Early sensory and hormonal experience modulate age-related changes in NR2B mRNA within a forebrain region controlling avian vocal learning

Singh, Tryambak Deo; Basham, Mark E.; Nordeen, Ernest J.; Nordeen, Kathy W.

doi:10.1002/1097-4695(200007)44:1<82::aid-neu8>3.0.co;2-w

Cited by 54 publications

(37 citation statements)

References 70 publications

(130 reference statements)

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“…Nearly all glutamate receptor subunits/ subtypes showed differential expression in one or more cerebral vocal nuclei. Prior studies have shown differential expression of some genes in songbird and parrot vocal nuclei (Arnold et al, 1976;Bottjer, 1993;Ball, 1994;Casto and Ball, 1994;Aamodt et al, 1995;Holzenberger et al, 1997;Durand et al, 1998;Denisenko-Nehrbass et al, 2000), including the three previously cloned glutamate receptor subunits, NR1, NR2A, and NR2B from songbirds (Singh et al, 2000;Heinrich et al, 2002). However, none have shown systematic differential expression of nearly one entire gene family and across all vocal learning orders.…”

Section: Discussionmentioning

confidence: 98%

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Differential expression of glutamate receptors in avian neural pathways for learned vocalization

Wada

Sakaguchi

Jarvis

et al. 2004

J of Comparative Neurology

141

188

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Learned vocalization, the substrate for human language, is a rare trait. It is found in three distantly related groups of birds-parrots, hummingbirds, and songbirds. These three groups contain cerebral vocal nuclei for learned vocalization not found in their more closely related vocal nonlearning relatives. Here, we cloned 21 receptor subunits/subtypes of all four glutamate receptor families (AMPA, kainate, NMDA, and metabotropic) and examined their expression in vocal nuclei of songbirds. We also examined expression of a subset of these receptors in vocal nuclei of hummingbirds and parrots, as well as in the brains of dove species as examples of close vocal nonlearning relatives. Among the 21 subunits/subtypes, 19 showed higher and/or lower prominent differential expression in songbird vocal nuclei relative to the surrounding brain subdivisions in which the vocal nuclei are located. This included relatively lower levels of all four AMPA subunits in lMAN, strikingly higher levels of the kainite subunit GluR5 in the robust nucleus of the arcopallium (RA), higher and lower levels respectively of the NMDA subunits NR2A and NR2B in most vocal nuclei and lower levels of the metabotropic group I subtypes (mGluR1 and -5) in most vocal nuclei and the group II subtype (mGluR2), showing a unique expression pattern of very low levels in RA and very high levels in HVC. The splice variants of AMPA subunits showed further differential expression in vocal nuclei. Some of the receptor subunits/subtypes also showed differential expression in hummingbird and parrot vocal nuclei. The magnitude of differential expression in vocal nuclei of all three vocal learners was unique compared with the smaller magnitude of differences found for nonvocal areas of vocal learners and vocal nonlearners. Our results suggest that evolution of vocal learning was accompanied by differential expression of a conserved gene family for synaptic transmission and plasticity in vocal nuclei. They also suggest that neural activity and signal transduction in vocal nuclei of vocal learners will be different relative to the surrounding brain areas.

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Section: Discussionmentioning

confidence: 98%

“…However, to date only three glutamate receptor subunits have been cloned from the songbird brain (NR1, NR2A, and NR2B, belonging to the NMDA subfamily; Singh et al, 2000;Heinrich et al, 2002). Here we report the identification and presence of nearly all glutamate receptor subunits/subtypes discovered in mammals within the songbird brain.…”

mentioning

confidence: 90%

Differential expression of glutamate receptors in avian neural pathways for learned vocalization

Wada

Sakaguchi

Jarvis

et al. 2004

J of Comparative Neurology

141

188

View full text Add to dashboard Cite

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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%

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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“…For example, ZENK induced by hearing conspecific song could influence the expression of NR1 in the MSt outside of Area X. ZENK is integral in the modulation of neuronal excitability (reviewed in [17]), and expression of zif-268 (of which ZENK is an avian homolog) in rodents plays a role in maintaining plastic changes associated with long-term potentiation (LTP) [17]. 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].…”

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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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Early sensory and hormonal experience modulate age-related changes in NR2B mRNA within a forebrain region controlling avian vocal learning

Cited by 54 publications

References 70 publications

Differential expression of glutamate receptors in avian neural pathways for learned vocalization

Differential expression of glutamate receptors in avian neural pathways for learned vocalization

Development of NMDA R1 expression in chicken auditory brainstem

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

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