Postlearning Consolidation of Birdsong: Stabilizing Effects of Age and Anterior Forebrain Lesions

Abstract

Birdsong is a learned, sequenced motor skill. For the zebra finch, learned song normally remains unchanging beyond early adulthood. However, stable adult song will gradually deteriorate after deafening (Nordeen and Nordeen, 1992), indicating an ongoing influence of auditory feedback on learned song. This plasticity of adult song in response to deafening gradually declines with age (Lombardino and Nottebohm, 2000), suggesting that, after song learning, there continue to be changes in the brain that progressively stabilize the song motor program. A qualitatively similar stabilization of learned song can be precipitated artificially by lesions of a basal ganglia circuit in the songbird anterior forebrain (Brainard and Doupe, 2000), raising the question of whether and how these two forms of song stabilization are related. We investigated this issue by characterizing the deterioration of song that occurs after deafening in young adult birds and the degree to which that deterioration is reduced by age or by lesions of the anterior forebrain that were directed at the lateral portion of the magnocellular nucleus of the anterior neostriatum (LMAN). In most respects, LMAN lesions stabilized song to a significantly greater extent than did aging; whereas old-deafened birds eventually exhibited significant deterioration of song, lesioned-deafened birds generally did not differ from controls. The one exception was for song tempo, which was significantly stabilized by age, but not by LMAN lesions. The results indicate that LMAN lesions do not simply mimic a normal aging process, and likewise suggest that the anterior forebrain pathway continues to play a role even in the residual song plasticity that is observed after the agedependent stabilization of song.

Social Modulation of Sequence and Syllable Variability in Adult Birdsong

“…Our results extend the finding of variability regulation from syllable structure to syllable sequencing and suggest that plasticity of syllable sequencing could also be heightened during UD song. Furthermore, our results are consistent with the possibility that species differences in the intrinsic variability of syllable sequencing are correlated with differences in the plasticity of syllable sequencing in adult song; syllable sequencing in adult Bengalese finch song is more variable than in zebra finch song, and adult Bengalese finches demonstrate more rapid plasticity of sequencing following manipulations of auditory feedback than adult zebra finches (Brainard and Doupe 2001;Nordeen and Nordeen 1992;Okanoya and Yamaguchi 1997;Sakata and Brainard 2006;Scott et al 2000;Woolley and Rubel 1997).…”

“…In zebra finches, songs produced to females are faster than songs produced in isolation (Cooper and Goller 2006;Kao and Brainard 2006;Sossinka and Böhner 1980), and lesions of IMAN lead to a gradual acceleration of song and an attenuation of context effects on song tempo (Brainard and Doupe 2001;Kao and Brainard 2006;Williams and Mehta 1999). Alterations in vocal quality are often reported in patients with Parkinson's disease (Goberman et al 2005;reviewed in Pinto 2004), and interference with dopamine function alters the bandwidth of ultrasonic vocalizations in rats (Ciucci et al 2007).…”

Vocal learning is constrained by the statistics of sensorimotor experience

“…Although the mechanisms governing juvenile song acquisition and adult error correction might be distinct, it is possible that they rely on the same underlying computation. Although the absolute size of errors in young birds is very large, so is the variability of song itself (25)(26)(27)(28)(29). Constraining learning based on variability (Fig.…”

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

“…Pairing-induced potentiation in male adult zebra finches provides a possible mechanism underlying active song maintenance in adult songbirds and could also contribute to song degradation known to occur after manipulation of the auditory feedback (Woolley and Rubel, 1997;Leonardo and Konishi, 1999;Lombardino and Nottebohm, 2000;Brainard and Doupe, 2001) or tracheosyringeal nerve injury (Williams and Mehta, 1999). We next tested whether this form of LTP is also present in young zebra finches undergoing song learning.…”

“…LTP is inducible in adult and juvenile birds, suggesting that it may contribute to song degradation in adult birds, induced by manipulations of auditory feedback or sectioning of tracheosyringeal nerves (Woolley and Rubel, 1997;Leonardo and Konishi, 1999;Williams and Mehta, 1999;Lombardino and Nottebohm, 2000;Brainard and Doupe, 2001), and to sensorimotor learning in juvenile birds. Although our inability to induce LTP in younger birds does not necessarily exclude its presence, the difficulty suggests that this form of plasticity may not play a primary role during sensory learning.…”