Developmental experience alters information coding in auditory midbrain and forebrain neurons

Abstract

In songbirds, species identity and developmental experience shape vocal behavior and behavioral responses to vocalizations. The interaction of species identity and developmental experience may also shape the coding properties of sensory neurons. We tested whether responses of auditory midbrain and forebrain neurons to songs differed between species and between groups of conspecific birds with different developmental exposure to song. We also compared responses of individual neurons to conspecific and heterospecific songs. Zebra and Bengalese finches that were raised and tutored by conspecific birds, and zebra finches that were cross-tutored by Bengalese finches were studied. Single-unit responses to zebra and Bengalese finch songs were recorded and analyzed by calculating mutual information (MI), response reliability, mean spike rate, fluctuations in time-varying spike rate, distributions of time-varying spike rates, and neural discrimination of individual songs. MI quantifies a response's capacity to encode information about a stimulus. In midbrain and forebrain neurons, MI was significantly higher in normal zebra finch neurons than in Bengalese finch and cross-tutored zebra finch neurons, but not between Bengalese finch and cross-tutored zebra finch neurons. Information rate differences were largely due to spike rate differences. MI did not differ between responses to conspecific and heterospecific songs. Therefore, neurons from normal zebra finches encoded more information about songs than did neurons from other birds, but conspecific and heterospecific songs were encoded equally. Neural discrimination of songs and MI were highly correlated. Results demonstrate that developmental exposure to vocalizations shapes the information coding properties of songbird auditory neurons.

Figure 1

Spectrograms show the acoustic features of zebra finch, Bengalese finch and cross-tutored zebra finch songs. Cross-tutored zebra finches copied the song syllables of their tutors’ songs but produced songs with some zebra finch-like temporal patterns. Color indicates sound intensity. Red is high and blue is low. Tutor songs are on the left and the learned songs of the tutees are on the right.

Figure 2

Zebra and Bengalese finch songs differ in spectral and temporal acoustics. A. Spectrograms of zebra (left) and Bengalese (right) finch songs. B. Frequency power spectra of zebra and Bengalese finch songs. C. Modulation spectra of zebra and Bengalese finch songs show the spectrotemporal modulations that characterize the songs of each species. Color indicates power. Red is high and blue is low. Contour lines on the color plots outline 80% of the total power for each spectrum.

Figure 3

Responses of midbrain (MLd) neurons to song. A. Responses of one normal zebra finch neuron (left) and one Bengalese finch neuron (right) to a Bengalese finch song. The top row shows the song spectrogram. The middle row shows the spike rasters obtained for 10 trials. The bottom row shows the poststimulus time histograms of the responses. B. Power spectra of the time-varying spike rates for each neuron show that, despite similar mean spike rates, the responses of the zebra finch neuron (left) cover a wider bandwidth than do the responses of the Bengalese finch neuron (right). The power spectra include responses to all of the 20 Bengalese finch songs.

Figure 4

Responses of forebrain (field L) neurons to song. A. Responses of one normal zebra finch neuron (left) and one cross-tutored zebra finch neuron (right) to a zebra finch song. The top row shows the song spectrogram. The middle row shows the spike rasters obtained for 10 trials. The bottom row shows the poststimulus time histograms of the responses. B. The distributions of time-varying spike rates for each neuron show that the responses of the normal zebra finch neuron (left) were distributed across rates with a shape that was closer to that of an exponential distribution than were the responses of the cross-tutored zebra finch neuron (right). The distributions were obtained from the responses to all 20 zebra finch songs. Because the mean spike rate was different between the two neurons, the distributions were rescaled to a mean of 10 spikes/s. The distribution for the normal zebra finch neuron was fit with a gamma order of 1.17. The distribution for the cross-tutored zebra finch neuron was better fit with a gamma order of 2.31. The cross-tutored distribution has smaller variance and smaller entropy.

Figure 5

Mutual information values differ for neurons from normal and cross-tutored birds within species and between species. Average mutual information values for responses to songs are shown for neurons from normal zebra finches (ZF), cross-tutored zebra finches (xZF) and normal Bengalese finches (BF). Values for responses to zebra finch song are on the left. Values for responses to Bengalese finch song are on the right. Error bars are one SD, ** is p < 0.01, and *** is p < 0.001. Correlation plots (right) show that information values for responses to zebra finch song and Bengalese finch song are highly correlated, within a neuron. Each point represents the average information rate in responses to 20 zebra finch songs on the x axis and the average information rate in responses to 20 Bengalese finch songs on the y axis, for a single neuron. A. Midbrain (MLd). B. Primary forebrain (field L).

Figure 6

Mean firing rate and response bandwidth differ significantly between zebra finch groups with different developmental experience and between species, in midbrain neurons. Reliability and rate distribution do not differ across groups. Average values for the four response properties are shown for neurons from normal zebra finches (ZF), cross-tutored zebra finches (xZF) and normal Bengalese finches (BF). Values for responses to zebra finch song are on the left. Values for responses to Bengalese finch song are on the right. Error bars are one SD, ** is p < 0.01 and *** is p < 0.001.

Figure 7

Mean firing rate and spike rate distribution differ significantly between zebra finch groups with different developmental experience and between species, in primary forebrain neurons. Reliability and bandwidth do not differ across groups. Average values for the four response properties are shown for neurons from normal zebra finches (ZF), cross-tutored/tutored zebra finches (xZF) and normal Bengalese finches. Values for responses to zebra finch song are on the left. Values for responses to Bengalese finch song are on the right. Error bars are one SD, ** is p < 0.01 and *** is p < 0.001.

Figure 8

Percent correct neural discrimination among songs differs between zebra finch groups with different developmental experience and between species in midbrain neurons, and with experience but not between species in forebrain neurons (upper). Percent correct values are more variable among forebrain neurons than among midbrain neurons. Information values and % correct are highly correlated within a neuron (lower). A. Midbrain (MLd). B. Forebrain (field L). Error bars are one SD. * is p < 0.05, ** is p < 0.01 and *** is p < 0.001.