Transformation of temporal properties between auditory midbrain and cortex in the awake Mongolian gerbil

Abstract

The neural representation of meaningful stimulus features is thought to rely on precise discharge characteristics of the auditory cortex. Precisely timed onset spikes putatively carry the majority of stimulus-related information in auditory cortical neurons but make a small contribution to stimulus representation in the auditory midbrain. Because these conclusions derive primarily from anesthetized preparations, we reexamined temporal coding properties of single neurons in the awake gerbil inferior colliculus (IC) and compared them with primary auditory cortex (AI). Surprisingly, AI neurons displayed a reduction of temporal precision compared with those in the IC. Furthermore, this hierarchical transition from high to low temporal fidelity was observed for both static and dynamic stimuli. Because most of the data that support temporal precision were obtained under anesthesia, we also reexamined response properties of IC and AI neurons under these conditions. Our results show that anesthesia has profound effects on the trial-to-trial variability and reliability of discharge and significantly improves the temporal precision of AI neurons to both tones and amplitude-modulated stimuli. In contrast, IC temporal properties are only mildly affected by anesthesia. These results underscore the pitfalls of using anesthetized preparations to study temporal coding. Our findings in awake animals reveal that AI neurons combine faster adaptation kinetics and a longer temporal window than evident in IC to represent ongoing acoustic stimuli.

Figure 1.

Location and tuning characteristics of recording sites. A, Dark-field image of a coronal section through the left AI showing an electrode track in which a fluorescein injection was made. Dorsal is toward the top and lateral is to the left. B, Sagittal section through IC showing an electrode track terminating in a lesion site. Both sections are counterstained with cresyl violet. C, D, Histograms of BF of all recorded units in AI and IC. E, Electrode insertion depths for recorded units in anesthetized and awake AI. Horizontal lines indicate population medians.

Figure 2.

First-spike timing is less precise in AI than in IC. A, B, Rasters of responses of an example awake AI (A) and awake IC (B) cell to a 200 ms BF tone. Windowed portions indicate the ROI for latency analysis, shown expanded on the right. The first spike in the ROI in each trial is shown in blue. C, Population plot of SD of the minimum latency in response to BF tone pips in AI and IC.

Figure 3.

AI first-spike latency and latency variability are reduced by anesthesia. A, Response of an example anesthetized AI cell to a 200 ms BF tone; conventions as in Figure 2. B, Population plot of minimum first-spike latency and SD of the minimum latency in response to BF tone pips in anesthetized and awake AI. C, Histogram of SD of the latency in anesthetized and awake AI. Filled bars indicate anesthetized AI, and open bars indicate awake AI. Only values up to 4 ms are shown to highlight the difference between the populations.

Figure 4.

IC latency variability is unaffected by anesthesia. A, Response of an example anesthetized IC cell to a 200 ms BF tone. B, Population plot of minimum first-spike latency and SD of the minimum latency in response to BF tone pips in anesthetized and awake IC. C, Histogram of SD of the latency in anesthetized and awake IC. Conventions as in Figure 3.

Figure 5.

AI tone responses are more reliable in awake animals. A, B, Rasters of the first 100 ms of the responses of an example anesthetized (A) and awake (B) AI cell to a 200 ms BF tone. Windowed portions indicate the 20 ms ROI for determining the number of missed trials. C, Histogram of the proportion of missed trials in anesthetized and awake AI cells. Filled bars indicate anesthetized AI, and open bars indicate awake AI. D, Population plot of average firing rate for a 200 ms BF tone in anesthetized and awake AI. Horizontal lines indicate population medians.

Figure 6.

Temporal response profile to long constant stimuli in AI and IC. A, B, PSTH of the response of an example awake AI (A) and awake IC (B) cell to 10 trials of a 2 s BF tone. C, Response adaptation profiles in response to a 2 s BF tone for a typical cell in AI (gray lines) and IC (black lines), obtained from the population median parameters of an exponential decay curve fit to the PSTH of each cell. The curve begins at 50 ms to match the corresponding PSTH. Solid lines denote awake populations, and dashed lines denote anesthetized populations. Inset, Plateau firing rates for an example awake AI cell for four different types of continuous stimuli, from exponential decay curve fits.

Figure 7.

Temporal representation of envelope modulations in AI and IC. A, Period histograms of responses of four example cells, one from each study group, to six SAM frequencies. Normalization was performed separately for AI and IC. B, C, tMTFs of three representative awake AI (B) and IC (C) cells. A vertical line has been added to each graph at 20 Hz to facilitate comparison. D, Percentage of cells in AI (gray lines) and IC (black lines) showing significant synchrony (Rayleigh test, p < 0.001) to the period of SAM as a function of the modulation frequency. Solid lines denote awake and dashed lines denote anesthetized populations.

Figure 8.

SAM tMTF cutoff is correlated with minimum latency and depends on stimulus duration. A, Individual cells in awake IC (filled squares) and AI (open circles). The sample is a subset of the full data because it was not always possible to obtain a reliable measure of minimum latency and SAM cutoff frequency in the same cell. B, Synchrony cutoff in 14 awake IC cells as assessed with 10 s and 400 ms SAM tones.

Figure 9.

Discharge precision to the SAM envelope in AI and IC. Pooled period histograms of the responses of all tested AI (A) and IC (B) neurons to the period of a 10-s-long 2 Hz SAM tone. The stimulus envelope is indicated at the top. Awake data are represented by shaded bars, and anesthetized data are represented by semitransparent white bars, which are superimposed. Histograms were generated by adding the period histograms of individual cells in each population and normalizing. Values along the abscissa correspond to modulation phase, in which one 500 ms period equals 360°.