Neural coding of interaural time differences with bilateral cochlear implants: effects of congenital deafness

Abstract

Human bilateral cochlear implant users do poorly on tasks involving interaural time differences (ITD), a cue that provides important benefits to the normal hearing, especially in challenging acoustic environments, yet the precision of neural ITD coding in acutely deafened, bilaterally implanted cats is essentially normal (Smith and Delgutte, 2007a). One explanation for this discrepancy is that the extended periods of binaural deprivation typically experienced by cochlear implant users degrades neural ITD sensitivity, by either impeding normal maturation of the neural circuitry or altering it later in life. To test this hypothesis, we recorded from single units in inferior colliculus of two groups of bilaterally implanted, anesthetized cats that contrast maximally in binaural experience: acutely deafened cats, which had normal binaural hearing until experimentation, and congenitally deaf white cats, which received no auditory inputs until the experiment. Rate responses of only half as many neurons showed significant ITD sensitivity to low-rate pulse trains in congenitally deaf cats compared with acutely deafened cats. For neurons that were ITD sensitive, ITD tuning was broader and best ITDs were more variable in congenitally deaf cats, leading to poorer ITD coding within the naturally occurring range. A signal detection model constrained by the observed physiology supports the idea that the degraded neural ITD coding resulting from deprivation of binaural experience contributes to poor ITD discrimination by human implantees.

Figure 1.

The BIC of ABR is reduced in congenitally deaf cats. A, B, Example BIC waveforms from one acutely deafened cat (A) and one congenitally deaf cat (B). Each trace corresponds to a different stimulus level. BIC amplitude was measured between the notch and the following peak (arrows). C, BIC amplitudes as a function of stimulus level in congenitally deaf and acutely deafened cats. Gray shading shows the range of BIC amplitudes measured in acutely deafened cats by Smith and Delgutte (2007b). D, Monaural wave 4 amplitudes are also smaller in congenitally deaf cats. Amplitudes shown are average of responses to stimulation of each ear alone. E, BIC latencies are similar between congenitally deaf and acutely deafened cats, with the exception of one cat. F, Monaural wave 4 latencies tend to be shorter in congenitally deaf cats. Values shown are averages for stimulation of each ear alone. In B–F, stimulus levels are expressed relative to the monaural ABR thresholds, defined as the stimulus amplitude required to evoke 1 μV wave 4. Monaural wave 4 amplitudes were always equalized during binaural stimulation by application of an appropriate ILD.

Figure 2.

ITD tuning of two example neurons illustrating typical differences between acutely deafened (top row) and congenitally deaf (bottom row) cats. A, C, Temporal discharge patterns (dot rasters) as a function of ITD. Alternating colors indicate blocks of stimulus trials at different ITDs. Stimulus pulse train (20 pps) shown at the top. B, D, Firing rate versus ITD.

Figure 3.

ITD-sensitive neurons are less prevalent in congenitally deaf cats. A, Distributions of ITD SNR for the samples of IC neurons in the two groups of animals. B, Scatter plot of ITD SNR versus recording depth from dorsal surface of IC. Crosses, Acutely deafened cats; circles, congenitally deaf cats.

Figure 4.

Examples of three types of temporal discharge patterns evoked by pulse-train stimulation in deaf animals. Period histograms plot spike times relative to the onset of each stimulus pulse with 0.5 ms resolution. A, Precisely timed early response. B, Poorly timed late responses presumably reflect suppression of spontaneous activity. C, Combination of early and late responses. Black lines, Automatic classification of period histogram shape based on sum-of-Gaussians fit.

Figure 5.

Late responses are more prevalent in congenitally deaf cats and are associated with poor ITD sensitivity. A, Distributions of period histogram shapes compared between acutely deafened and congenitally deaf cats. B, Comparison of median ITD SNR between groups of cats and across shape categories.

Figure 6.

Effect of congenital deafness on spontaneous rate and spike timing. A–C, Histograms comparing the distributions of mean spike latency (A), latency jitter (B), and spontaneous discharge rates (C) between acutely deafened and congenitally deaf cats. Latencies and jitter are shown for early responses only. D–F, Scatter plots of ITD SNR against mean spike latency (D), latency jitter (E), and spontaneous rate (F) for the two samples of IC neurons.

Figure 7.

Shapes of rate–ITD curves do not differ between acutely deafened and congenitally deaf cats. Histograms show incidence of rate–ITD curve shapes based on the four templates (top) of Smith and Delgutte (2007). Analysis limited to IC neurons with statistically significant ITD SNRs.

Figure 8.

Congenital deafness alters ITD tuning metrics. Analysis applied to rate–ITD curves containing a peak. A, Illustration of metrics derived from Gaussian fits to rate–ITD curves. Best ITD, ITD of the peak response; Halfwidth, width of rate–ITD curve at 50% of maximum rate. ITD_ms, ITD for which the slope of rate-ITD curve is maximal. B, Best ITD distribution is broader and lacks contralateral bias in congenitally deaf cats. C, Rate–ITD curves are broader in congenitally deaf cats. D, ITD_MS distribution is not concentrated in naturally occurring range of ITD in congenitally deaf cats. B, D, Dashed lines, approximate naturally occurring ITD range in cat.

Figure 9.

Best ITD increases with width of ITD tuning in both normal-hearing and bilaterally implanted cats. Left column, Data from normal-hearing cats (Hancock and Delgutte, 2004; Devore et al., 2009); right column, data from acutely deafened, bilaterally implanted cats (Smith and Delgutte, 2007a; present study). A, Best ITD decreases with increasing BF. Colored squares show mean values for each quintile of BFs. B, Best ITD increases with half-width of ITD tuning. C, Parallel trend holds in acutely deafened, implanted cats. D, E, Average rate–ITD curves for each BF or half-width quintiles in B and C. F, G, ITD_MS is more nearly independent of half-width than is best ITD.

Figure 10.

Physiologically based model of psychophysical ITD discrimination with bilateral CI. A, Grid of model neurons. Each model neuron has a Gaussian-shaped rate–ITD curve. Half-width varies in one dimension, ITD_MS in the other. Rates are summed across half-widths before computing D values, and then the D values are combined optimally across ITD_MS. B, ITD JND versus reference ITD for two bilateral implant subjects (gray line) and various model configurations.