song learning and communication in relation to classical studies of birdsong, and points to the circuit and developmental mechanisms that may give rise to auditory-vocal mirroring in the songbird's brain.

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Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch

Cited by 401 publications

References 18 publications

Task-related “cortical” bursting depends critically on basal ganglia input and is linked to vocal plasticity

Task-related “cortical” bursting depends critically on basal ganglia input and is linked to vocal plasticity

Sexual dimorphism in song-induced ZENK expression in the medial striatum of juvenile zebra finches

Auditory–vocal mirroring in songbirds

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