Auditory Research publications

Acoustic communication involves both the generation and the detection of a signal. In the coqui frog ( Eleutherodactylus coqui ), it is known that the spectral contents of its calls systematically change with altitude above sea level. Here, distortion product otoacoustic emissions are used to assess the frequency range over which the inner ear is sensitive. It is found that both the spectral contents of the calls and the inner-ear sensitivity change in a similar fashion along an altitudinal gradient. As a result, the call frequencies and the auditory tuning are closely matched at all altitudes. We suggest that the animal's body size determines the frequency particulars of the call apparatus and the inner ear.

Spatial and non-spatial sensory information is hypothesized to be evaluated in parallel pathways. In this study, we tested the spatial and non-spatial sensitivity of auditory neurons in the ventrolateral prefrontal cortex (vPFC), a cortical area in the non-spatial pathway. Activity was tested while non-human primates reported changes in an auditory stimulus' spatial or non-spatial features. We found that vPFC neurons were reliably modulated during a non-spatial auditory task but were not modulated during a spatial auditory task. The degree of modulation during the non-spatial task correlated positively with the monkeys' behavioral performance. These results are consistent with the hypotheses that the vPFC is part of a circuit involved in non-spatial auditory processing and that the vPFC plays a functional role in non-spatial auditory cognition.

The role of innate immunity and macrophage recruitment to the inner ear after hair cell injury is a subject where little is known. In this paper, we demonstrate recruitment of monocytes and macrophages to the inner ear after kanamycin. We also examined the effect of fractalkine receptor (CX3CR1) deletion in kanamycin ototoxicity. We observed more functional and structural damage in CX3CR1 null mice compared to wild-type and heterozygous littermates. In order to determine if increased susceptibility to kanamycin resulted from CX3CR1 deletion from cochlear leukocytes, we created bone marrow chimeras by transplanting CX3CR1-null bone marrow into wild-type mice whose native bone marrow was ablated by lethal irradiation. These mice were then treated with kanamycin sulfate. Auditory brainstem responses (ABR), hair cell counts, and numbers of macrophages recruited to the cochlea were recorded in irradiated mice that received either wild-type, CX3CR1 heterozygous, or CX3CR1 knockout bone marrow. A strong correlation was present between numbers of macrophages and hair cell death in recipients transplanted with CX3CR1 null marrow. No correlation between macrophage number and hair cell loss was present in mice transplanted with wild-type or CX3CR1 heterozygous marrow. We suggest that CX3CR1 plays a role in modulating the detrimental effects of cochlear macrophages after kanamycin ototoxicity. Our data point to the possibility that CX3CR1-deficient cochlear macrophages exacerbate kanamycin ototoxicity while CX3CR1-expressing monocytes do not.

Adaptive behavior requires that animals integrate current and past information with their decision-making. One important type of information is auditory-communication signals (i.e., species-specific vocalizations). Here, we tested how rhesus monkeys incorporate the opportunity to listen to different species-specific vocalizations into their decision-making processes. In particular, we tested how monkeys value these vocalizations relative to the opportunity to get a juice reward. To test this hypothesis, monkeys chose one of two targets to get a varying juice reward; at one of those targets, in addition to the juice reward, a vocalization was presented. By titrating the juice amounts at the two targets, we quantified the relationship between the monkeys' juice choices relative to the opportunity to listen to a vocalization. We found that, rhesus were not willing to give up a large juice reward to listen to vocalizations indicating that, relative to a juice reward, listening to vocalizations has a low value.

Responses to tones with frequency < or = 5 kHz were recorded from auditory nerve fibers (ANFs) of anesthetized chinchillas. With increasing stimulus level, discharge rate-frequency functions shift toward higher and lower frequencies, respectively, for ANFs with characteristic frequencies (CFs) lower and higher than approximately 0.9 kHz. With increasing frequency separation from CF, rate-level functions are less steep and/or saturate at lower rates than at CF, indicating a CF-specific nonlinearity. The strength of phase locking has lower high-frequency cutoffs for CFs >4 kHz than for CFs < 3 kHz. Phase-frequency functions of ANFs with CFs lower and higher than approximately 0.9 kHz have inflections, respectively, at frequencies higher and lower than CF. For CFs >2 kHz, the inflections coincide with the tip-tail transitions of threshold tuning curves. ANF responses to CF tones exhibit cumulative phase lags of 1.5 periods for CFs 0.7-3 kHz and lesser amounts for lower CFs. With increases of stimulus level, responses increasingly lag (lead) lower-level responses at frequencies lower (higher) than CF, so that group delays are maximal at, or slightly above, CF. The CF-specific magnitude and phase nonlinearities of ANFs with CFs < 2.5 kHz span their entire response bandwidths. Several properties of ANFs undergo sharp transitions in the cochlear region with CFs 2-5 kHz. Overall, the responses of chinchilla ANFs resemble those in other mammalian species but contrast with available measurements of apical cochlear vibrations in chinchilla, implying that either the latter are flawed or that a nonlinear "second filter" is interposed between vibrations and ANF excitation.

A form of processed speech is described that is highly discriminable in a closed-set identification format. The processing renders speech into a set of sinusoidal pulses played synchronously across frequency. The processing and results from several experiments are described. The number and width of frequency analysis channels and tone-pulse duration were variables. In one condition, various proportions of the tones were randomly removed. The processed speech was remarkably resilient to these manipulations. This type of speech may be useful for examining multitalker listening situations in which a high degree of stimulus control is required.

A key function of the auditory system is to provide reliable information about the location of sound sources. Here, we describe how sound location is represented by synaptic input arriving onto pyramidal cells within auditory cortex by combining free-field acoustic stimulation in the frontal azimuthal plane with in vivo whole-cell recordings. We found that subthreshold activity was panoramic in that EPSPs could be evoked from all locations in all cells. Regardless of the sound location that evoked the largest EPSP, we observed a slowing in the EPSP slope along the contralateral–ipsilateral plane that was reflected in a temporal sequence of peak EPSP times. Contralateral sounds evoked EPSPs with earlier peak times and consequently generated action potential firing with shorter latencies than ipsilateral sounds. Thus, whereas spiking probability reflected the region of space evoking the largest EPSP, across the population, synaptic inputs enforced a gradient of spike latency and precision along the horizontal axis. Therefore, within auditory cortex and regardless of preferred location, the time window of synaptic integration reflects sound source location and ensures that spatial acoustic information is represented by relative timings of pyramidal cell output.

The auditory cortex of the cat is composed of 13 distinct fields that have been defined on the basis of anatomy, physiology, and behavior. Although an anatomically based hierarchical processing scheme has been proposed in auditory cortex, few functional studies have examined how these areas influence one another. The purpose of the present study was to examine the bidirectional processing contributions between primary auditory cortex (A1) and the nonprimary posterior auditory field (PAF). Multiunit acute recording techniques in eight mature cats were used to measure neuronal responses to tonal stimuli in A1 or PAF while synaptic activity from PAF or A1 was suppressed with reversible cooling deactivation techniques. Specifically, in four animals, electrophysiological recordings in A1 were conducted before, during, and after deactivation of PAF. Similarly, in the other four animals, PAF activity was measured before, during, and after deactivation of A1. The characteristic frequency, bandwidth, and neuronal threshold were calculated at each receptive field collected and the response strength and response latency measures were calculated from cumulative peristimulus time histograms. Two major changes in PAF response properties were observed during A1 deactivation: a decrease in response strength and a reduction in receptive field bandwidths. In comparison, we did not identify any significant changes in A1 neuronal responses during deactivation of PAF neurons. These findings support proposed models of hierarchal processing in cat auditory cortex.

Overexposure to intense sound can cause temporary or permanent hearing loss. Postexposure recovery of threshold sensitivity has been assumed to indicate reversal of damage to delicate mechano-sensory and neural structures of the inner ear and no persistent or delayed consequences for auditory function. Here, we show, using cochlear functional assays and confocal imaging of the inner ear in mouse, that acoustic overexposures causing moderate, but completely reversible, threshold elevation leave cochlear sensory cells intact, but cause acute loss of afferent nerve terminals and delayed degeneration of the cochlear nerve. Results suggest that noise-induced damage to the ear has progressive consequences that are considerably more widespread than are revealed by conventional threshold testing. This primary neurodegeneration should add to difficulties hearing in noisy environments, and could contribute to tinnitus, hyperacusis, and other perceptual anomalies commonly associated with inner ear damage.

Previous studies have shown that residual acoustic hearing supplements cochlear implant function to improve speech recognition in noise as well as perception of music. The current study had two primary objectives. First, we sought to determine how cochlear implantation and electrical stimulation over a time period of 14 to 21 months influence cochlear structures such as hair cells and spiral ganglion neurons. Second, we sought to investigate whether the structures that provide acoustic hearing also affect the perception of electrical stimulation. We compared psychophysical responses to cochlear implant stimulation in two groups of adult guinea pigs. Group I (11 animals) received a cochlear implant in a previously untreated ear, while group II (ten animals) received a cochlear implant in an ear that had been previously infused with neomycin to destroy hearing. Psychophysical thresholds were measured in response to pulse-train and sinusoidal stimuli. Histological analysis of all group I animals and a subset of group II animals was performed. Nine of the 11 group I animals showed survival of the organ of Corti and spiral ganglion neurons adjacent to the electrode array. All group I animals showed survival of these elements in regions apical to the electrode array. Group II animals that were examined histologically showed complete loss of the organ of Corti in regions adjacent and apical to the electrode array and severe spiral ganglion neuron loss, consistent with previous reports for neomycin-treated ears. Behaviorally, group II animals had significantly lower thresholds than group I animals in response to 100 Hz sinusoidal stimuli. However, group I animals had significantly lower thresholds than group II animals in response to pulse-train stimuli (0.02 ms/phase; 156 to 5,000 pps). Additionally, the two groups showed distinct threshold versus pulse rate functions. We hypothesize that the differences in detection thresholds between groups are caused by the electrical activation of the hair cells in group I animals and/or differences between groups in the condition of the spiral ganglion neurons.

Training-induced improvements on perceptual skills can be attributed to at least two learning types: learning of general aspects of the trained condition (conceptual learning) and learning of specific feature values of the stimulus used in training (stimulus learning). Here we asked whether conceptual and stimulus learning on interaural time difference (ITD) discrimination emerge along different time courses. Conceptual learning was clearly evident 10 h after training, when performance on a target ITD condition was equivalent following training on that condition or on a non-target condition differing only in the stimulus, and was better in both cases than immediately after training. In contrast, stimulus learning emerged 24 h after training. At that time, performance on the target ITD condition was better following target- than non-target training, due to a worsening in performance between 10 and 24 h after non-target training rather than from additional improvements over this time period after target training. Training amount influenced performance immediately, but not 10 or 24 h, after training. Thus, conceptual learning emerged before stimulus learning, and each manifested through different improvement trajectories many hours after training. These results suggest that on ITD discrimination, conceptual learning is consolidated earlier, and with different behavioral consequences, than stimulus learning.

Background: When sound arrives at the eardrum it has already been filtered by the body, head, and outer ear. This process is mathematically described by the head-related transfer functions (HRTFs), which are characteristic for the spatial position of a sound source and for the individual ear. HRTFs in the barn owl (Tyto alba) are also shaped by the facial ruff, a specialization that alters interaural time differences (ITD), interaural intensity differences (ILD), and the frequency spectrum of the incoming sound to improve sound localization. Here we created novel stimuli to simulate the removal of the barn owl's ruff in a virtual acoustic environment, thus creating a situation similar to passive listening in other animals, and used these stimuli in behavioral tests. Methodology/principal findings: HRTFs were recorded from an owl before and after removal of the ruff feathers. Normal and ruff-removed conditions were created by filtering broadband noise with the HRTFs. Under normal virtual conditions, no differences in azimuthal head-turning behavior between individualized and non-individualized HRTFs were observed. The owls were able to respond differently to stimuli from the back than to stimuli from the front having the same ITD. By contrast, such a discrimination was not possible after the virtual removal of the ruff. Elevational head-turn angles were (slightly) smaller with non-individualized than with individualized HRTFs. The removal of the ruff resulted in a large decrease in elevational head-turning amplitudes. Conclusions/significance: The facial ruff a) improves azimuthal sound localization by increasing the ITD range and b) improves elevational sound localization in the frontal field by introducing a shift of iso-ILD lines out of the midsagittal plane, which causes ILDs to increase with increasing stimulus elevation. The changes at the behavioral level could be related to the changes in the binaural physical parameters that occurred after the virtual removal of the ruff. These data provide new insights into the function of external hearing structures and open up the possibility to apply the results on autonomous agents, creation of virtual auditory environments for humans, or in hearing aids.

The inferior colliculus (IC) is unique, having both glutamatergic and GABAergic projections ascending to the thalamus. Although subpopulations of GABAergic neurons in the IC have been proposed, criteria to distinguish them have been elusive and specific types have not been associated with specific neural circuits. Recently, the largest IC neurons were found to be recipients of somatic terminals containing vesicular glutamate transporter 2 (VGLUT2). Here, we show with electron microscopy that VGLUT2-positive (VGLUT2 + ) axonal terminals make axosomatic synapses on IC neurons. These terminals contain only VGLUT2 even though others in the IC have VGLUT1 or both VGLUT1 and 2. We demonstrate that there are two types of GABAergic neurons: larger neurons with VGLUT2 + axosomatic endings and smaller neurons without such endings. Both types are present in all subdivisions of the IC, but larger GABAergic neurons with VGLUT2 + axosomatic terminals are most prevalent in the central nucleus. The GABAergic tectothalamic neurons consist almost entirely of the larger cells surrounded by VGLUT2 + axosomatic endings. Thus, two types of GABAergic neurons in the IC are defined by different synaptic organization and neuronal connections. Larger tectothalamic GABAergic neurons are covered with glutamatergic axosomatic synapses that could allow them to fire rapidly and overcome a slow membrane time constant; their axons may be the largest in the brachium of the IC. Thus, large GABAergic neurons could deliver IPSPs to the medial geniculate body before EPSPs from glutamatergic IC neurons firing simultaneously.

Changes in the sensory environment are good indicators for behaviorally relevant events and strong triggers for the reallocation of attention. In the auditory domain, violations of a pattern of repetitive stimuli precipitate in the event-related potentials as mismatch negativity (MMN). Stimulus-specific adaptation (SSA) of single neurons in the auditory cortex has been proposed to be the cellular substrate of MMN (Nelken and Ulanovsky, 2007). However, until now, the existence of SSA in the awake auditory cortex has not been shown. In the present study, we recorded single and multiunits in parallel with evoked local field potentials ( e LFPs) in the primary auditory cortex of the awake rat. Both neurons and e LFPs in the awake animal adapted in a stimulus-specific manner, and SSA was controlled by stimulus probability and frequency separation. SSA of isolated units was significant during the first stimulus-evoked “on” response but not in the following inhibition and rebound of activity. The e LFPs exhibited SSA in the first negative deflection and, to a lesser degree, in a slower positive deflection but no MMN. Spike adaptation correlated closely with adaptation of the fast negative deflection but not the positive deflection. Therefore, we conclude that single neurons in the auditory cortex of the awake rat adapt in a stimulus-specific manner and contribute to corresponding changes in e LFP but do not generate a late deviant response component directly equivalent to the human MMN. Nevertheless, the described effect may reflect a certain part of the process needed for sound discrimination.

Traditionally, the calyx of Held synapse is viewed as a highly reliable relay in the sound localization circuit of the auditory brainstem, with every presynaptic action potential triggering a postsynaptic action potential in vivo . However, this view is at odds with slice recordings that report large short-term depression (STD). To investigate the reliability and precision of this synapse, we compared slice and in vivo recordings from medial nucleus of the trapezoid body neurons of young adult mice. We show that the extracellularly recorded complex waveform can be used to estimate both presynaptic release and postsynaptic excitability. Whereas under standard slice conditions the synapse underwent large STD, both extracellular and whole-cell recordings indicated that in vivo the size of the EPSPs was independent of recent history. The estimated quantal content was typically <20 in vivo , much lower than in the resting synapse under standard slice conditions. However, due to the large quantal size and summation of EPSPs, the safety factor of this synapse was generally still sufficiently large and postsynaptic failures were observed only infrequently in vivo . When present, failures were typically due to stochastic fluctuations in EPSP size or postsynaptic spike depression. In vivo , the calyx of Held synapse thus functions as a tonic synapse. The price it pays for its low release probability is an increase in jitter and synaptic latency and occasional postsynaptic failures.

Spontaneous activity plays an important role in the function of neural circuits. Although many similarities between spontaneous and sensory-evoked neocortical activity have been reported, little is known about consistent differences between them. Here, using simultaneously recorded cortical populations and morphologically identified pyramidal cells, we compare the laminar structure of spontaneous and sensory-evoked population activity in rat auditory cortex. Spontaneous and evoked patterns both exhibited sparse, spatially localized activity in layer 2/3 pyramidal cells, with densely distributed activity in larger layer 5 pyramidal cells and putative interneurons. However, the propagation of spontaneous and evoked activity differed, with spontaneous activity spreading upward from deep layers and slowly across columns, but sensory responses initiating in presumptive thalamorecipient layers, spreading rapidly across columns. The similarity of sparseness patterns for both neural events and distinct spread of activity may reflect similarity of local processing and differences in the flow of information through cortical circuits, respectively.

Budgerigars and zebra finches were tested, using operant conditioning techniques, on their ability to identify a zebra finch song in the presence of a background masker emitted from either the same or a different location as the signal. Identification thresholds were obtained for three masker types differing in their spectrotemporal characteristics (noise, modulated noise, and a song chorus). Both bird species exhibited similar amounts of spatial unmasking across the three masker types. The amount of unmasking was greater when the masker was played continuously compared to when the target and masker were presented simultaneously. These results suggest that spatial factors are important for birds in the identification of natural signals in noisy environments.

Some past studies suggest that when sound elements are heard as one object, the spatial cues in the component elements are integrated to determine perceived location, and that this integration is reduced when the elements are perceived in separate objects. The current study explored how object localization depends on the spatial, spectral, and temporal configurations of sound elements in an auditory scene. Localization results are interpreted in light of results from a series of previous experiments studying perceptual grouping of the same stimuli, e.g., Shinn-Cunningham et al. [Proc. Natl. Acad. Sci. U.S.A. 104, 12223–12227 (2007)]. The current results suggest that the integration (pulling) of spatial information across spectrally interleaved elements is obligatory when these elements are simultaneous, even though past results show that these simultaneous sound elements are not grouped strongly into a single perceptual object. In contrast, perceptually distinct objects repel (push) each other spatially with a strength that decreases as the temporal separation between competing objects increases. These results show that the perceived location of an attended object is not easily predicted by knowledge of how sound elements contribute to the perceived spectro-temporal content of that object.

Neural representations of even temporally unstructured stimuli can show complex temporal dynamics. In many systems, neuronal population codes show ‘progressive differentiation’, whereby population responses to different stimuli grow further apart during a stimulus presentation. Here we analysed the response of auditory cortical populations in rats to extended tones. At onset (up to 300 ms), tone responses involved strong excitation of a large number of neurons; during sustained responses (after 500 ms) overall firing rate decreased, but most cells still showed statistically significant rate modulation. Population vector trajectories evoked by different tone frequencies expanded rapidly along an initially similar trajectory in the first tens of milliseconds after tone onset, later diverging to smaller amplitude fixed points corresponding to sustained responses. The angular difference between onset and sustained responses to the same tone was greater than between different tones in the same stimulus epoch. No clear orthogonalization of responses was found with time, and predictability of the stimulus from population activity also decreased during this period compared with onset. The question of whether population activity grew more or less sparse with time depended on the precise mathematical sense given to this term. We conclude that auditory cortical population responses to tones differ from those reported in many other systems, with progressive differentiation not seen for sustained stimuli. Sustained acoustic stimuli are typically not behaviorally salient: we hypothesize that the dynamics we observe may instead allow an animal to maintain a representation of such sounds, at low energetic cost.

Acoustic processing requires integration over time. We have used in vivo intracellular recording to measure neuronal integration times in anesthetized rats. Using natural sounds and other stimuli, we found that synaptic inputs to auditory cortical neurons showed a rather long context dependence, up to ≥4 s (τ ∼ 1 s), even though sound-evoked excitatory and inhibitory conductances per se rarely lasted ≳100 ms. Thalamic neurons showed only a much faster form of adaptation with a decay constant τ <100 ms, indicating that the long-lasting form originated from presynaptic mechanisms in the cortex, such as synaptic depression. Restricting knowledge of the stimulus history to only a few hundred milliseconds reduced the predictable response component to about half that of the optimal infinite-history model. Our results demonstrate the importance of long-range temporal effects in auditory cortex and suggest a potential neural substrate for auditory processing that requires integration over timescales of seconds or longer, such as stream segregation.