Nathaniel T. Greene

Effects of Reward and Behavioral Context on Neural Activity in the Primate Inferior Colliculus

Neural activity in the inferior colliculus (IC) likely plays an integral role in the processing of various auditory parameters, such as sound location and frequency. However, little is known about the extent to which IC neural activity may be influenced by the context in which sounds are presented. In this study, we examined neural activity of IC neurons in the rhesus monkey during an auditory task in which a sound served as a localization target for a saccade. Correct performance was rewarded, and the magnitude of the reward was varied in some experiments. Neural activity was also assessed during a task in which the monkey maintained fixation of a light while ignoring the sound, as well as when sounds were presented in the absence of any task. We report that neural activity increased late in the trial in the saccade task in 58% of neurons and that the level of activity throughout the trials could be modulated by reward magnitude for many neurons. The late-trial neural activity similarly increased in the fixation task in 39% of the neurons tested for this task but was not observed when sounds were presented in the absence of a behavioral task and reward. Together, these results suggest that a reward-related signal influences neural activity in the IC.

Effects of Skin Thickness on Cochlear Input Signal Using Transcutaneous Bone Conduction Implants.

Hypothesis Intracochlear sound pressures (PIC) and velocity measurements of the stapes, round window, and promontory (VStap/RW/Prom) will show frequency-dependent attenuation using magnet-based transcutaneous bone conduction implants (TCBCIs) in comparison with direct-connect skin-penetrating implants (DCBCIs). Background TCBCIs have recently been introduced as alternatives to DCBCIs. Clinical studies have demonstrated elevated high-frequency thresholds for TCBCIs as compared with DCBCIs; however, little data exist examining the direct effect of skin thickness on the cochlear input signal using TCBCIs. Methods Using seven cadaveric heads, PIC was measured in the scala vestibuli and tympani with fiber-optic pressure sensors concurrently with VStap/RW/Prom via laser Doppler vibrometry. Ipsilateral titanium implant fixtures were placed and connected to either a DCBCI or a TCBCI. Soft tissue flaps with varying thicknesses (no flap and 3, 6, and 9 mm) were placed successively between the magnetic plate and sound processor magnet. A bone conduction transducer coupled to custom software provided pure-tone stimuli between 120 and 10,240 Hz. Results Stimulation via the DCBCI produced the largest response magnitudes. The TCBCI showed similar PSV/ST and VStap/RW/Prom with no intervening flap and a frequency-dependent nonlinear reduction of magnitude with increasing flap thickness. Phase shows a comparable dependence on transmission delay as the acoustic baseline, and the slope steepens at higher frequencies as flap thickness increases, suggesting a longer group delay. Conclusion Proper soft tissue management is critical to optimize the cochlear input signal. The skin thickness–related effects on cochlear response magnitudes should be taken into account when selecting patients for a TCBCI.

The acoustical cues to sound location in the guinea pig (Cavia porcellus)

There are three main acoustical cues to sound location, each attributable to space- and frequency-dependent filtering of the propagating sound waves by the outer ears, head, and torso: Interaural differences in time (ITD) and level (ILD) as well as monaural spectral shape cues. While the guinea pig has been a common model for studying the anatomy, physiology, and behavior of binaural and spatial hearing, extensive measurements of their available acoustical cues are lacking. Here, these cues were determined from directional transfer functions (DTFs), the directional components of the head-related transfer functions, for 11 adult guinea pigs. In the frontal hemisphere, monaural spectral notches were present for frequencies from ∼10 to 20 kHz; in general, the notch frequency increased with increasing sound source elevation and in azimuth toward the contralateral ear. The maximum ITDs calculated from low-pass filtered (2 kHz cutoff frequency) DTFs were ∼250 μs, whereas the maximum ITD measured with low-frequency tone pips was over 320 μs. A spherical head model underestimates ITD magnitude under normal conditions, but closely approximates values when the pinnae were removed. Interaural level differences (ILDs) strongly depended on location and frequency; maximum ILDs were <10 dB for frequencies <4 kHz and were as large as 40 dB for frequencies >10 kHz. Removal of the pinna reduced the depth and sharpness of spectral notches, altered the acoustical axis, and reduced the acoustical gain, ITDs, and ILDs; however, spectral shape features and acoustical gain were not completely eliminated, suggesting a substantial contribution of the head and torso in altering the sounds present at the tympanic membrane.

Cochlear Implant Electrode Effect on Sound Energy Transfer Within the Cochlea During Acoustic Stimulation.

Hypothesis: Cochlear implants (CIs) designed for hearing preservation will not alter mechanical properties of the middle and inner ears as measured by intracochlear pressure (PIC) and stapes velocity (Vstap). Background: CIs designed to provide combined electroacoustic stimulation are now available. To maintain functional acoustic hearing, it is important to know if a CI electrode can alter middle or inner ear mechanics because any alteration could contribute to elevated low-frequency thresholds in electroacoustic stimulation patients. Methods: Seven human cadaveric temporal bones were prepared, and pure-tone stimuli from 120 Hz to 10 kHz were presented at a range of intensities up to 110 dB sound pressure level. PIC in the scala vestibuli (PSV) and tympani (PST) were measured with fiber-optic pressure sensors concurrently with VStap using laser Doppler vibrometry. Five CI electrodes from two different manufacturers with varying dimensions were inserted via a round window approach at six different depths (16–25 mm). Results: The responses of PIC and VStap to acoustic stimulation were assessed as a function of stimulus frequency, normalized to sound pressure level in the external auditory canal, at baseline and electrode-inserted conditions. Responses measured with electrodes inserted were generally within approximately 5 dB of baseline, indicating little effect of CI electrode insertion on PIC and VStap. Overall, mean differences across conditions were small for all responses, and no substantial differences were consistently visible across electrode types. Conclusion: Results suggest that the influence of a CI electrode on middle and inner ear mechanics is minimal despite variation in electrode lengths and configurations.

A Preliminary Investigation of the Air-Bone Gap: Changes in Intracochlear Sound Pressure With Air- and Bone-conducted Stimuli After Cochlear Implantation.

Hypothesis: A cochlear implant electrode within the cochlea contributes to the air-bone gap (ABG) component of postoperative changes in residual hearing after electrode insertion. Background: Preservation of residual hearing after cochlear implantation has gained importance as simultaneous electric-acoustic stimulation allows for improved speech outcomes. Postoperative loss of residual hearing has previously been attributed to sensorineural changes; however, presence of increased postoperative ABG remains unexplained and could result in part from altered cochlear mechanics. Here, we sought to investigate changes to these mechanics via intracochlear pressure measurements before and after electrode implantation to quantify the contribution to postoperative ABG. Methods: Human cadaveric heads were implanted with titanium fixtures for bone conduction transducers. Velocities of stapes capitulum and cochlear promontory between the two windows were measured using single-axis laser Doppler vibrometry and fiber-optic sensors measured intracochlear pressures in scala vestibuli and tympani for air- and bone-conducted stimuli before and after cochlear implant electrode insertion through the round window. Results: Intracochlear pressures revealed only slightly reduced responses to air-conducted stimuli consistent with previous literature. No significant changes were noted to bone-conducted stimuli after implantation. Velocities of the stapes capitulum and the cochlear promontory to both stimuli were stable after electrode placement. Conclusion: Presence of a cochlear implant electrode causes alterations in intracochlear sound pressure levels to air, but not bone, conducted stimuli and helps to explain changes in residual hearing noted clinically. These results suggest the possibility of a cochlear conductive component to postoperative changes in hearing sensitivity.

Intracochlear Pressure Transients During Cochlear Implant Electrode Insertion.

Hypothesis: Cochlear implant (CI) electrode insertion into the round window induces pressure transients in the cochlear fluid comparable to high-intensity sound transients. Background: Many patients receiving a CI have some remaining functional hearing at low frequencies; thus, devices and surgical techniques have been developed to use this residual hearing. To maintain functional acoustic hearing, it is important to retain function of any hair cells and auditory nerve fibers innervating the basilar membrane; however, in a subset of patients, residual low-frequency hearing is lost after CI insertion. Here, we test the hypothesis that transient intracochlear pressure spikes are generated during CI electrode insertion, which could cause damage and compromise residual hearing. Methods: Human cadaveric temporal bones were prepared with an extended facial recess. Pressures in the scala vestibuli and tympani were measured with fiber-optic pressure sensors inserted into the cochlea near the oval and round windows, whereas CI electrodes (five styles from two manufacturers) were inserted into the cochlea via a round window approach. Results: Pressures in the scala tympani tended to be larger in magnitude than pressures in the scala vestibuli, consistent with electrode insertion into the scala tympani. CI electrode insertion produced a range of pressure transients in the cochlea that could occur alone or as part of a train of spikes with equivalent peak sound pressure levels in excess of 170 dB sound pressure level. Instances of pressure transients varied with electrode styles. Conclusion: Results suggest electrode design, insertion mechanism, and surgical technique affect the magnitude and rate of intracochlear pressure transients during CI electrode insertion. Pressure transients showed intensities similar to those elicited by high-level sounds and thus could cause damage to the basilar membrane and/or hair cells.

Effects of Active and Passive Hearing Protection Devices on Sound Source Localization, Speech Recognition, and Tone Detection.

Hearing protection devices (HPDs) such as earplugs offer to mitigate noise exposure and reduce the incidence of hearing loss among persons frequently exposed to intense sound. However, distortions of spatial acoustic information and reduced audibility of low-intensity sounds caused by many existing HPDs can make their use untenable in high-risk (e.g., military or law enforcement) environments where auditory situational awareness is imperative. Here we assessed (1) sound source localization accuracy using a head-turning paradigm, (2) speech-in-noise recognition using a modified version of the QuickSIN test, and (3) tone detection thresholds using a two-alternative forced-choice task. Subjects were 10 young normal-hearing males. Four different HPDs were tested (two active, two passive), including two new and previously untested devices. Relative to unoccluded (control) performance, all tested HPDs significantly degraded performance across tasks, although one active HPD slightly improved high-frequency tone detection thresholds and did not degrade speech recognition. Behavioral data were examined with respect to head-related transfer functions measured using a binaural manikin with and without tested HPDs in place. Data reinforce previous reports that HPDs significantly compromise a variety of auditory perceptual facilities, particularly sound localization due to distortions of high-frequency spectral cues that are important for the avoidance of front-back confusions.

Discharge patterns in the lateral superior olive of decerebrate cats.

Anatomical and pharmacological studies have shown that the lateral superior olive (LSO) receives inputs from a number of sources and that LSO cells can alter the balance of their own excitatory and inhibitory drive. It is thus likely that the ongoing sound-evoked responses of LSO cells reflect a complex interplay of excitatory and inhibitory events, which may be affected by anesthesia. The goal of this study was to characterize the temporal discharge patterns of single units in the LSO of unanesthetized, decerebrate cats in response to long-duration ipsilateral best-frequency tone bursts. A decision tree is presented to partition LSO units on the basis of poststimulus time histogram shape, adaptation of instantaneous firing rate as a function of time, and sustained discharge rate. The results suggest that LSO discharge patterns form a continuum with four archetypes: sustained choppers that show two or more peaks of activity at stimulus onset and little adaptation of rate throughout the response, transient choppers that undergo a decrease in rate that eventually stabilizes with time, primary-like units that display an initial peak of activity followed by a monotonic decline in rate to a steady-state value, and onset-sustained units that exhibit an initial peak of activity at stimulus onset followed by a low sustained activity. Compared with the chopper units, the nonchopper units tend to show longer first-spike latencies, lower peak firing rates, and more irregular sustained discharge patterns. Modeling studies show that the full range of LSO response types can be obtained from an underlying sustained chopper by varying the strength and latency of a sound-driven ipsilateral inhibition relative to that of excitation. Together, these results suggest that inhibition plays a major role in shaping the temporal discharge patterns of units in unanesthetized preparations.

Drill-induced Cochlear Injury During Otologic Surgery: Intracochlear Pressure Evidence of Acoustic Trauma

HYPOTHESIS Drilling on the incus produces intracochlear pressure changes comparable to pressures created by high-intensity acoustic stimuli. BACKGROUND New-onset sensorineural hearing loss (SNHL) following mastoid surgery can occur secondary to inadvertent drilling on the ossicular chain. To investigate this, we test the hypothesis that high sound pressure levels are generated when a high-speed drill contacts the incus. METHODS Human cadaveric heads underwent mastoidectomy, and fiber-optic sensors were placed in scala tympani and vestibuli to measure intracochlear pressures (PIC). Stapes velocities (Vstap) were measured using single-axis laser Doppler vibrometry. PIC and Vstap were measured while drilling on the incus. Four-millimeter diamond and cutting burrs were used at drill speeds of 20k, 50k, and 80k Hz. RESULTS No differences in peak equivalent ear canal noise exposures (134-165 dB SPL) were seen between drill speeds or burr types. Root-mean-square PIC amplitude calculated in third-octave bandwidths around 0.5, 1, 2, 4, and 8 kHz revealed equivalent ear canal (EAC) pressures up to 110 to 112 dB SPL. A statistically significant trend toward increasing noise exposure with decreasing drill speed was seen. No significant differences were noted between burr types. Calculations of equivalent EAC pressure from Vstap were significantly higher at 101 to 116 dB SPL. CONCLUSION Our results suggest that incidental drilling on the ossicular chain can generate PIC comparable to high-intensity acoustic stimulation. Drill speed, but not burr type, significantly affected the magnitude of PIC. Inadvertent drilling on the ossicular chain produces intense cochlear stimulation that could cause SNHL.

Stapes displacement and intracochlear pressure in response to very high level, low frequency sounds

ABSTRACT The stapes is held in the oval window by the stapedial annular ligament (SAL), which restricts total peak‐to‐peak displacement of the stapes. Previous studies have suggested that for moderate (<130 dB SPL) sound levels intracochlear pressure (PIC), measured at the base of the cochlea far from the basilar membrane, increases directly proportionally with stapes displacement (DStap), thus a current model of impulse noise exposure (the Auditory Hazard Assessment Algorithm for Humans, or AHAAH) predicts that peak PIC will vary linearly with DStap up to some saturation point. However, no direct tests of DStap, or of the relationship with PIC during such motion, have been performed during acoustic stimulation of the human ear. In order to examine the relationship between DStap and PIC to very high level sounds, measurements of DStap and PIC were made in cadaveric human temporal bones. Specimens were prepared by mastoidectomy and extended facial recess to expose the ossicular chain. Measurements of PIC were made in scala vestibuli (PSV) and scala tympani (PST), along with the SPL in the external auditory canal (PEAC), concurrently with laser Doppler vibrometry (LDV) measurements of stapes velocity (VStap). Stimuli were moderate (˜100 dB SPL) to very high level (up to ˜170 dB SPL), low frequency tones (20–2560 Hz). Both DStap and PSV increased proportionally with sound pressure level in the ear canal up to approximately ˜150 dB SPL, above which both DStap and PSV showed a distinct deviation from proportionality with PEAC. Both DStap and PSV approached saturation: DStap at a value exceeding 150 &mgr;m, which is substantially higher than has been reported for small mammals, while PSV showed substantial frequency dependence in the saturation point. The relationship between PSV and DStap remained constant, and cochlear input impedance did not vary across the levels tested, consistent with prior measurements at lower sound levels. These results suggest that PSV sound pressure holds constant relationship with DStap, described by the cochlear input impedance, at these, but perhaps not higher, stimulation levels. Additionally, these results indicate that the AHAAH model, which was developed using results from small animals, underestimates the sound pressure levels in the cochlea in response to high level sound stimulation, and must be revised. HIGHLIGHTSLow frequency stapes velocity and intracochlear pressure described in human cadaver.Stapes displacement increases linearly with sound level up to ˜150 dB SPL.Peak‐to‐peak DStap asymptotes at ˜150 &mgr;m in humans, not ˜30 &mgr;m as in cat/rabbit.Cochlear input impedance remains constant up to ˜170 dB SPL at low frequencies.