Sequential Learning From Multiple Tutors and Serial Retuning of Auditory Neurons in a Brain Area Important to Birdsong Learning

Abstract

Yazaki-Sugiyama, Yoko and Richard Mooney. Sequential learning from multiple tutors and serial retuning of auditory neurons in a brain area important to birdsong learning. J Neurophysiol 92: 2771-2788, 2004. First published June 30, 2004 10.1152/jn.00467.2004. Songbirds hear many vocal models during a juvenile sensitive period, transiently imitating some while retaining imitations of others in their repertoires. Despite subsequent conflicting experiences, early experience can exert lasting effects on neural structure and function, raising the possibility that transiently expressed vocalizations or their relevant models are stored in the adult songbird's brain. One site where learned song representations could be stored is the lateral magnocellular nucleus of the anterior nidopallium (LMAN), which in the adult songbird contains neurons responsive to playback of the bird's own song (BOS) and the tutor song (TS). To test whether LMAN neurons develop and retain responses to transiently learned songs, we exposed zebra finch hatchlings [posthatch day 0 (PHD0)] to a first TS (TS1) for about 30 days, isolated them for about 30 days, then exposed them to a second TS (TS2) for 30 days starting at PHD 60. Behavioral analysis showed that PHD 60 juveniles had started to copy TS1, although this copying was transient, because the adult BOS resembled TS2 and not TS1. We found that LMAN auditory responses paralleled these behavioral changes: LMAN neurons at PHD 60 responded strongly and selectively to both the juvenile BOS and TS1, whereas LMAN neurons in adults responded to the adult BOS and TS2, but not to the transiently learned song or its model. Therefore LMAN auditory responses can be lost or overwritten as the juvenile copies a new song, suggesting that the adult LMAN does not store information about transiently learned songs or their models.

Song Selectivity in the Pallial-Basal Ganglia Song Circuit of Zebra Finches Raised Without Tutor Song Exposure

“…Our results clearly demonstrate, however, that despite the presumed lack of an acquired song template in isolate birds, maximal development of BOS selectivity does not require sensory learning of tutor song. The findings here provide further evidence that BOS selectivity is strongly shaped by the bird's experience of its own song during learning and support the idea that song-selective neurons represent an auditory version of the bird's current song (Margoliash 1983;Nick and Konishi 2005;Doupe 1997, 1999;Volman 1993;Yazaki-Sugiyama and Mooney 2004). FIG.…”

“…These results indicate that song selectivity can develop in the AFP in the absence of sensory learning of tutor song and with sensorimotor matching likely limited to innate information about song rather than to a learned template. Together with the existing evidence on how tightly song selectivity follows the motor development of BOS (Doupe 1997;Nick and Konishi 2005;Roy and Mooney 2007;Doupe 1997, 1999;Yazaki-Sugiyama and Mooney 2004), our data provide further support for the critical importance of song sensorimotor learning to the properties of songselective neurons.…”

“…1B), a pallial-basal ganglia circuit that is essential for both sensory and sensorimotor learning (Basham et al 1996;Bottjer et al 1984;Scharff and Nottebohm 1991;Sohrabji et al 1990). By the end of the sensory learning phase and partway through the sensorimotor learning phase (posthatch day 60, PHD 60), auditory neurons in two nuclei of the AFP, Area X and the lateral portion of the magnocellular nucleus of the anterior nidopallium (LMAN), have developed selective responsiveness for the bird's own song (BOS) relative to songs of other zebra finches (conspecifics) and temporally altered versions of BOS, even when BOS has been made abnormal by manipulation of the peripheral motor system (Doupe 1997;Doupe 1997, 1999;Yazaki-Sugiyama and Mooney 2004). This "song selectivity" suggests that these neurons are shaped by the bird hearing its own song during sensorimotor learning.…”

Early auditory experience generates long-lasting memories that may subserve vocal learning in songbirds

“…In those reports, BOS is typically the preferred stimulus, although, during song development, responses selective for the tutor have also been observed (11)(12)(13)(14)(15). In the adult zebra finch, responses to the tutor in the anterior forebrain pathway persist (14,15), but are either very rare (14) or may be attributable to the similarity between the tutor and BOS (15).…”

“…Neurophysiological studies have looked for evidence of this template memory in the auditory responses of song system neurons in both the direct song motor pathway (11) and the anterior forebrain pathway (12)(13)(14)(15), which is implicated in song learning (16,17). In those reports, BOS is typically the preferred stimulus, although, during song development, responses selective for the tutor have also been observed (11)(12)(13)(14)(15).…”