Long-Term Potentiation in an Avian Basal Ganglia Nucleus Essential for Vocal Learning

Ding, Long; Perkel, David J.

doi:10.1523/jneurosci.4358-03.2004

Cited by 89 publications

(62 citation statements)

References 52 publications

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“…NIH-PA Author Manuscript NIH-PA Author Manuscript the "critical period" window for plasticity in mouse visual cortex (Quinlan et al, 1999a) and barrel cortex ) and in vocal learning regions of songbirds (Basham et al, 1999;Singh et al, 2000;Ding and Perkel, 2004). Near the end of the critical period, there is a gradual increase in the contribution of NR2A subunits in parallel with changes in NMDAR-mediated currents.…”

Section: Nih-pa Author Manuscriptmentioning

confidence: 99%

“…Forebrain NMDAR are composed of NR2B and NR1 subunits during the critical period, followed by a progressive inclusion of the NR2A subunit in parallel with changes in NMDAR-mediated currents (Stocca and Vicini, 1998;Basham et al, 1999;Quinlan et al, 1999a;Singh et al, 2000;Ding and Perkel, 2004;Liu et al, 2004). Later in development, the proportion of NMDAR consisting of NR2B and NR1 in visual cortex may be altered by changing visual experience (Quinlan et al, 1999b;Philpot et al, 2001).…”

Section: Nmdar Subunit Changes and Development Of The Circuit For Detmentioning

confidence: 99%

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Development of NMDA R1 expression in chicken auditory brainstem

Tang

Carr

2004

Hearing Research

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N-methyl-D-aspartate (NMDA) receptor subunit-specific probes were used to characterize developmental changes in the distribution of excitatory amino acid receptors in the chicken's auditory brainstem nuclei. Although NR1 subunit expression does not change greatly during the development of the cochlear nuclei in the chicken Hear. , there are significant developmental changes in NR2 subunit expression. We used in situ hybridization against NR1, NR2A, NR2B, NR2C, and NR2D to compare NR1 and NR2 expression during development. All five NMDA subunits were expressed in the auditory brainstem before embryonic day (E) 10, when electrical activity and synaptic responses appear in the nucleus magnocellularis (NM) and the nucleus laminaris (NL). At this time, the dominant form of the receptor appeared to contain NR1 and NR2B. NR2A appeared to replace NR2B by E14, a time that coincides with synaptic refinement and evoked auditory responses. NR2C did not change greatly during auditory development, whereas NR2D increased from E10 and remained at fairly high levels into adulthood. Thus changes in NMDA NR2 receptor subunits may contribute to the development of auditory brainstem responses in the chick. Indexing termscochlear nucleus; magnocellularis; laminaris; angularis; tonotopic gradient Physiological studies have shown that the auditory system is characterized by fast, accurate encoding of auditory information (Warchol and Dallos, 1990; Zhang and Trussell, 1994a,b;Fukui and Ohmori, 2003). We have therefore investigated the distribution of subtypes of Nmethyl-D-aspartate (NMDA) receptors (NMDAR) in the brainstem auditory nuclei of the chicken to determine whether changes in receptors may reflect the development of specializations for temporal processing. NMDAR can contain two classes of subunits, NR1 and NR2 (A-D). The third class of subunits (NR3), containing NR3A and NR3B, is thought to act as modulators of the NMDAR (Ciabarra et al., 1995;Nishi et al., 2001; for review see Cull-Candy, 2001). A functional NMDAR appears to consist of two NR1 subunits and two or three NR2 subunits. NR1 is the fundamental subunit necessary for the NMDAR complex, and its expression is spatiotemporally ubiquitous compared with that of NR2 subunits in vertebrate brain (Watanabe et al., 1992;Wada et al., 2004).Changes in NMDAR composition characterize the development of forebrain circuits. NR2B has been shown to be necessary for synapse formation and plasticity (Tang et al., 1999;Slutsky et al., 2004), whereas NR2A expression is associated with synaptic maturation (Fu et al., 2005). NMDAR made up of NR2B and NR1 subunits are the dominant form during NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript the "critical period" window for plasticity in mouse visual cortex (Quinlan et al., 1999a) and barrel cortex ) and in vocal learning regions of songbirds (Basham et al., 1999;Singh et al., 2000;Ding and Perkel, 2004). Near the end of the critical period, there is a gradual increase in the contribution of NR2A subunits i...

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Section: Nih-pa Author Manuscriptmentioning

confidence: 99%

Section: Nmdar Subunit Changes and Development Of The Circuit For Detmentioning

confidence: 99%

Development of NMDA R1 expression in chicken auditory brainstem

Tang

Carr

2004

Hearing Research

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“…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].…”

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confidence: 99%

“…Glutamatergic receptors are important in LTP as well [22], and activation of them during song template acquisition is vital to song learning and perhaps even the opening of the sensitive period for it [1,5,10,22,27,29]. Evidence from slice preparations from adult males and those as young as d47 shows that neurons within Area X exhibit activity-dependent LTP that is not induced between d24 and d37 [7] and can be blocked by the NMDA receptor antagonist AP5 [7]. An analysis of whether ZENK and these other genes are co-expressed at various developmental stages in cells within Area X and the rest of the MSt following directed singing and presentations of conspecific song can lead to more of an understanding of their roles in influencing song learning and behavior.…”

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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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“…This LTD was not accompanied by a change in the paired-pulse ratio (119 ± 12% of baseline, n = 9, P = 0.20), suggesting that release probability was not altered. High-frequency stimulation (HFS; 100-Hz presynaptic stimulation for 1 s, delivered three times with postsynaptic depolarization to 0 mV), which induces LTP in other brain regions (1,19), caused EPSC amplitude to return to baseline levels ( Fig. 2E) (147 ± 39% of baseline, n = 5, P = 0.275).…”

Section: Resultsmentioning

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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Long-Term Potentiation in an Avian Basal Ganglia Nucleus Essential for Vocal Learning

Cited by 89 publications

References 52 publications

Development of NMDA R1 expression in chicken auditory brainstem

Development of NMDA R1 expression in chicken auditory brainstem

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

Premotor synaptic plasticity limited to the critical period for song learning

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