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. 2011 Jul 6;31(27):9958-70.
doi: 10.1523/JNEUROSCI.4509-10.2011.

Impaired Auditory Temporal Selectivity in the Inferior Colliculus of Aged Mongolian Gerbils

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Impaired Auditory Temporal Selectivity in the Inferior Colliculus of Aged Mongolian Gerbils

Leila Khouri et al. J Neurosci. .
Free PMC article

Abstract

Aged humans show severe difficulties in temporal auditory processing tasks (e.g., speech recognition in noise, low-frequency sound localization, gap detection). A degradation of auditory function with age is also evident in experimental animals. To investigate age-related changes in temporal processing, we compared extracellular responses to temporally variable pulse trains and human speech in the inferior colliculus of young adult (3 month) and aged (3 years) Mongolian gerbils. We observed a significant decrease of selectivity to the pulse trains in neuronal responses from aged animals. This decrease in selectivity led, on the population level, to an increase in signal correlations and therefore a decrease in heterogeneity of temporal receptive fields and a decreased efficiency in encoding of speech signals. A decrease in selectivity to temporal modulations is consistent with a downregulation of the inhibitory transmitter system in aged animals. These alterations in temporal processing could underlie declines in the aging auditory system, which are unrelated to peripheral hearing loss. These declines cannot be compensated by traditional hearing aids (that rely on amplification of sound) but may rather require pharmacological treatment.

Figures

Figure 1.
Figure 1.
Pulse matrix. A, Schematic of a pulse train consisting of two trapezoid pulses with 1 ms rise and fall times each. Pulse duration is defined as the entire duration of the pulse including rise and fall time; pause duration is defined as the entire silent interval between pulses. B, Pulse matrix. The pulse matrix consists of 49 trains of trapezoid broadband noise pulses. Pulse and pause duration span from 2 to 128 ms in logarithmic intervals. Pulse trains are 512–640 ms long.
Figure 2.
Figure 2.
Types of neuronal response patterns evoked by broadband noise. A–F show PSTHs (bin width, 5 ms) of selected neurons from six temporal response types in response to 250 ms broadband noise pulses. Gray shaded areas indicate the duration of the stimulus. All neurons were recorded from aged animals. A, Onset (on) neuron, discharging during the first 50 ms of stimulus presentation. B, Spontaneously (spont.) active primary-like neuron (plb), responding ≥30% stronger during stimulus onset (first 50 ms) than during the later portion of the stimulus. Note that this neuron (in contrast to the neuron presented in D) does not show a dip in discharge after stimulus offset (arrows in B and D). This behavior was exclusively observed for aged neurons. C, Sustained neuron (sus). This type of neuron showed a sustained discharge pattern during the entire sound presentation. D, Spontaneously active primary-like neuron (plb), which discharged with a primary-like pattern during sound presentation, paused, and recovered spontaneous activity during the silent interval between noise burst presentations. E, Late sustained/build-up neuron (lsus). This type of neuron exhibited a build-up or a sustained discharged pattern after a latency of ≥50 ms. F, Offset/inhibitory neuron (off); neurons from this class either suppressed discharge below spontaneous activity during stimulus presentation or exclusively discharged after stimulus presentation. G, Absolute time of first action potential after stimulus offset (mean ± SD over repetitions) versus rate of discharge between stimuli for spontaneously active neurons. Response types of neurons are coded in colors: onset (on), primary-like (plb), sustained (sub), late sustained (lsus), offset (off), and sparse (spa) cells that showed spontaneous activity. Whereas in young adult animals, only offset neurons strongly discharged within 150 ms after stimulus offset, in aged animals, primary-like and offset neurons strongly discharged within 150 ms in aged animals (gray shaded areas).
Figure 3.
Figure 3.
Single-neuron responses to pulse matrix. A, Raster plot of an offset neuron from a young adult animal. This neuron responded preferentially to pulse trains of short pulse and long pause durations; it was not driven by stimuli of short pulse and short pause duration. Stimuli that suppressed response are indicated by arrows. B, Raster plot of an offset neuron (off) from an aged animal. This neuron responded preferentially to pulse trains of short pulse and long pause durations, but it was also driven by stimuli of short pulse and pause durations. Discharge of this neuron was not suppressed by any stimulus in our set. C, 3-D rate function (PM receptive field) of the offset neuron presented in A (young adult). Each square in the surface plot represents the average rate over nine repetitions of the pulse train. Discharge rate is color coded (black, no discharge; dark red, maximum discharge). TSI in the right top corner gives the difference between maximum and minimum discharge rate divided by the maximum discharge rate of the neuron in response to the pulse matrix. D, PM receptive field for the offset neuron presented in B (aged). E, PM receptive field for a sustained spontaneous (sub) neuron from a young adult animal. F, PM receptive field for a sustained spontaneous (sub) neuron from an aged animal. Note that discharges of young adult neurons presented in this figure were completely suppressed by a subset of pulse trains from the pulse matrix (TSI = 1), but the discharges of aged neurons were never completely suppressed (TSI = 0.55 and TSI = 0.88).
Figure 4.
Figure 4.
Decrease in temporal selectivity in aged animals. A, Distribution of TSIs of neurons from young adult (white) and aged (gray) animals. TSI is the difference between maximum and minimum discharge rate divided by the maximum discharge rate of each neuron in response to the pulse matrix. More neurons from young adult animals did not respond to a subset of pulse trains (TSI = 1), and more neurons from aged animals responded with >6% (TSI < 0.94) of their maximum discharge rate to every pulse train from the pulse matrix. B, Box plot of selectivity indices. Temporal selectivity was significantly lower for aged neurons (Wilcoxon's rank sum test, ***p = 8 × 10−4).
Figure 5.
Figure 5.
Suppressive effect of pulse trains on neurons from young adult and aged animals. A, Probability of each pulse train from the pulse matrix to suppress neurons from young adult animals. Each square in the surface plot depicts the percentage of cells the pulse train of the indicated pulse and pause duration was suppressive to. Percentage is color coded. Discharges of neurons from young adult animals were mostly suppressed by pulse trains of short pulse and short pause durations. B, Probability of each pulse train from the pulse matrix to suppress neurons from aged animals. Similar to young adult animals, discharges of neurons from aged animals were most effectively suppressed by pulse trains of short pulse and short pause durations C, Difference between probability distributions of pulse trains suppressing neurons from young adult and from aged animals, respectively. Pulse trains of long pulse durations independent of pause duration and pulse trains of short pulse and pause duration were more likely to suppress discharges in young adult animals than in aged animals. Pulse trains of short pulse duration and long pause duration were more likely to suppress discharges in aged animals (Wilcoxon's rank sum test, p = 0.04).
Figure 6.
Figure 6.
Decreased dynamic range of discharge to pulse matrix in aged neurons with low selectivity indices. A, Maximum (top) and minimum (bottom) discharge rates in response to PM in relation to the TSI. Maximum and minimum discharge rates in response to PM increased with decreasing TSI for neurons from young adult animals (maximum, r = −0.5, p = 5 × 10−7; minimum, r = −0.9, p = 1.8 × 10−29), but maximum discharge rate remained constant and minimum discharge rate increased with decreasing TSI in aged animals (maximum, r = 0.05, p = 0.6; minimum, r = −0.8, p = 1 × 10−22). B, Absolute dynamic range of discharge rate in response to PM for neurons from young adult (white) and neurons from aged (gray) animals. Neurons with low TSI from aged animals showed smaller dynamic ranges than neurons with low TSI from young adult animals (correlation between TSI and absolute dynamic range for young adult animals, r = −0.43, p = 2 × 10−5; for aged animals, r = 0.03, p = 0.7).
Figure 7.
Figure 7.
Increased width of PM receptive fields in aged animals. Neurons were grouped according to neuronal response type. Surface plots of 2-D histograms summarize numbers of neurons of each response type that responded with a rate >10% of their maximum discharge to the indicated pulse trains. The top shows neurons from young adult, and the bottom shows neurons from aged animals. Dark blue signifies that the corresponding pulse train was very unlikely to elicit a response >10% of maximum discharge and dark red that the corresponding pulse train elicited a response >10% of maximum discharge in all neurons tested. Note that dark red areas are particularly large for primary-like spontaneous (plb), sustained spontaneous (sub), and offset neurons from aged animals. Over all neurons recorded, the number of pulse trains per neuron that elicit a discharge rate >10% of the maximum discharge rate was significantly higher in aged animals (Wilcoxon's rank sum test, p = 0.04). spa, Sparse; on, onset; sus, sustained; pl, primary-like spontaneous; sub, sustained spontaneous; plb, primary-like spontaneous; lsus, late sustained/build-up; off, offset/inhibitory.
Figure 8.
Figure 8.
Strong duty cycle preference in PM receptive fields of sustained neurons from aged animals. A, Variance in PM receptive fields of sustained neurons from young adult and aged animals explained by PCs. PCs were computed from PM receptive fields of young adult and aged animals separately. For sustained neurons from young adult animals, 50% of the variance is explained by the first, 30% by the second, and ∼10% by the third PC. In contrast, in the aged population, 90% of the variance is explained by the first and only 10% by the second PC. B, First, second, and third PC of PM receptive fields of sustained neurons from young adult and aged animals. In all the 3-D plots, dark red depicts strong responses and dark blue weak responses. Distributions of weights for principal components of individual PM receptive fields are shown in the right. Weights for the second PC tend to more positive values for young adult than for aged animals (not significant). Weights for the third PC tend to cluster around 0 for aged but are spread to positive and negative values for young adult animals (Ansari-Bradley test, p = 0.02). C, Mean PM receptive fields of neurons from young adult and aged animals. Neurons were clustered based on their representation in three-dimensional principal component space (weights). Note that cluster 2 comprises neurons that showed a strong preference in discharge for short duty cycles and was mostly dominated by neurons from aged animals. Cluster 3 comprised neurons that showed a clear preference for pulse trains with short to medium pulse and pause durations. This cluster was dominated by sustained neurons from young adult animals.
Figure 9.
Figure 9.
Increase in strong positive correlations between pairs of neurons from aged animals. A, Raster plots and PM receptive fields of two example neurons from a young adult animal. Neuronal response types were late sustained (left) and offset (right). The sustained neuron was well driven by pulse trains of long pulse and short pause durations, whereas the offset neuron was hardly driven by these stimuli. Receptive fields of these two neurons were therefore of nearly opposite directions (correlation coefficient, r = −0.76). B, Probability distribution of r of all possible pairs of neurons from young adult (black) and aged (gray) animals. Significantly less pairs of neurons from aged animals show high negative correlations (Wilcoxon's rank sum test, p = 1.8 × 10−4).
Figure 10.
Figure 10.
Decrease in benefit of joined encoding of speech for pairs of neurons from aged animals. A, Smoothed PSTHs of neuronal responses to 125 ms speech snippets from one primary-like spontaneous (plb) and one sustained spontaneous (sub) neuron from a young adult animal (top 2 rows) and from an aged animal (bottom 2 rows), respectively. B, Neuronal responses to eight speech snippets were decoded based on dissimilarity of rate responses using a distance metric. Benefit of pairwise encoding was defined as the difference between classification success of every possible pair of neuron (cells1&2) and each neuron separately (cell1, cell2). Arrows indicate benefit of paired encoding. C, Probability distribution of benefit of paired encoding for neurons from young adult (black) and aged (gray) animals. Benefit of paired encoding was significantly larger for neurons from young adult than for neurons from aged animals (Wilcoxon's rank sum test, p = 7 × 10−13).

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