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Although LMAN is not necessary for singing, neurons in LMAN show strong singing-related immediate early gene expression 20 and neural activity that is correlated with song structure 24, 25. The lateral part of MAN (LMAN) is a critical output node of the vocal cortical-basal ganglia-thalamic circuit onto RA. Abbreviations: Av, avalanche aDLM, anterior dorso-lateral nucleus of the thalamus DM, dorsal medial nucleus of the midbrain H, hyperpallium HVC, a vocal nucleus (no abbreviation) L2, field L2 M, mesopallium MAN, magnocellular nucleus of the anterior nidopallium MO, oval nucleus of the anterior mesopallium N, nidopallium Nif, interfacial nucleus of the nidopallium RA, robust nucleus of the arcopallium XII, 12 th nucleus, tracheosyringeal part. Not all connections are shown, for simplicity. Italicized letters indicates that these regions mainly show motor (m), auditory (a), equally both motor and auditory (m/a) neural activity or activity-dependent gene expression in awake animals. Black arrows, posterior vocal motor pathway White arrows, anterior vocal learning pathway Dashed arrows, connections between the two pathways Red arrow, specialized direct projection from forebrain to brainstem vocal motor neurons in vocal learners. Figure modified from Chakraborty and Jarvis 23.
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Schematic of brain pathways controlling song in songbirds. The song nuclei are adjacent to non-vocal movement activated regions 22, and are proposed to have arisen by duplication of these preexisting motor areas 23, suggesting that discoveries in the song learning systems could be relevant to understanding sensorimotor learning broadly. 1): (1) an anterior song pathway that includes a cortical-striatal-thalamic loop connecting MAN (magnocellular nucleus of the anterior nidopallium) in the cortical analog, to Area X in the striatum, to DLM (dorsal lateral nucleus of the medial thalamus) in the thalamus, and back to MAN, which is necessary for vocal learning and modifying vocalizations in different social contexts 18, 19, 20, 21 and (2) a posterior vocal pathway that projects from the pallial-cortical song nucleus HVC (a vocal nucleus, no abbreviation) to RA (robust nucleus of the arcopallium), to the midbrain vocal center DM (dorsal medial nucleus of the midbrain) and brainstem (nXIIts) vocal motor neurons that control the muscles of the syrinx, necessary for producing learned vocalizations. These forebrain song nuclei are distributed in two pathways (Fig. All vocal learning birds have seven forebrain song nuclei necessary for learning and producing learned vocalizations (Fig. Vocal learning requires a complex and specialized neural circuitry 11, 12, 13. However, studies show that even in a closed-ended vocal learner, there are dynamic changes in sensorimotor processes where song stereotypy and the resistance to modify songs increases with age 8, 9.Therefore, production of stereotyped songs in adult male zebra finches represents an attractive model system to test hypotheses on neural and genetic mechanisms underlying song stereotypy 10. Among avian species, zebra finches are “closed-ended” vocal learners and display little ability to further modify their vocalizations beyond the critical period as adults, when their songs become highly stereotyped 1, 4, 5, 6, 7. Similar to speech in humans, song learning in vocal learning birds occurs most predominantly within a critical period during development 1, 2, 3. Our results suggest that low NR2B subunit expression in adult LMAN is important in conserving features of stereotyped adult courtship song.
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We did not observe these effects in control birds with overexpression of NR2B outside of LMAN or with the green fluorescent protein (GFP) in LMAN. We found that increased NR2B expression in adult LMAN induced increases in song sequence diversity and slower song tempo more similar to juvenile songs, but also increased syllable repetitions similar to stuttering.
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To test for the role of NR2B in generating song plasticity, we manipulated NR2B expression in LMAN of adult male zebra finches by increasing its protein levels to those found in juvenile birds, using a lentivirus containing the full-length coding sequence of the human NR2B subunit. Consistent with this idea, NR2B levels are high in the song learning nucleus LMAN (lateral magnocellular nucleus of the anterior nidopallium) during juvenile vocal learning, and decreases to low levels in adults after learning is complete and the song becomes more stereotyped. One candidate gene implicated in influencing learning is the N-methyl-D-aspartate (NMDA) subtype 2B glutamate receptor ( NR2B). Zebra finches ( Taeniopygia guttata) learn to produce songs in a manner reminiscent of spoken language development in humans.