Auditory Research publications

Distortion product otoacoustic emissions (DPOAEs) are traditionally evoked by two-tone stimuli. In this study, emission data from Mongolian gerbils are reported that were obtained with stimuli consisting of six to 10 tones. The stimuli were constructed by replacing one of the tones of a tone pair by a narrowband multitone complex. This produced rich spectra of the ear canal sound pressure in which many of the third-order DPOAEs originated from the interaction of triplets of stimulus components. A careful choice of the stimulus frequencies ensured that none of these DPOAE components coincided. Three groups of DPOAEs are reported, two of which are closely related to DPOAEs evoked by tone pairs. The third group has no two-tone equivalent and only arises when using a multitone stimulus. We analyzed the relation between multitone-evoked DPOAEs and DPOAEs evoked by tone pairs, and explored the new degrees of freedom offered by the multitone paradigm.

Objectives/Hypothesis: One limitation with cochlear implants is the difficulty stimulating spatially discrete spiral ganglion cell groups because of electrode interactions. Multipolar electrodes have improved on this some, but also at the cost of much higher device power consumption. Recently, it has been shown that spatially selective stimulation of the auditory nerve is possible with a mid‐infrared laser aimed at the spiral ganglion via the round window. However, these neurons must be driven at adequate rates for optical radiation to be useful in cochlear implants. We herein use single‐fiber recordings to characterize the responses of auditory neurons to optical radiation. Study Design: In vivo study using normal‐hearing adult gerbils. Methods: Two diode lasers were used for stimulation of the auditory nerve. They operated between 1.844 μm and 1.873 μm, with pulse durations of 35 μs to 1,000 μs, and at repetition rates up to 1,000 pulses per second (pps). The laser outputs were coupled to a 200‐μm‐diameter optical fiber placed against the round window membrane and oriented toward the spiral ganglion. The auditory nerve was exposed through a craniotomy, and recordings were taken from single fibers during acoustic and laser stimulation. Results: Action potentials occurred 2.5 ms to 4.0 ms after the laser pulse. The latency jitter was up to 3 ms. Maximum rates of discharge averaged 97 ± 52.5 action potentials per second. The neurons did not strictly respond to the laser at stimulation rates over 100 pps. Conclusions: Auditory neurons can be stimulated by a laser beam passing through the round window membrane and driven at rates sufficient for useful auditory information. Optical stimulation and electrical stimulation have different characteristics; which could be selectively exploited in future cochlear implants. Laryngoscope, 2010

Lungfishes are the closest living relatives of the tetrapods, and the ear of recent lungfishes resembles the tetrapod ear more than the ear of ray-finned fishes and is therefore of interest for understanding the evolution of hearing in the early tetrapods. The water-to-land transition resulted in major changes in the tetrapod ear associated with the detection of air-borne sound pressure, as evidenced by the late and independent origins of tympanic ears in all of the major tetrapod groups. To investigate lungfish pressure and vibration detection, we measured the sensitivity and frequency responses of five West African lungfish ( Protopterus annectens ) using brainstem potentials evoked by calibrated sound and vibration stimuli in air and water. We find that the lungfish ear has good low-frequency vibration sensitivity, like recent amphibians, but poor sensitivity to air-borne sound. The skull shows measurable vibrations above 100 Hz when stimulated by air-borne sound, but the ear is apparently insensitive at these frequencies, suggesting that the lungfish ear is neither adapted nor pre-adapted for aerial hearing. Thus, if the lungfish ear is a model of the ear of early tetrapods, their auditory sensitivity was limited to very low frequencies on land, mostly mediated by substrate-borne vibrations.

The inferior colliculus (IC) of the pallid bat has a large percentage of neurons that respond selectively to the rate and direction of the bat's echolocation pulse, a downward FM sweep. Three underlying mechanisms have been previously described. Here we describe a fourth mechanism, facilitation, that shapes selectivity for both sweep rate and direction. The neurons studied are termed FM specialists, because they do not respond to tones. Most were selective for the downward sweep direction, and this preference was expressed even when presented with narrowband, 1 kHz sweeps that crossed only a fraction of their excitatory receptive fields. This selectivity was also expressed in response to two tones delayed in time, termed two-tone facilitation (TTF). Direction-selective neurons showed a greatly facilitated response when a higher-frequency tone preceded a lower-frequency tone, simulating conditions in a downward sweep. The degree of temporal asymmetry in facilitation accurately predicted direction selectivity. When the spectral difference between the two tones was increased, the best delay also increased and could be used to predict a neuron's preferred sweep rate. To determine whether TTF alone created rate and direction selectivity, low- and high-frequency inhibitory sidebands, which can also shape selectivity, were eliminated from sweeps. In most cases, selectivity persisted. These results support the idea of spectral delay lines that produce an overlap and summation of excitatory inputs only when a dynamic stimulus traverses a receptive field in one direction at a specific velocity.

In this study, combinations of interaural time differences (ITD) and interaural level differences (ILD) were applied to trains of 4000 Hz Gabor clicks (Gaussian-filtered impulses) and presented to listeners over headphones. ITD/ILD equivalence functions, or "trading ratios" (TR) were estimated using two different procedures: a "closed-loop" procedure in which subjects adjusted (via head-turn) the ILD of a target click train to counteract the effects of an imposed ITD, and an "open-loop" procedure in which subjects indicated (also via head-turn) the lateral position of click trains containing independent combinations of ITD and ILD. For both tasks, TR values increasingly favored ILD over ITD as inter-click interval (ICI) decreased from 10 to 2 ms. Subsequent analysis confirmed that this change reflected a loss of sensitivity to envelope ITD at short ICI rather than a gain in sensitivity to ILD, consistent with prior studies demonstrating rate-limited processing of ongoing envelope ITD. Significant intersubject differences in the data included two subjects whose TR values obtained under both procedures were consistently lower (greater influence of ITD) than other subjects', and did not vary with ICI. Such differences suggest that multiple mechanisms of ITD/ILD combination may be utilized to varying degrees by individual listeners. By at least one of those mechanisms, ITD sensitivity (but not ILD sensitivity) is limited to low modulation rates.

Experience-dependent enhancement of neural encoding of pitch in the auditory brainstem has been observed for only specific portions of native pitch contours exhibiting high rates of pitch acceleration, irrespective of speech or nonspeech contexts. This experiment allows us to determine whether this language-dependent advantage transfers to acceleration rates that extend beyond the pitch range of natural speech. Brainstem frequency-following responses (FFRs) were recorded from Chinese and English participants in response to four, 250-ms dynamic click-train stimuli with different rates of pitch acceleration. The maximum pitch acceleration rates in a given stimulus ranged from low (0.3Hz/ms; Mandarin Tone 2) to high (2.7Hz/ms; 2 octaves). Pitch strength measurements were computed from the FFRs using autocorrelation algorithms with an analysis window centered at the point of maximum pitch acceleration in each stimulus. Between-group comparisons of pitch strength revealed that Chinese exhibit more robust pitch representation than English across all four acceleration rates. Regardless of language group, pitch strength was greater in response to acceleration rates within or proximal to natural speech relative to those beyond its range. Though both groups showed decreasing pitch strength with increasing acceleration rates, pitch representations of the Chinese group were more resistant to degradation. FFR spectral data were complementary across acceleration rates. These findings demonstrate that perceptually salient pitch cues associated with lexical tone influence brainstem pitch extraction not only in the speech domain, but also in auditory signals that clearly fall outside the range of dynamic pitch that a native listener is exposed to.

The intensity of a noise-induced startle response can be reduced by the presentation of an otherwise neutral stimulus immediately before the noise ("prepulse inhibition" or PPI). We used a form of PPI to study the effects of damage to auditory cortex on the discrimination of speech sounds by rats. Subjects underwent control surgery or treatment of the auditory cortex with the vasoconstrictor endothelin-1. This treatment caused damage concentrated in primary auditory cortex (A1). Both before and after lesions, subjects were tested on 5 tasks, most presenting a pair of human speech sounds (consonant-vowel syllables) so that the capacity for discrimination would be evident in the extent of PPI. Group comparisons failed to reveal any consistent lesion effect. At the same time, the analysis of individual differences in performance by multiple regression suggests that some of the temporal processing required to discriminate speech sounds is concentrated anteroventrally in the right A1. These results also confirm that PPI can be adapted to studies of the brain mechanisms involved in the processing of speech and other complex sounds.

Associative learning induces plasticity in the representation of sensory information in sensory cortices. Such high-order associative representational plasticity (HARP) in the primary auditory cortex (A1) is a likely substrate of auditory memory: it is specific, rapidly acquired, long-lasting and consolidates. Because HARP is likely to support the detailed content of memory, it is important to identify the necessary behavioral factors that dictate its induction. Learning strategy is a critical factor for the induction of plasticity (Bieszczad & Weinberger, 2010b). Specifically, use of a strategy that relies on tone onsets induces HARP in A1 in the form of signal-specific decreased threshold and bandwidth. The present study tested the hypothesis that the form and degree of HARP in A1 reflects the amount of use of an "onset strategy". Adult male rats (n=7) were trained in a protocol that increased the use of this strategy from approximately 20% in prior studies to approximately 80%. They developed signal-specific gains in representational area, transcending plasticity in the form of local changes in threshold and bandwidth. Furthermore, the degree of area gain was proportional to the amount of use of the onset strategy. A second complementary experiment demonstrated that use of a learning strategy that specifically did not rely on tone onsets did not produce gains in representational area; but rather produced area loss. Together, the findings indicate that the amount of strategy use is a dominant factor for the induction of learning-induced cortical plasticity along a continuum of both form and degree.

Songbirds, which, like humans, learn complex vocalizations, provide an excellent model for the study of acoustic pattern recognition. Here we examined the role of three basic acoustic parameters in an ethologically relevant categorization task. Female zebra finches were first trained to classify songs as belonging to one of two males and then asked whether they could generalize this knowledge to songs systematically altered with respect to frequency, timing, or intensity. Birds' performance on song categorization fell off rapidly when songs were altered in frequency or intensity, but they generalized well to songs that were changed in duration by >25%. Birds were not deaf to timing changes, however; they detected these tempo alterations when asked to discriminate between the same song played back at two different speeds. In addition, when birds were retrained with songs at many intensities, they could correctly categorize songs over a wide range of volumes. Thus although they can detect all these cues, birds attend less to tempo than to frequency or intensity cues during song categorization. These results are unexpected for several reasons: zebra finches normally encounter a wide range of song volumes but most failed to generalize across volumes in this task; males produce only slight variations in tempo, but females generalized widely over changes in song duration; and all three acoustic parameters are critical for auditory neurons. Thus behavioral data place surprising constraints on the relationship between previous experience, behavioral task, neural responses, and perception. We discuss implications for models of auditory pattern recognition.

Interaural time differences (ITDs) are the primary cue for the localization of low-frequency sound sources in the azimuthal plane. For decades, it was assumed that the coding of ITDs in the mammalian brain was similar to that in the avian brain, where information is sparsely distributed across individual neurons, but recent studies have suggested otherwise. In this study, we characterized the representation of ITDs in adult male and female gerbils. First, we performed behavioral experiments to determine the acuity with which gerbils can use ITDs to localize sounds. Next, we used different decoders to infer ITDs from the activity of a population of neurons in central nucleus of the inferior colliculus. These results show that ITDs are not represented in a distributed manner, but rather in the summed activity of the entire population. To contrast these results with those from a population where the representation of ITDs is known to be sparsely distributed, we performed the same analysis on activity from the external nucleus of the inferior colliculus of adult male and female barn owls. Together, our results support the idea that, unlike the avian brain, the mammalian brain represents ITDs in the overall activity of a homogenous population of neurons within each hemisphere.

The generalization of learning from trained to untrained conditions is of great potential value because it markedly increases the efficacy of practice. In principle, generalization and the learning itself could arise from either the same or distinct neural changes. Here, we assessed these two possibilities in the realm of human perceptual learning by comparing the time course of improvement on a trained condition (learning) to that on an untrained condition (generalization) for an auditory temporal-interval discrimination task. While significant improvement on the trained condition occurred within 2 d, generalization to the untrained condition lagged behind, only emerging after 4 d. The different time courses for learning and generalization suggest that these two types of perceptual improvement can arise from at least partially distinct neural changes. The notably longer time course for generalization than learning demonstrates that increasing the duration of training can be an effective means to increase the number of conditions to which learning generalizes on perceptual tasks.

Primary sensory cortex integrates sensory information from afferent feedforward thalamocortical projection systems and convergent intracortical microcircuits. Both input systems have been demonstrated to provide different aspects of sensory information. Here we have used high-density recordings of laminar current source density (CSD) distributions in primary auditory cortex of Mongolian gerbils in combination with pharmacological silencing of cortical activity and analysis of the residual CSD, to dissociate the feedforward thalamocortical contribution and the intracortical contribution to spectral integration. We found a temporally highly precise integration of both types of inputs when the stimulation frequency was in close spectral neighborhood of the best frequency of the measurement site, in which the overlap between both inputs is maximal. Local intracortical connections provide both directly feedforward excitatory and modulatory input from adjacent cortical sites, which determine how concurrent afferent inputs are integrated. Through separate excitatory horizontal projections, terminating in cortical layers II/III, information about stimulus energy in greater spectral distance is provided even over long cortical distances. These projections effectively broaden spectral tuning width. Based on these data, we suggest a mechanism of spectral integration in primary auditory cortex that is based on temporally precise interactions of afferent thalamocortical inputs and different short- and long-range intracortical networks. The proposed conceptual framework allows integration of different and partly controversial anatomical and physiological models of spectral integration in the literature.

Spatial attention mediates the selection of information from different parts of space. When a brief cue is presented shortly before a target [cue to target onset asynchrony (CTOA)] in the same location, behavioral responses are facilitated, a process called attention capture. At longer CTOAs, responses to targets presented in the same location are inhibited; this is called inhibition of return (IOR). In the visual modality, these processes have been demonstrated in both humans and non‐human primates, the latter allowing for the study of the underlying neural mechanisms. In audition, the effects of attention have only been shown in humans when the experimental task requires sound localization. Studies in monkeys with the use of similar cues but without a sound localization requirement have produced negative results. We have studied the effects of predictive acoustic cues on the latency of gaze shifts to visual and auditory targets in monkeys experienced in localizing sound sources in the laboratory with the head unrestrained. Both attention capture and IOR were demonstrated with acoustic cues, although with a faster time course than with visual cues. Additionally, the effect was observed across sensory modalities (acoustic cue to visual target), suggesting that the underlying neural mechanisms of these effects may be mediated within the superior colliculus, a center where inputs from both vision and audition converge.

Young normal-hearing (YNH) and older normal-hearing (ONH) listeners identified vowels in naturally produced /bVb/ syllables and in modified syllables that consisted of variable portions of the vowel edges (silent-center [SC] stimuli) or vowel center (center-only [CO] stimuli). Listeners achieved high levels of performance for all but the shortest stimuli, indicating that they were able to access vowel cues throughout the syllable. ONH listeners performed similarly to YNH listeners for most stimuli, but performed more poorly for the shortest CO stimuli. SC and CO stimuli were equally effective in supporting vowel identification except when acoustic information was limited to 20 ms.

Dynamin-1 (Dnm1) encodes a large multimeric GTPase necessary for activity-dependent membrane recycling in neurons, including synaptic vesicle endocytosis. Mice heterozygous for a novel spontaneous Dnm1 mutation--fitful--experience recurrent seizures, and homozygotes have more debilitating, often lethal seizures in addition to severe ataxia and neurosensory deficits. Fitful is a missense mutation in an exon that defines the DNM1a isoform, leaving intact the alternatively spliced exon that encodes DNM1b. The expression of the corresponding alternate transcripts is developmentally regulated, with DNM1b expression highest during early neuronal development and DNM1a expression increasing postnatally with synaptic maturation. Mutant DNM1a does not efficiently self-assemble into higher order complexes known to be necessary for proper dynamin function, and it also interferes with endocytic recycling in cell culture. In mice, the mutation results in defective synaptic transmission characterized by a slower recovery from depression after trains of stimulation. The DNM1a and DNM1b isoform pair is highly conserved in vertebrate evolution, whereas invertebrates have only one isoform. We speculate that the emergence of more specialized forms of DNM1 may be important in organisms with complex neuronal function.

Adult rats were trained to detect the occurrence of a two-element sound sequence in a background of nine other nontarget sound pairs. Training resulted in a modest, enduring, static expansion of the cortical areas of representation of both target stimulus sounds. More importantly, once the initial stimulus A in the target A-B sequence was presented, the cortical “map” changed dynamically, specifically to exaggerate further the representation of the “anticipated” stimulus B. If B occurred, it was represented over a larger cortical area by more strongly excited, more coordinated, and more selectively responding neurons. This biasing peaked at the expected time of B onset with respect to A onset. No dynamic biasing of responses was recorded for any sound presented in a nontarget pair. Responses to nontarget frequencies flanking the representation of B were reduced in area and in response strength only after the presentation of A at the expected time of B onset. This study shows that cortical areas are not representationally static but, to the contrary, can be biased moment by moment in time as a function of behavioral context.

Objective: To further examine the reliability of categorical loudness scaling (CLS) for individual loudness categories and for the slope of the CLS functions. And, to evaluate the relationship between CLS and audiometric threshold. Design: CLS functions were obtained in 74 subjects, 58 with hearing loss and 16 with normal hearing. CLS functions were measured at three frequencies (1, 2, and 4 kHz) in two separate sessions separated by as little as 1 wk and as much as 6 mo. Reliability of mean and median levels within each loudness category was assessed using SDs and correlation coefficients. Lines were fit to the CLS functions, and slopes of the lines were used to assess reliability and the relation between CLS and audiometric threshold. Results: Similar reliability for CLS measurements was observed in both normal-hearing and hearing-impaired subjects at all frequencies. Across both groups of subjects, correlations describing the reliability of mean stimulus level within category exceeded 0.92 at all frequencies. In addition, SDs of the mean stimulus-level difference between visits ranged from 6.6 to 7.8 dB, depending on frequency. The correlation between the slope of a straight line fitted to the entire CLS function and audiometric threshold collapsed across frequencies was 0.72. Two line segments were then fit to the CLS function: one segment was fit to the soft portion of the CLS function (categorical units < or =20) and the other segment to the loud portion (categorical unit >20). Slopes of the line fit to the entire CLS function and of the line fit to the soft portion of the CLS function were both reliable across sessions. The slope of the line fit to the soft portion increased as audiometric threshold increased, with the correlations greater than 0.86 at all frequencies. No relationship was observed between slope of the line fit to the loud portion of the CLS function and audiometric threshold. Iso-loudness contours were constructed from the CLS data and used to determine the gain that would be needed to produce "normal" loudness percepts for hearing-impaired individuals. Conclusions: Within-subject CLS measurements were reliable across sessions both for individual loudness categories and for slope of the CLS functions. In addition, the slope of the low-level portion of the CLS function varied in a predictable manner with audiometric threshold, with slope increasing as audiometric threshold increased. Finally, gain as a function of input level needed to provide loudness percepts for individuals with hearing loss equal to the loudness percepts of normal-hearing individuals can be estimated from audiometric threshold. This finding supports the assumption that audiometric threshold and response growth (loudness) are both determined by the same underlying cochlear mechanisms.

In the intermediate nucleus of the lateral lemniscus (INLL), some neurons display a form of spectral integration in which excitatory responses to sounds at their best frequency are inhibited by sounds within a frequency band at least one octave lower. Previous work showed that this response property depends on low-frequency-tuned glycinergic input. To identify all sources of inputs to these INLL neurons, and in particular the low-frequency glycinergic input, we combined retrograde tracing with immunohistochemistry for the neurotransmitter glycine. We deposited a retrograde tracer at recording sites displaying either high best frequencies (>75 kHz) in conjunction with combination-sensitive inhibition, or at sites displaying low best frequencies (23-30 kHz). Most retrogradely labeled cells were located in the ipsilateral medial nucleus of the trapezoid body (MNTB) and contralateral anteroventral cochlear nucleus. Consistent labeling, but in fewer numbers, was observed in the ipsilateral lateral nucleus of the trapezoid body (LNTB), contralateral posteroventral cochlear nucleus, and a few other brainstem nuclei. When tracer deposits were combined with glycine immunohistochemistry, most double-labeled cells were observed in the ipsilateral MNTB (84%), with fewer in LNTB (13%). After tracer deposits at combination-sensitive recording sites, a striking result was that MNTB labeling occurred in both medial and lateral regions. This labeling appeared to overlap the MNTB labeling that resulted from tracer deposits in low-frequency recording sites of INLL. These findings suggest that MNTB is the most likely source of low-frequency glycinergic input to INLL neurons with high best frequencies and combination-sensitive inhibition. This work establishes an anatomical basis for frequency integration in the auditory brainstem.

The monoclonal antibody SMI-32 was used to characterize and distinguish individual areas of cat auditory cortex. SMI-32 labels non-phosphorylated epitopes on the high- and medium-molecular weight subunits of neurofilament proteins in cortical pyramidal cells and dendritic trees with the most robust immunoreactivity in layers III and V. Auditory areas with unique patterns of immunoreactivity included: primary auditory cortex (AI), second auditory cortex (AII), dorsal zone (DZ), posterior auditory field (PAF), ventral posterior auditory field (VPAF), ventral auditory field (VAF), temporal cortex (T), insular cortex (IN), anterior auditory field (AAF), and the auditory field of the anterior ectosylvian sulcus (fAES). Unique patterns of labeling intensity, soma shape, soma size, layers of immunoreactivity, laminar distribution of dendritic arbors, and labeled cell density were identified. Features that were consistent in all areas included: layers I and IV neurons are immunonegative; nearly all immunoreactive cells are pyramidal; and immunoreactive neurons are always present in layer V. To quantify the results, the numbers of labeled cells and dendrites, as well as cell diameter, were collected and used as tools for identifying and differentiating areas. Quantification of the labeling patterns also established profiles for ten auditory areas/layers and their degree of immunoreactivity. Areal borders delineated by SMI-32 were highly correlated with tonotopically-defined areal boundaries. Overall, SMI-32 immunoreactivity can delineate ten areas of cat auditory cortex and demarcate topographic borders. The ability to distinguish auditory areas with SMI-32 is valuable for the identification of auditory cerebral areas in electrophysiological, anatomical, and/or behavioral investigations.

Cave fish have rarely been investigated with regard to their inner ear morphology, hearing abilities, and acoustic communication. Based on a previous study that revealed morphological differences in the saccular otolith between a cave and two surface populations of Poecilia mexicana, we checked for additional differences in utricular and lagenar otoliths and tested whether different populations have similar hearing sensitivities. We found pronounced differences in the shape of all three otoliths. Otoliths of the saccule and lagena from cave fish differed from those of surface fish in the features of the face oriented towards the sensory epithelium. In addition, otoliths of the utricle and lagena were significantly heavier in cave fish. Auditory sensitivities were measured between 100 and 1500Hz, utilizing the auditory evoked potential recording technique. We found similar hearing abilities in cave and surface fish, with greatest sensitivity between 200 and 300Hz. An acoustic survey revealed that neither ecotype produced species-specific sounds. Our data indicate that cave dwelling altered the otolith morphology in Atlantic mollies, probably due to metabolic differences. Different otolith morphology, however, did not affect general auditory sensitivity or acoustic behavior.