Effects of Bilateral Olivocochlear Lesions on Pure-Tone Intensity Discrimination in Cats

Abstract

Behavioral experiments examined the effects of olivocochlear efferent lesions on performance in an intensity discrimination task. Five cats were trained with food reinforcement to signal the detection of a change in the intensity of pure tones by releasing a response lever. Intensity cues were conveyed by 1 and 8-kHz tone bursts in quiet and in the presence of continuous broadband noise. After the collection of baseline behavioral data, the olivocochlear bundle (OCB) was sectioned with bilateral knife cuts on the floor of the IVth ventricle. The completeness of OCB lesions was evaluated at the conclusion of post-lesion behavioral testing by light microscopic examination of cochlear acetylcholinesterase staining and electrophysiological measures of contralateral noise suppression of compound action potentials (CAPs). Cats with OCB lesions showed greatest performance deficits for the discrimination of 8-kHz intensity changes in continuous background noise. The subjects' ability to discriminate 1-kHz intensity changes in noise was poor prior to OCB lesioning and did not change after the surgical procedure. Lesioning effects were not observed at either frequency when tests were conducted in quiet. These results suggest that olivocochlear feedback contributes to the auditory processing of mid-frequency acoustic signals in noisy backgrounds.

Keywords: Olivocochlear efferent lesion; acetylcholinesterase; compound action potential; intensity discrimination; noise.

FIGURE 1

Operant testing platform and restraint system.

FIGURE 2. Contingencies of reinforcement for the intensity discrimination task

The basic behavioral paradigm cycled through a flashing cue light (1), a series of standard tones (2), intensity changes that were created by alternating standard tones with louder comparison tones (3), and a food reward that was delivered to the cat’s mouth by a pneumatic spout if the lever was released in response to the presentation of an intensity change (4).

FIGURE 3. Surgical schematic showing placement of OCB lesions

(a) Surface view of the cat’s brainstem with cerebellum partially removed to reveal site of bilateral lesions (black stripes). (b) Medial and lateral olivocochlear projections to one cochlea shown in transverse view at medullar plane of section in (a). Bilateral lesions potentially transect crossed and uncrossed projections (filled triangles). IVth, fourth ventricle; VIIIth, eighth nerve; CBL, cerebellum; CN, cochlear nucleus; LOC, lateral olivocochlear system; IC, inferior colliculus; MOC medial olivocochlear system; SC, superior colliculus; SL, sulcus limitans.

FIGURE 4. Photomicrographs showing the pattern of acetylcholinesterase (AChE) labeling in the cochleas of an intact control subject

(a) Dense silver precipitate in this low magnification trans-modiolar view indicates the distribution of lateral olivocochlear terminals beneath inner hair cells in the basal turn of the left cochlea. Medial olivocochlear terminals beneath outer hair cells stain well in basal turns but AChE labeling is less intense in apical turns. Arrow points to the organ of Corti. (b) AChE labeling in this higher magnification view of a basal turn in the right cochlea of the same control animal identifies terminal zones of efferent fibers under cochlear hair cells as well as their radial course across the spiral lamina and through the tunnel of Corti. Arrow points to tunnel crossing fibers.

FIGURE 5. Acetylcholinesterase (AChE) labeling in cochleas of cats that showed behavioral deficits after OCB lesions

(a, b) Light AChE labeling was observed in basal turns of cochleae from cats 91cv3 and 91cp2. Large behavioral deficits were associated with this pattern of labeling. (c, d) Cochleae of cat 92olq1 show more intense AChE labeling than lesioned cochleae in (a) and (b), but less labeling than control cochleae in Figure 4. A smaller decrease in discrimination performance were observed after the OCB was lesioned in this animal. Measures of CAP suppression are shown for cat 92olq1 in Figure 7c.

FIGURE 6. Acetylcholinesterase (AChE) labeling in basal turns of the left cochleas from (a) cat 92olf1, a behavioral subject that did not exhibit behavioral deficits after OCB lesions and (b) cat 91kj5, a behavioral subject that received a sham lesion

Cochleas from both cats show AChE labeling beneath inner and outer hair cell although less dense staining was noted in cat 91kj5. Gross examination of brainstem tissue suggested that lesions were made too caudal in cat 92olf1. Results of electrophysiological assessment of efferent influences in this cat are shown in Figure 7b.

FIGURE 7. Click-evoked compound action potentials (CAPs) obtained in quiet (solid lines) and in contralateral noise (dashed lines)

(a) Contralateral noise suppressed the CAP in the left cochlea of an intact control subject by 70%. (b) Both cochleae of cat 92olf1 were incompletely lesioned and like the intact cat showed large reductions of CAP in contralateral noise, (c) The left cochlea of cat 92olq1 was successfully lesioned and shows only weak efferent suppression.

FIGURE 8. Pre-lesion psychometric functions for intensity discrimination of pure tones at (a) 1 kHz and (b) 8 kHz

Signal detection methods were used to derive d′ values from the percentage of hits at each intensity change and overall false-alarm rates, which are plotted at the 0-dB intensity change (squares). The resulting d′ values are shown in (c) for tests with 1-kHz tones and in (d) for tests with 8-kHz tones.

FIGURE 9. The d′ index of discriminability for pre-lesion detection of a 3-dB intensity change at 1 kHz (a) and 8 kHz (b)

Cat 92olq1 would not perform the task when tested with 1-kHz tones.

FIGURE 10. Pre-lesion intensity discrimination in six levels of background noise and in quiet for tests with 1-kHz tones (a) and 8-kHz tones (b)

Percentages of hits (solid lines) and false alarms (dashed lines) are presented for each stimulus condition. d′ values derived from the psychometric functions are shown for 1-kHz tones (c) and for 8-kHz tones (d).

FIGURE 11. d′ values for pre-lesion detection of pure-tone intensity changes in the presence of continuous broadband noise with 8-dB spectrum level

A fixed 3-dB change was conveyed by 1-kHz tones (a) and 8-kHz tones (b). All cats exhibited less sensitivity (i.e., lower d′ values) for the discrimination of low-frequency tones in noise; cat 92olq1 would not perform the task when tested under this stimulus condition.

FIGURE 12. Effects of OCB lesions on the discrimination of 3-dB intensity changes in quiet for 1-kHz tones (a) and 8-kHz tones (b)

Three cats with more complete lesions (91cv3, 91cp2 and 92olq1) showed no consistent performance deficits for the discrimination of 1-kHz tones and only slight deficits for 8-kHz tones. Cat 92olf1 was relatively unaffected by an incomplete lesion, and cat 91kj5 exhibited better discrimination of low-frequency intensity changes after receiving a sham lesion.

FIGURE 13. Effects of OCB lesions on the discrimination of pure-tone intensity changes in 8-dB spectrum level background noise

(a) All five cats showed no change or improved performance for the discrimination of a 3-dB intensity change at 1 kHz. (b) Cats with more complete lesions (91cv3, 91cp2, and 92olq1) exhibited consistent deficits in the discrimination of 8-kHz intensity changes in noise. Cats with intact olivocochlear projections (92olf1 and 91kj5) displayed no change in discrimination after the surgical procedure.