Robert D. Frisina

Speech recognition in noise and presbycusis: relations to possible neural mechanisms

This study is part of ongoing efforts to characterize and determine the neural bases of presbycusis. These efforts utilize humans and animals in sets of overlapping hypotheses and experiments. Here, 50 young adult and elderly subjects, with normal audiometric thresholds or high-frequency hearing loss, were presented three types of linguistic materials at suprathreshold levels to determine speech recognition performance in noise. The study sought to determine how peripheral and central auditory system dysfunctions might be implicated in the speech recognition problems of elderly humans. There were four main findings. (1) Peripheral auditory nervous system pathologies, manifested as reduced sensitivity for speech-frequency pure tones and speech materials, contribute to elevated speech reception thresholds in quiet, and to reduced speech recognition in noise. (2) Good cognitive ability was demonstrated in the old subjects who took advantage of supportive context as well or better than young subjects, strongly indicating that the cortical portions of the speech/language nervous system did not account for the speech understanding dysfunctions of the old subjects. (3) When audibility and cognitive functioning were not affected, the demonstrated speech-recognition in-noise dysfunction remained in old subjects. This implicates auditory brainstem or auditory cortex temporal-resolution dysfunctions in accounting for the observed differences in speech processing. (4) Performance differences between young and elderly subjects with elevated thresholds illustrate the effects of age plus hearing loss and thereby implicate both peripheral and central dysfunctions in presbycusics. This is because the differences in performance between young and elderly subjects with normal peripheral sensitivity identified a central auditory dysfunction.

Encoding of amplitude modulation in the gerbil cochlear nucleus. I: A hierarchy of enhancement

The main goal of the present study was to investigate the encoding of a biologically-relevant acoustic feature--amplitude modulation (AM)--in single neurons of the auditory nerve and ventral cochlear nucleus (VCN). In the anesthetized gerbil auditory-nerve fibers and VCN units show strong synchronous responses to low-intensity, low-frequency AM. As frequency increases, the strength of the synchronous response decreases. In the auditory nerve the strength of the synchronous response is substantially less at high intensities than at low intensities and does not change significantly with AM frequency at high intensities. In contrast to the auditory nerve, VCN units show strong responses at high intensities. They have a particular AM frequency to which they are maximally responsive, and this frequency varies from unit to unit. Therefore, VCN units transform their ascending inputs by enhancing the synchronous response to AM. A correlation exists between a units ability to encode AM and its responses to simple sounds. Specifically, onset units show the strongest synchronous responses, followed in order by chopper, primarylike-with-notch and primarylike units. This enhancement is greatest at high intensities and can occur up to 90 dB above a units threshold. Thus, a hierarchy of enhancement for AM processing exists in the most peripheral nucleus of the central auditory system.

Quantitative measures of hair cell loss in CBA and C57BL/6 mice throughout their life spans

The CBA mouse shows little evidence of hearing loss until late in life, whereas the C57BL/6 strain develops a severe and progressive, high-frequency sensorineural hearing loss beginning around 3-6 months of age. These functional differences have been linked to genetic differences in the amount of hair cell loss as a function of age; however, a precise quantitative description of the sensory cell loss is unavailable. The present study provides mean values of inner hair cell (IHC) and outer hair cell (OHC) loss for CBA and C57BL/6 mice at 1, 3, 8, 18, and 26 months of age. CBA mice showed little evidence of hair cell loss until 18 months of age. At 26 months of age, OHC losses in the apex and base of the cochlea were approximately 65% and 50%, respectively, and IHC losses were approximately 25% and 35%. By contrast, C57BL/6 mice showed approximately a 75% OHC and a 55% IHC loss in the base of the cochlea at 3 months of age. OHC and IHC losses increased rapidly with age along a base-to-apex gradient. By 26 months of age, more than 80% of the OHCs were missing throughout the entire cochlea; however, IHC losses ranged from 100% near the base of the cochlea to approximately 20% in the apex.

Age-Related Alteration in Processing of Temporal Sound Features in the Auditory Midbrain of the CBA Mouse

The perception of complex sounds, such as speech and animal vocalizations, requires the central auditory system to analyze rapid, ongoing fluctuations in sound frequency and intensity. A decline in temporal acuity has been identified as one component of age-related hearing loss. The detection of short, silent gaps is thought to reflect an important fundamental dimension of temporal resolution. In this study we compared the neural response elicited by silent gaps imbedded in noise of single neurons in the inferior colliculus (IC) of young and old CBA mice. IC neurons were classified by their temporal discharge patterns. Phasic units, which accounted for the majority of response types encountered, tended to have the shortest minimal gap thresholds (MGTs), regardless of age. We report three age-related changes in neural processing of silent gaps. First, although the shortest MGTs (1–2 msec) were observed in phasic units from both young and old animals, the number of neurons exhibiting the shortest MGTs was much lower in old mice, regardless of the presentation level. Second, in the majority of phasic units, recovery of response to the stimulus after the silent gap was of a lower magnitude and much slower in units from old mice. Finally, the neuronal map representing response latency versus best frequency was found to be altered in the old IC. These results demonstrate a central auditory system correlate for age-related decline in temporal processing at the level of the auditory midbrain.

Subcortical neural coding mechanisms for auditory temporal processing.

Biologically relevant sounds such as speech, animal vocalizations and music have distinguishing temporal features that are utilized for effective auditory perception. Common temporal features include sound envelope fluctuations, often modeled in the laboratory by amplitude modulation (AM), and starts and stops in ongoing sounds, which are frequently approximated by hearing researchers as gaps between two sounds or are investigated in forward masking experiments. The auditory system has evolved many neural processing mechanisms for encoding important temporal features of sound. Due to rapid progress made in the field of auditory neuroscience in the past three decades, it is not possible to review all progress in this field in a single article. The goal of the present report is to focus on single-unit mechanisms in the mammalian brainstem auditory system for encoding AM and gaps as illustrative examples of how the system encodes key temporal features of sound. This report, following a systems analysis approach, starts with findings in the auditory nerve and proceeds centrally through the cochlear nucleus, superior olivary complex and inferior colliculus. Some general principles can be seen when reviewing this entire field. For example, as one ascends the central auditory system, a neural encoding shift occurs. An emphasis on synchronous responses for temporal coding exists in the auditory periphery, and more reliance on rate coding occurs as one moves centrally. In addition, for AM, modulation transfer functions become more bandpass as the sound level of the signal is raised, but become more lowpass in shape as background noise is added. In many cases, AM coding can actually increase in the presence of background noise. For gap processing or forward masking, coding for gaps changes from a decrease in spike firing rate for neurons of the peripheral auditory system that have sustained response patterns, to an increase in firing rate for more central neurons with transient responses. Lastly, for gaps and forward masking, as one ascends the auditory system, some suppression effects become quite long (echo suppression), and in some stimulus configurations enhancement to a second sound can take place.

Neural correlates of behavioral gap detection in the inferior colliculus of the young CBA mouse

Abstract The gap detection paradigm is frequently used in psychoacoustics to characterize the temporal acuity of the auditory system. Neural responses to silent gaps embedded in white-noise carriers, were obtained from mouse inferior colliculus (IC) neurons and the results compared to behavioral estimates of gap detection. Neural correlates of gap detection were obtained from 78 single neurons located in the central nucleus of the IC. Minimal gap thresholds (MGTs) were computed from single-unit gap functions and were found to be comparable, 1–2 ms, to the behavioral gap threshold (2 ms). There was no difference in MGTs for units in which both carrier intensities were collected. Single unit responses were classified based on temporal discharge patterns to steady-state noise bursts. Onset and primary-like units had the shortest mean MGTs (2.0 ms), followed by sustained units (4.0 ms) and phasic-off units (4.2 ms). The longest MGTs were obtained for inhibitory neurons (x¯ = 14 ms). Finally, the time-course of behavioral and neurophysiological gap functions were found to be in good agreement. The results of the present study indicate the neural code necessary for behavioral gap detection is present in the temporal discharge patterns of the majority of IC neurons.

Characterization of hearing loss in aged type II diabetics.

Presbycusis - age-related hearing loss - is the number one communicative disorder and a significant chronic medical condition of the aged. Little is known about how type II diabetes, another prevalent age-related medical condition, and presbycusis interact. The present investigation aimed to comprehensively characterize the nature of hearing impairment in aged type II diabetics. Hearing tests measuring both peripheral (cochlea) and central (brainstem and cortex) auditory processing were utilized. The majority of differences between the hearing abilities of the aged diabetics and their age-matched controls were found in measures of inner ear function. For example, large differences were found in pure-tone audiograms, wideband noise and speech reception thresholds, and otoacoustic emissions. The greatest deficits tended to be at low frequencies. In addition, there was a strong tendency for diabetes to affect the right ear more than the left. One possible interpretation is that as one develops presbycusis, the right ear advantage is lost, and this decline is accelerated by diabetes. In contrast, auditory processing tests that measure both peripheral and central processing showed fewer declines between the elderly diabetics and the control group. Consequences of elevated blood sugar levels as possible underlying physiological mechanisms for the hearing loss are discussed.

Encoding of amplitude modulation in the gerbil cochlear nucleus : II. Possible neural mechanisms

Rapid changes in sound amplitude--amplitude modulation (AM)--comprise an important feature of biologically-relevant sounds, including speech. In the companion paper, a hierarchy of enhancement for AM processing was demonstrated for unit types of the gerbil ventral cochlear nucleus (VCN) [Frisina, et al., Hear. Res. 44, 1990]. In the present report additional neurophysiological findings are presented as an initial test of alternative hypotheses of how VCN unit types amplify or enhance AM information, and how they accomplish this over a wide intensity range. These hypotheses invoke mechanisms such as off-CF excitatory or inhibitory inputs, input from high-threshold auditory-nerve fibers, amplification of residual AM responses of auditory-nerve fibers at high intensities, or post-synaptic cell feedback. From consideration of VCN unit response properties such as onset and steady-state rate-intensity functions, pure-tone tuning, and non-CF responses to AM, it is concluded that: Off-CF excitatory inputs do not play a significant role in VCN AM encoding; Off-CF inhibitory inputs could work in conjunction with one or more of the other proposed mechanisms to account for differential enhancement of AM by VCN neurons.

Effects of age on contralateral suppression of distortion product otoacoustic emissions in human listeners with normal hearing

The auditory efferent system presumably plays a role in enhancing signals in noise and, in particular, speech perception in background noise. This study measured the age-related changes of the medial olivocochlear (MOC) system by comparing distortion product otoacoustic emissions (DPOAEs) with and without contralateral white noise stimulation. Otoacoustic emissions were typically reduced in level (magnitude) when white noise was presented to the contralateral ear. This contralateral suppression (CS) is attributed to activation of the MOC system, which has an inhibitory effect on the outer hair cell (OHC) system. By studying CS on cochlear output in human listeners of different ages, it is possible to describe aging effects on the MOC system. Human subjects were young adult, middle aged and old (n = 10/group). All subjects had normal hearing and middle-ear function based upon standard audiometric criteria. The present study recorded 2f1–f2 DPOAE-grams in response to moderate primary tones (L1 = 75, L2 = 65 dB SPL), from 1 to 6.3 kHz. The principal findings were that DPOAE levels were smaller in the old compared to the young group and that CS declined with age for the middle-aged and old groups. In addition, CS in the 1- to 2-kHz range was greater than in the 4- to 6-kHz range for all ages, but especially for the old group. These findings suggest that a functional decline of the MOC system with age precedes OHC degeneration. Moreover, the MOC system maintains better function in the 1- to 2-kHz range than in the 4- to 6-kHz range as a function of age.

Sex differences in distortion product otoacoustic emissions as a function of age in CBA mice

Age-related hearing loss--presbycusis--is the number one communication problem of the aged. A major contributor to presbycusis is the progressive degeneration of cochlear outer hair cells (OHCs). Distortion product otoacoustic emissions (DPOAEs) are effective in vivo, physiological measures of hearing, assessing the health and functioning of the OHCs in mammals. We and others have previously demonstrated that DPOAE amplitudes decline with age in humans and mice. The present studys objective was to measure age-related declines in the OHCs in CBA mice (slow, progressive age-related hearing loss) by comparing DPOAEs and auditory brainstem responses (ABRs) generated from females and males. Young adult (2.1-2.9 months) and middle-aged CBA (14.0-16.4 months) mice were tested, as well as old CBAs (24.3-29.0 months). DPOAE-grams were obtained with L1 = 65 and L2 = 50 dB SPL, f1/f2 = 1.25, using eight points per octave covering a frequency range from 5.6 to 44.8 kHz (geometric mean frequency). ABRs ranged from 3 to 48 kHz. Analyses revealed that DPOAE levels decreased with age for middle-aged and old male CBAs, but for female CBAs, declines did not occur until old age - after menopause. In contrast, ABR amplitudes for female and male young adult and middle-aged CBAs were the same. Female ABR thresholds were lower than males for old CBAs. In conclusion, we discovered that pre-menopausal CBA female mice have healthier OHCs relative to middle-aged males, but much of this relative advantage is lost post-menopause. Understanding sex differences in age-related sensory disorders will be quite helpful for the goals of preventing, slowing or curing sensory problems in old age for both women and men.