Contralateral effects and binaural interactions in dorsal cochlear nucleus

Abstract

The dorsal cochlear nucleus (DCN) receives afferent input from the auditory nerve and is thus usually thought of as a monaural nucleus, but it also receives inputs from the contralateral cochlear nucleus as well as descending projections from binaural nuclei. Evidence suggests that some of these commissural and efferent projections are excitatory, whereas others are inhibitory. The goals of this study were to investigate the nature and effects of these inputs in the DCN by measuring DCN principal cell (type IV unit) responses to a variety of contralateral monaural and binaural stimuli. As expected, the results of contralateral stimulation demonstrate a mixture of excitatory and inhibitory influences, although inhibitory effects predominate. Most type IV units are weakly, if at all, inhibited by tones but are strongly inhibited by broadband noise (BBN). The inhibition evoked by BBN is also low threshold and short latency. This inhibition is abolished and excitation is revealed when strychnine, a glycine-receptor antagonist, is applied to the DCN; application of bicuculline, a GABAA-receptor antagonist, has similar effects but does not block the onset of inhibition. Manipulations of discrete fiber bundles suggest that the inhibitory, but not excitatory, inputs to DCN principal cells enter the DCN via its output pathway, and that the short latency inhibition is carried by commissural axons. Consistent with their respective monaural effects, responses to binaural tones as a function of interaural level difference are essentially the same as responses to ipsilateral tones, whereas binaural BBN responses decrease with increasing contralateral level. In comparison to monaural responses, binaural responses to virtual space stimuli show enhanced sensitivity to the elevation of a sound source in ipsilateral space but reduced sensitivity in contralateral space. These results show that the contralateral inputs to the DCN are functionally relevant in natural listening conditions, and that one role of these inputs is to enhance DCN processing of spectral sound localization cues produced by the pinna.

Fig. 1

Contralateral monaural frequency response maps for type IV units in the dorsal cochlear nucleus (DCN). (A) A unit showing inhibition to contralateral tones (98/05/28, unit 4.01); (B) a unit showing excitation (99/03/22, unit 5.02). Stimulus-driven rates are plotted against frequency at multiple sound levels (numerical labels on right). Horizontal lines indicate average spontaneous rates (SR). Black (gray) regions identify excitatory (inhibitory) response areas. Sound levels are given in dB attenuation; actual sound pressure level (SPL) varies with the acoustic calibration, but 0 dB attn. is near 100 dB re 20 μPa for tones. Solid vertical lines indicate BFs to contralateral tones; the arrows at the top of the plots mark ipsilateral BFs.

Fig. 2

Range of responses to contralateral stimulation among DCN type IV units. Plots show discharge rate vs. level in response to tones (at the ipsilateral BF; thin lines) and broadband noise (heavy lines) presented to the contralateral ear. Sound levels are shown in dB attenuation (0 dB attn. is near 100 dB SPL re 20 μPa for tones and near 40 dB spectrum level re 20 μPa/vHz for noise). Shaded bars show the range of SR for these units. Class ii units (A) are inhibited by both tones and noise (98/09/02, unit 5.04, BF=16.5 kHz); class oi units (B) are unaffected by tones and inhibited by noise (99/07/08, unit 5.06, BF = 27.5 kHz); class ei units (C) are excited by tones but inhibited by noise (98/05/28, unit 2.02, BF = 12.2 kHz); and class ee units (D) are excited by both tones and noise (99/03/22, unit 7.03, BF = 15.4 kHz).

Fig. 3

Magnitude of contralateral effects on DCN type IV units. Comparison of each unit's maximum driven rate for noise vs. tone stimulation. The symbol used to plot each point indicates the effect that contralateral stimuli had on the unit (see legend). Data points along the center ordinate are shifted slightly to avoid overlap. The dashed line indicates equal driven rates to both stimuli. Note that most units are weakly, if at all, inhibited by tones but are inhibited strongly by contralateral noise (open and gray circles).

Fig. 4

Threshold of contralateral effects on DCN type IV units. Comparison of each unit's threshold to contralateral vs. ipsilateral tones (A) and noise (B). The symbol used to plot each point indicates the effect that contralateral stimuli had on the unit (see legend in B). Contralateral thresholds greater than 40 dB above ipsilateral thresholds to the same stimulus were rejected due to the possibility of cross talk; symbols for such units are plotted above the ordinate. Dashed lines show points of equal threshold. Note that threshold differences for noise are usually smaller than those for tones.

Fig. 5

Time course of effects of contralateral tones and noise on DCN type IV units. A, C: Plots show discharge rate vs. time for an individual class ii (A: 98/09/02, unit 5.04, BF=16.5 kHz) and class ee unit (C: 99/03/22, unit 7.03, BF = 15.4 kHz). Poststimulus time histograms (PSTHs) show effects of contralateral stimuli on the spontaneous activity of the unit; the range of SR is shown by the shaded bar. PSTHs were constructed from rate-level responses of units at stimulus levels that elicited similar, near-maximum, effects (typically, levels ≥20 dB re threshold). The duration of the stimulus is marked by the black bar below the abscissa. B, D: Scatter plots of contralateral vs. ipsilateral latencies for tones (B) and noise (D) for all units. Symbols indicate the effect of contralateral tones and noise on each unit (see legend in D). Two symbols (asterisks and filled squares) are plotted for each class ee unit in panel D to highlight the dual nature of the response (inhibition followed by excitation) to contralateral noise. Dashed lines indicate equal latency. Note that latency differences for noise are usually smaller than those for tones.

Fig. 6

Effects of strychnine and bicuculline on the rate-level function (A) and PSTH (B) of a DCN type IV unit (12/14/98, unit 1.02, BF = 16 kHz) in response to contralateral broadband noise. In both panels, responses before iontophoretic application of any agent (control condition) are shown as heavy solid lines, responses under strychnine are shown as thin solid lines, and responses under bicuculline are shown as dashed lines. Shaded bars show the range of SR for this unit before (light shading) and during (heavy shading) application of a drug; in this case, the SR changed only under bicuculline. Note that application of either strychnine or bicuculline blocks the net inhibitory response of the type IV unit to contralateral noise and reveals underlying excitation (A). Both agents show their largest affects over the initial time course of the response (B); however, only strychnine abolishes the onset of inhibition.

Fig. 7

Effects of blockade of the contralateral (left) and ipsilateral (right) acoustic striae on the responses of DCN type IV units to contralateral broadband noise. A, C: Plots show discharge rate vs. noise level functions (A) and PSTHs (C) for a type IV unit (98/09/02, unit 5.01, BF = 24 kHz) before (heavy solid lines) and 5 min after (dotted lines) pressure injection of lidocaine into the contralateral dorsal (DAS) and intermediate acoustic striae (IAS). The shaded bars show the range of SR. Note that blockade of the contralateral DAS/IAS blocks, in part, the inhibitory responses of type IV units to contralateral noise, including the onset of inhibition, and reveals underlying excitation. B, D: Noise rate-level function (B) and PSTH (D) for a type IV unit (98/10/20, unit 6.02, BF = 33.5 kHz) after the ipsilateral DAS/IAS is surgically cut. Type IV units are strictly excited by contralateral stimulation after this manipulation.

Fig. 8

Sensitivity of DCN type IV units to interaural level differences (ILDs). (A) Tone (dashed line) and noise (solid line) ILD functions for a type IV unit (99/07/08, unit 5.03, BF = 27.5 kHz). The level of the ipsilateral stimulus was held constant at 10 dB re ipsilateral threshold, whereas the contralateral level was varied from 20 dB below (+20 dB ILD condition) to 20 dB above (−20 dB ILD condition) this level. Note that changes in discharge rate are greater for increasing levels of contralateral noise than for tones. B, C: Comparisons of each unit's driven rate for tones (B) and noise (C) at an ILD of −20 dB vs. an ILD of +20 dB. Symbols indicate the effect of contralateral tones and noise on each unit (see legend). Symbols falling along the dashed line indicate units that showed no change in driven rate under the two binaural conditions. Note that the changes are larger for noise than for tones.

Fig. 9

Comparison of monaural and binaural spatial receptive fields of DCN type IV units. (A, B) Spatial receptive field for a type IV unit (04/04/07, unit 3.05, BF = 16.5 kHz) in response to ipsilateral monaural (A) and binaural virtual space (VS) stimulation (B). Cat head-related transfer functions (HRTFs) were used to synthesize monaural and binaural VS stimuli at azimuths and elevations where the gridlines intersect. The sampling rate of these stimuli was adjusted for each unit to shift in effect the BF of the unit to 12 kHz. Firing rates at each stimulus location are color-coded (bar to the right). White solid (dotted) lines enclose regions of rate that exceed 1 standard deviation above (below) the SR. Note that in response to monaural stimulation, the unit achieved its lowest discharge rates (blue) along a diagonal contour connecting low ipsilateral elevations with high contralateral elevations. The binaural response is more strongly inhibited along this contour, but also shows a loss of specificity in the contralateral field (i.e., the region of inhibition expands). (C) Median driven rates of type IV units at the 12-kHz notch elevation as a function of azimuth for monaural (green) and binaural (red) stimulation. The rates to binaural stimulation are significantly lower (P < 0.05, Friedman test) than those to monaural stimulation at all azimuths. (D) Median lower and upper edges of inhibition in the responses of type IV units to monaural (green lines) and binaural VS stimulation (red lines). The dashed line indicates the trajectory of the 12-kHz notch contour. Note that the inhibitory area widens in the contralateral hemifield (positive azimuths) under binaural stimulus conditions.

Fig. 10

Model of contralateral inputs to the DCN. Filled symbols are excitatory connections, and empty symbols are inhibitory connections. Putative glycinergic connections are heavy solid lines, and GABAergic connections are dashed lines. IV, type IV unit; T, T-stellate cell; DAS, dorsal acoustic stria; VNTB, ventral nucleus of the trapezoid body; O_c, onset-C unit; IAS, intermediate acoustic stria.