Representation of early sensory experience in the adult auditory midbrain: implications for vocal learning

Abstract

Vocal learning in songbirds and humans occurs by imitation of adult vocalizations. In both groups, vocal learning includes a perceptual phase during which juveniles birds and infants memorize adult vocalizations. Despite intensive research, the neural mechanisms supporting this auditory memory are still poorly understood. The present functional MRI study demonstrates that in adult zebra finches, the right auditory midbrain nucleus responds selectively to the copied vocalizations. The selective signal is distinct from selectivity for the bird's own song and does not simply reflect acoustic differences between the stimuli. Furthermore, the amplitude of the selective signal is positively correlated with the strength of vocal learning, measured by the amount of song that experimental birds copied from the adult model. These results indicate that early sensory experience can generate a long-lasting memory trace in the auditory midbrain of songbirds that may support song learning.

Figure 1. Sonograms illustrating the song tutoring protocol for two experimental birds (Bird 1 and Bird 2).

Tutors 1 and 2 learned their song from the same song model (via tape playback) while experimental birds 1 and 2 learned their song by being housed with respectively tutor 1 and tutor 2 (one-to-one paradigm). As a result, songs of Bird 1 and 2 were acoustically close. During the fMRI experiment, bird 1 was exposed to the song of bird 1 (BOS), the song of Tutor 1 (TUT) and the song of Bird 2 (CON).

Figure 2. Statistical maps of BOLD activation induced by all stimuli together.

Results (compared to Rest) are superimposed on anatomical sagittal and axial images coming from the MRI zebra finch atlas. T values are color coded according to the scale displayed on the right side of the figure. Only significant voxels (one-tailed t-test, p<0.05, corrected at the whole brain level) are displayed. L: left, R: right, D: dorsal, V: ventral, A: anterior, P: posterior.

Figure 3. Illustration of the predefined regions of interest on sagittal and axial anatomical images.

The anatomical images come from the zebra finch MRI atlas. L: left, R: right, D: dorsal, V: ventral, A: anterior, P: posterior.

Figure 4. Statistical maps of BOLD activation induced by the different stimuli in left and right MLd.

Results are superimposed on sagittal anatomical slices coming from the MRI zebra finch atlas. T values are color coded according to the scale displayed at the bottom of the figure. Note that the analysis was restricted to MLd and only voxels found to be significant (one-tailed t-test, p<0.05, corrected at MLd level) are displayed. D: dorsal, V: ventral, A: anterior, P: posterior.

Figure 5. Correlation between MRI signals and the acoustic similarity between the stimuli in right MLd.

The MRI signals (expressed in non-dimensional units) correspond to the mean amplitude estimate of the differential BOLD signals between TUT and CON (left), BOS and CON (middle) and TUT and BOS (right). Positive values on the y axis indicate higher activations induced by the first stimulus of the comparison than the second one while negative values indicate higher activations induced by the second stimulus of the comparison than the first one. All correlations are statistically non-significant.

Figure 6. Correlation of TUT (left) and BOS (right) selectivity with vocal learning strength in right MLd.

TUT and BOS selectivity are expressed as the mean amplitude estimate of the differential BOLD signals of [TUT minus CON], and [BOS minus CON], in non-dimensional units. Positive values on the y axis indicate a higher activation induced by TUT (or BOS) compared to CON while negative values indicate a higher activation induced by CON compared to TUT (or BOS). Both correlations are statistically significant.

Figure 7. Statistical maps of BOLD activation induced by the different stimuli in left and right NCM.

Results are superimposed on sagittal anatomical slices coming from the zebra finch MRI atlas. T values are color coded according to the scale displayed at the bottom of the figure. Note that in the figure other auditory regions (Field L and caudo-medial mesopallium) seem not activated only because the statistical analysis was restricted to NCM (for the whole activation pattern in the telencephalic auditory regions, see fig. 2). Only significant voxels (one-tailed t-test, p<0.05, corrected at NCM level) are displayed. D: dorsal, V: ventral, A: anterior, P: posterior.

Figure 8. Correlation map of [TUT minus Rest] versus vocal learning strength in left NCM.

Results are superimposed on sagittal and axial anatomical slices coming from the zebra finch MRI atlas and displayed at a p threshold of 0.05 without correction for multiple tests. R² values are color coded according to the scale displayed at the right side of the figure. D: dorsal, V: ventral, A: anterior, P: posterior; L: left; R: right.

Figure 9. Correlation of TUT, BOS and CON responsiveness with vocal learning strength in left NCM.

TUT, BOS and CON responsiveness are expressed as the mean amplitude estimates of the BOLD activations [TUT minus Rest], [BOS minus Rest] and [CON minus Rest], in non-dimensional unit) in the left NCM cluster illustrated in Fig. 8. Note that the R² value in the left panel (0.3089) corresponds to the correlation value between learning strength and the [TUT minus Rest] signal averaged over the NCM cluster illustrated in Fig. 8 whereas the value reported in the text (0.36) corresponds to the correlation in the voxel where this correlation is the highest (R² _max). These two R² values are significantly different than 0. Correlation of BOS and CON responsiveness with learning strength are not significant.

Figure 10. Schematic representation of the songbird brain (parasagittal view).

The auditory regions are in blue and the vocal motor regions in grey. Only the main connections are represented. NIf: nucleus interface of the nidopallium; Ov: nucleus ovoidalis; RA: nucleus robustus of the arcopallium; Uva: nucleus uvaeformis; CN: cochlear nucleus.