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

Abstract

In both humans and songbirds, infants learn vocalizations by imitating the sounds of adult tutors with whom they interact during an early sensitive period. Vocal learning occurs in few animal taxa; similarities in the imitation process between humans and songbirds make the songbird a unique system in which vocal learning mechanisms can be studied at the neurobiological level. One theory of vocal learning proposes that early auditory experience generates auditory memories that subsequently guide vocal imitation. We now present a combination of behavioral and neurophysiological results, obtained in a songbird, that support this theory. We show that neurons in a forebrain auditory area of adult male zebra finches are selectively tuned to the song of a tutor heard early in development. Furthermore, the strength of this selectivity shows a striking correlation with the fidelity of vocal imitation, suggesting that this auditory memory may have served as the model for song learning.development ͉ electrophysiology ͉ memory ͉ caudal medial nidopallium ͉ zebra finch

Functional MRI of the zebra finch brain during song stimulation suggests a lateralized response topography

“…In particular, there were significant differences in the BOLD response amplitude for a pure tone versus CON and BOS activation, and the TUT response was different from the BOS response. We could also demonstrate that the auditory responses in the forebrain show high sensitivity to BOS [as was found in electrophysiological recordings in anesthetized birds (22,26,28,38,39)] and TUT in areas corresponding to the higher auditory area NCM [as was found in awake birds (40)], but that other stimuli activate the brain as well.…”

“…Indeed, unit recordings show that neuronal responses are more selectively tuned to learned vocal sounds in NCM (20,21) and CM (43)(44)(45), whereas the primary auditory subregions L2a and L2b are responsive to sounds within the wider species-specific spectrotemporal range (24,46,47). Measurement of long-term response habituation in NCM, by both electrophysiology and the study of the song stimulation-induced up-regulation of ZENK, has suggested that this area might encode the long-lasting sensory memory of the TUT (31,40). Other experiments point to the fact that NCM and CM might be involved in short-term plasticity related to song discrimination (18,19,48).…”

Hemispheric differences in processing of vocalizations depend on early experience

“…In adulthood, we recorded multiunit auditory responses bilaterally in forebrain NCM by using multiple microelectrodes. NCM neurons are known to respond more strongly to conspecific vocalizations than to other sounds (12,13), and show stimulus-specific adaptation: a decrease in response amplitude with repeated playback of the same sound and a slower rate of adaptation for familiar than for novel sounds (12)(13)(14). This adaptation lasts much longer for conspecific vocalizations than for other sounds and can be thought of as a long-term recognition memory for these communication signals.…”

“…We further characterized the auditory responses recorded from left and right NCM by their adaptation rate, which measures the slope of the decrease in response amplitude as a function of repetition number, and can provide a measure of the familiarity of the stimuli tested (12)(13)(14). The differences described below do not simply reflect larger initial responses because the adaptation rate measure is normalized by absolute amplitude to correct for response amplitude (Materials and Methods).…”

“…Male and female zebra finches (Taeniopygia guttata) were raised in individual breeding cages, within the general aviary, with their parents and siblings until ≈10 days after hatch (phd) (14,30). At this time, the hatchlings and the mother were placed into sound-attenuated chambers.…”