Monaural Congenital Deafness Affects Aural Dominance and Degrades Binaural Processing

Abstract

Cortical development extensively depends on sensory experience. Effects of congenital monaural and binaural deafness on cortical aural dominance and representation of binaural cues were investigated in the present study. We used an animal model that precisely mimics the clinical scenario of unilateral cochlear implantation in an individual with single-sided congenital deafness. Multiunit responses in cortical field A1 to cochlear implant stimulation were studied in normal-hearing cats, bilaterally congenitally deaf cats (CDCs), and unilaterally deaf cats (uCDCs). Binaural deafness reduced cortical responsiveness and decreased response thresholds and dynamic range. In contrast to CDCs, in uCDCs, cortical responsiveness was not reduced, but hemispheric-specific reorganization of aural dominance and binaural interactions were observed. Deafness led to a substantial drop in binaural facilitation in CDCs and uCDCs, demonstrating the inevitable role of experience for a binaural benefit. Sensitivity to interaural time differences was more reduced in uCDCs than in CDCs, particularly at the hemisphere ipsilateral to the hearing ear. Compared with binaural deafness, unilateral hearing prevented nonspecific reduction in cortical responsiveness, but extensively reorganized aural dominance and binaural responses. The deaf ear remained coupled with the cortex in uCDCs, demonstrating a significant difference to deprivation amblyopia in the visual system.

Keywords: asymmetric hearing; auditory development; binaural cochlear implants; interaural time difference; sensory deprivation.

Figure 1.

(A) Schematic illustration of stimulation with bilateral cochlear implants. Stimulus: 3 biphasic charge-balanced pulses delivered to each ear at 6 dB above eABR threshold, 200 µs/phase, 500 Hz repetition rate. Recording in the primary auditory cortex, field A1 (yellow area). The terms “crossed” and “uncrossed” indicate the side of stimulated cochlea with respect to the recorded cortical hemisphere: crossed = stimulated cochlea contralateral to the recording side (dark arrow), uncrossed = stimulated cochlea and recorded cortex at the same side (light arrow). (B) Scheme illustrating the recording conditions in animals with unilateral congenital deafness (uCDCx), corresponding to the condition of SSD. Responses collected from the hemisphere of the same side as the hearing ear (ipsilateral) are designated uCDC_i (red arrow); those contralateral to the hearing ear are designated uCDC_c (blue arrow). (C) Animals investigated in the present study: HC: acutely deafened hearing controls; CDC: bilaterally congenitally deaf cats; uCDC_i, uCDC_c: unilaterally congenitally deaf cats recorded ipsilateral or contralateral to the hearing ear.

Figure 2.

Spontaneous and evoked firing rate analysis. (A) Raster plots of cortical responses to 30 repetitions of crossed (gray boxes), uncrossed (white boxes), and bilateral stimulation (light yellow boxes). Each dot represents an action potential. Responses were stronger for crossed than uncrossed stimulation in all conditions except uCDC_i (unilateral animals, hemisphere ipsilateral to the hearing ear) where a stronger uncrossed response was observed. (B) Spontaneous firing rate computed from all recording sites in binaurally normal-hearing and deaf animals (empty boxes) and unilateral deaf animals (filled boxes). The boxes cover the second and third quartiles of the distribution; the intersection line inside the box shows the median and the whiskers the range of the data. The drawings adjacent to the box plots illustrate the relation between recording hemisphere and the cochlea in deaf animals (crossed). Spontaneous firing rate was reduced in binaurally deaf cats and in the ipsilateral cortex of unilateral animals (uCDC_i). No difference between hearing control and contralateral cortex of unilateral animal was observed (uCDC_c). (C) Box plots of evoked firing rates for all groups and stimulus conditions. The stimulus, recording sides, and groups are depicted below the box plots. Firing rates were analyzed within a response window of 50 ms and calculated for 1 ms. Evoked firing rates for all stimulus conditions were lowest in CDCs, while highest rates were found in the contralateral cortex of the unilateral animal (uCDC_c) with crossed stimulation. In the ipsilateral cortex of the unilateral animal (uCDC_i), both uncrossed and binaural stimulation evoked the highest firing rates of all groups. Two-tailed Wilcoxon–Mann–Whitney test, *P < 0.05; **P < 0.01; ***P < 0.001.

Figure 3.

Basic unit response properties. (A) Rate-level functions for all groups and stimulus conditions (red = crossed, green = uncrossed, and blue = binaural stimulation). Broken lines indicate the sigmoid function fitted to the response curve. For each group, 3 examples of rate-level functions are shown to demonstrate the variability of responses. (B) Quantitative analysis of threshold (first row), saturation (second row), and DR (lower row) calculated from fitted rate-level functions for all groups and stimulus conditions (same scheme as in Fig. 2C). CDCs show the lowest stimulation thresholds and smallest DRs among all groups and for all stimulus conditions (two-tailed Wilcoxon–Mann–Whitney test *P < 0.05, **P < 0.01, ***P < 0.001).

Figure 4.

Monaural response classification. (A) Classification of monaural responses [based on Zhang et al. (2004)]. Depending on the response to crossed and uncrossed stimulation units, these are classified into EE (responding to the stimulation of crossed and uncrossed ear), E0 (responding only to the stimulation of the crossed ear), and 0E (responding only to the stimulation of the uncrossed ear). Units responding solely to binaural stimulation are designated PB. Testing with binaural stimuli was performed at ITD = 0 µs and ILD = 0 dB. (B) Statistical analysis of the distribution within the response classes. Most differences were found for EE and E0 responses. In the ipsilateral cortex of unilateral animals (uCDC_i), the highest number of EE responses was found, while the same group showed the lowest number of E0 responses. Two-tailed Wilcoxon–Mann–Whitney test, *P < 0.05; **P < 0.01; ***P < 0.001. (C) Histograms of ADI of multiunit responses in all studied groups 6 dB above EABR thresholds. Means of the population are marked by an arrow, and mean values are given above arrows. In hearing controls (blue color), the index was predominantly positive, demonstrating stronger responses in crossed ear stimulation. In CDCs (red color), the distribution is similar but with smaller mean. In uCDC_i (orange color, filled), a prominent shift in favor of the uncrossed ear (negative values) is observed. Again, a hemispheric specificity shows up, with crossed ear preference in uCDC_c (light blue color, filled). ADI = −1 corresponds to the ocular dominance score 7 in the visual system and ADI = 1 to the ocular dominance score of 1. For details on statistics, see text.

Figure 5.

Binaural response classification. (A) Classification of responses based on the relation between monaural and binaural responses [F = facilitation; N = neutral interaction; O = occlusion; S = suppression, after Zhang et al. (2004)]. Testing was performed at ITD = 0 µs and ILD = 0 dB. (B) Examples of rate-level functions for facilitatory, neutral occlusive, and suppression interactions (for description of rate-level functions, see Fig. 3A). (C) Distribution and statistics of binaural interaction classes for all animal groups. A significant reduction of facilitatory interactions was found for CDCs and both unilateral groups compared with HCs. The highest number of occlusions was found in the ipsilateral cortex of uCDCs, while the contralateral cortex showed the highest number of suppressions. Two-tailed Wilcoxon–Mann–Whitney test,*P < 0.05; **P < 0.01.

Figure 6.

ITD sensitivity (stimuli presented at interaural level difference of 0 dB). (A) Firing rate (color) as a function of peristimulus time (abscissa) and ITD (ordinate) of 4 typical units showing sensitivity to ITDs (one example per animal group). The lower panels show the number of spikes per stimulus as a function of ITD evaluated from the corresponding color plot. The line fitted along the original data points represents the ITD function showing changes in responsiveness with respect to ITD. (B) Statistical evaluation of ITD sensitivity, presented for all animal groups. Classified units (left) represent those units that systematically changed the firing rate with ITD, thus representing the true ITD-sensitive units (cf. Tillein et al. 2010). The majority of such units were observed in normal-hearing animals (HCs) and in the contralateral hemisphere of the unilateral animals (uCDC_c), with only a few in the hemisphere ipsilateral to the hearing ear (uCDC_i), and in the binaurally deaf animals (CDC). Correspondingly, nonclassified units and flat units (middle, responding with similar firing rates to different ITDs) were more frequent in the hemisphere ipsilateral to the hearing ear (uCDC_i). Units nonresponsive to stimulation (right) were most frequently found in binaurally deaf cats (CDCs), while they were very rare in the ipsilateral cortex of unilateral animals (uCDC_i). (C) Comparison of the properties of classified units in all animals and conditions. Analyzed ITD parameters are indicated in the inset. Both ITD_best and ITD_center showed larger spread over the tested ITD range in uCDCs, but no significant differences were found between groups and conditions (left and middle). MDs of ITD function (right), quantifying ITD sensitivity in the classified units, were lowest in the ipsilateral cortex of the unilateral animals. Two-tailed Wilcoxon–Mann–Whitney test, *P < 0.05, **P < 0.01, ***P < 0.001.