The effects of delayed auditory feedback revealed by bone conduction microphone in adult zebra finches

Abstract

Vocal control and learning are critically dependent on auditory feedback in songbirds and humans. Continuous delayed auditory feedback (cDAF) robustly disrupts speech fluency in normal humans and has ameliorative effects in some stutterers; however, evaluations of the effects of cDAF on songbirds are rare. We exposed singing young (141-151 days old) adult zebra finch males to high-amplitude cDAF. cDAF exposure was achieved by the recording of bone-conducted sounds using a piezoelectric accelerometer, which resulted in high-quality song recordings that were relatively uncontaminated by airborne sounds. Under this condition of cDAF, birds rapidly (2-6 days) changed their song syllable timing. The one bird for which we were able to maintain the accelerometer recordings over a long period of time recovered slowly over more than a month after cDAF was discontinued. These results demonstrate that cDAF can cause substantial changes in the motor program for syllable timing generation over short intervals of time in adult zebra finches.

Figure 1. Examples of bone conduction sounds recorded using piezoelectric accelerometers that were chronically mounted to the skulls of zebra finches.

(A) Picture of the accelerometer attached to the lateral surface of a zebra finch's skull. (B) Example spectrograms of a bone-conducted song of bird zf_yl11 recorded with an accelerometer (upper panel) and the same airborne song recoded by a microphone (lower panel). The recordings are shown for the frequency range below 4 kHz to facilitate evaluation of the similarity of the two spectrograms. The bone conduction song recording shows relatively higher power in the low frequency range (below 1 kHz) compared to the airborne recording. (C) Upper panel: The average of the power spectra of the bone-conducted and airborne songs recorded from five birds (solid line: average, dotted lines: ±SEM). For each bird, the spectrum was computed for syllables from 10 motifs and normalized by the power of the background noise level computed from silent periods (i.e., the log power noise was subtracted). The means and standard errors were computed from the log power spectra. The power spectrum of the airborne songs (P_mic; red line) shows lower power over a range of low frequencies (circa 400 Hz–850 Hz) compared to the power spectrum of the bone conduction songs (P_bone; blue line). Lower panel: The ratio between P_bone and P_mic was plotted in dB scale (i.e. 10 log₁₀(P_bone/P_mic)). This comparison is valid between 200 and 4000 Hz (see Methods).

Figure 2. Bone-conducted and airborne sound recorded simultaneously during loud continuous DAF.

The accelerometer recording of the bone-conducted sound during singing under loud continuous DAF (time delay of 100 ms) is shown in the top panel. The microphone recording of airborne sounds is shown in the bottom panel. The superposition of the bird's vocalization and the DAF from the speaker is noticeable. The accelerometer detected little of the DAF; for example, there are only a few low-amplitude delayed versions of the strongest signals visible in the spectrograms (which occur for the strongest spectral lines between 4 and 5 kHz; see the blue arrows). In contrast, the microphone recording clearly reflects two overlapping signals.

Figure 3. Exemplar song spectrograms before and after song de-crystallization from three birds exposed to DAF.

In each pair of spectrograms ((A) zf_yl11, (B) zf_yl47, (C), zf_bl117), the upper trace represents a normal song prior to de-crystallization, and the lower trace represents a song with abnormal syllable sequence that was recorded after de-crystallization while the bird was experiencing DAF. All spectrograms were derived from the bone-conducted sounds recorded via accelerometers; see the text. The durations of the inter-onset intervals (IOIs) of the detected ("target") syllables are indicated by blue lines and text. These examples all show typical effects of the DAF treatment, including songs with normal as well as abnormal syllable sequences, and little apparent effect on syllable morphology even in the presence of large effects on syllable sequence. Note that the de-crystallized songs had missing syllables and, hence, shorter IOIs. Each syllable is labeled by an alphabet (A, B, C,…). “n” in the upper panel in (A) indicates a connecting note between motifs. All exemplars are of a single song bout except for the lower trace in panel (C), which has two inter-syllable intervals ≥200 ms (see arrows), hence three song bouts.

Figure 4. Changes in the distribution of the inter–onset intervals (IOIs) during the initial days of DAF exposure in three birds.

The left panels show the durations of the IOIs plotted as a function of time (in days) for birds zf_yl11 (A), zf_yl47 (B), and zf_bl117 (C). Each dot corresponds to one IOI. Note there are one or two clusters of points in the IOI distributions prior to the onset of DAF. These clusters are maintained while additional ones appear two or more days after the onset of DAF. The right panels show data for the post-DAF period plotted as a function of the number of events (number of IOIs). The red lines correspond to boundaries between days. The data of the first 7 days of the right panels correspond to the data for Days 0–7 of the left panels.

Figure 5. De-crystallization and recovery of syllable sequence for bird zf_yl11.

The mean ±SD for each day is plotted. (A) Distribution of IOI durations. The data for the first nine days are identical to those in Figure 4. (B) Percentages of the detected ("target") syllable in a song bout as a function of the days. Note that the percentage starts to rise above baseline recordings on the sixth day of DAF, the same day abnormal syllables first appear in (A). (C) The tempo of a song bout. The tempo was defined as the number of syllables divided by the duration of a song bout (number of syllables/second). The change in tempo mirrors the change in the frequency of occurrence (B) of the target syllable. The reduction in tempo results from syllable D being of longer than average duration for the syllables of that song. (D) The number of syllables in each song bout.

Figure 6. Change in mean frequencies of one syllable in each of three birds as induced by frequency–shifted auditory feedback.

The three panels in the left column correspond to each of three birds. For each panel, each dot is calculated from a single rendition of the song syllable whose exemplar spectrogram is shown at right. Black dots indicate syllables that were sung with normal (unaltered) feedback. The red dots indicate the means of the mean frequencies from all syllables for each day. The right panel shows exemplar spectrograms of the song syllables prior to any FAF manipulations (baseline) and the indicated number of days after the start of FAF experiments. The mean frequencies are depicted by the yellow lines.