Auditory Research publications

Auditory information can reach the lateral nucleus of the amygdala (LA) through a monosynaptic thalamic projection or a polysynaptic cortical route. The polymodal input from the perirhinal cortex (PR) is a major informational gateway to the LA and nearby structures. Pretraining PR lesions impair fear conditioning to a context, but there have been no reports that they cause deficits in delay conditioning to an auditory cue. The direct subcortical projection to the LA seems sufficient to support delay conditioning to a tone conditional stimulus (CS). We examined the effect of PR lesions on delay conditioning to two different tone conditional stimuli (4 and 22 kHz tones; both 10 sec duration) and two different rat ultrasonic vocalization (USV) conditional stimuli (10 sec of “22 kHz USVs”). The two USV conditional stimuli were multi-call segments that were recorded (digitized at 100 kHz) from two different rats. One USV CS was a continuous sequence of eight calls, and the other was a portion of a continuous sequence of six calls. PR lesions significantly impaired conditioning to both USV conditional stimuli and to the training context but had no significant effect on conditioning to either tone CS. The role of PR in fear conditioning appears not to be determined by whether the conditional stimuli serve as contexts or cues, but instead by the nature or complexity of the stimuli or stimulus configurations. These cue-specific effects of PR lesions are suggested to reflect differences in the stimulus features that are encoded in the two CS pathways to the LA.

This study examined the interactions between electrical stimuli presented through two channels of a cochlear implant. Experiments were conducted in anesthetized guinea pigs. Multiunit spike activity recorded from the auditory cortex reflected the cumulative effects of electric field interactions in the cochlea as well as any neural interactions along the ascending auditory pathway. The cochlea was stimulated electrically through a 6-electrode intracochlear array. The stimulus on each channel was a single 80- micro s/phase biphasic pulse. Channel interactions were quantified as changes in the thresholds for elevation of cortical spike rates. Experimental parameters were interchannel temporal offset (0 to +/-2000 micro s), interelectrode cochlear spacing (1.5 or 2.25 mm), electrode configuration (monopolar, bipolar, or tripolar), and relative polarity between channels (same or inverted). In most conditions, presentation of a subthreshold pulse on one channel reduced the threshold for a pulse on a second channel. Threshold shifts were greatest for simultaneous pulses, but appreciable threshold reductions could persist for temporal offsets up to 640 micro s. Channel interactions varied strongly with electrode configuration: threshold shifts increased in magnitude in the order tripolar, bipolar, monopolar. Channel interactions were greater for closer electrode spacing. The results have implications for design of speech processors for cochlear implants.

The contention that normally binaural listeners can localize sound under monaural conditions has been challenged by Wightman and Kistler (J. Acoust. Soc. Am. 101:1050-1063, 1997), who found that listeners are almost completely unable to localize virtual sources of sound when sound is presented to only one ear. Wightman and Kistler's results raise the question of whether monaural spectral cues are used by listeners to localize sound under binaural conditions. We have examined the possibility that monaural spectral cues provide useful information regarding sound-source elevation and front-back hemifield when interaural time differences are available to specify sound-source lateral angle. The accuracy with which elevation and front-back hemifield could be determined was compared between a monaural condition and a binaural condition in which a wide-band signal was presented to the near ear and a version of the signal that had been lowpass-filtered at 2.5 kHz was presented to the far ear. It was found that accuracy was substantially greater in the latter condition, suggesting that information regarding sound-source lateral angle is required for monaural spectral cues to elevation and front-back hemifield to be correctly interpreted.

How do cortical neurons represent the acoustic environment? This question is often addressed by probing with simple stimuli such as clicks or tone pips. Such stimuli have the advantage of yielding easily interpreted answers, but have the disadvantage that they may fail to uncover complex or higher-order neuronal response properties. Here, we adopt an alternative approach, probing neuronal responses with complex acoustic stimuli, including animal vocalizations. We used in vivo whole-cell methods in the rat auditory cortex to record subthreshold membrane potential fluctuations elicited by these stimuli. Most neurons responded robustly and reliably to the complex stimuli in our ensemble. Using regularization techniques, we estimated the linear component, the spectrotemporal receptive field (STRF), of the transformation from the sound (as represented by its time-varying spectrogram) to the membrane potential of the neuron. We find that the STRF has a rich dynamical structure, including excitatory regions positioned in general accord with the prediction of the classical tuning curve. However, whereas the STRF successfully predicts the responses to some of the natural stimuli, it surprisingly fails completely to predict the responses to others; on average, only 11% of the response power could be predicted by the STRF. Therefore, most of the response of the neuron cannot be predicted by the linear component, although the response is deterministically related to the stimulus. Analysis of the systematic errors of the STRF model shows that this failure cannot be attributed to simple nonlinearities such as adaptation to mean intensity, rectification, or saturation. Rather, the highly nonlinear response properties of auditory cortical neurons must be attributable to nonlinear interactions between sound frequencies and time-varying properties of the neural encoder.

Focal excess sensory stimulation evokes reorganization of a sensory system. It is usually an expansion of the neural representation of that stimulus resulting from the shifts of the tuning curves (receptive fields) of neurons toward those of the stimulated neurons. The auditory cortex of the mustached bat has an area that is highly specialized for the processing of target-distance information carried by echo delays. In this area, however, reorganization is due to shifts of the delay-tuning curves of neurons away from those of the stimulated cortical neurons. Elimination of inhibition in the target-distance processing area in the auditory cortex by a drug reverses the direction of the shifts in neural tuning curves. Therefore, such unique reorganization in the time domain is due to strong lateral inhibition in the highly specialized area of the auditory cortex.

The term informational masking has traditionally been used to refer to elevations in signal threshold resulting from masker uncertainty. In the present study, the method of constant stimuli was used to obtain complete psychometric functions (PFs) from 44 normal-hearing listeners in conditions known to produce varying amounts of informational masking. The listener’s task was to detect a pure-tone signal in the presence of a broadband noise masker (low masker uncertainty) and in the presence of multitone maskers with frequencies and amplitudes that varied at random from one presentation to the next (high masker uncertainty). Relative to the broadband noise condition, significant reductions were observed in both the slope and the upper asymptote of the PF for multitone maskers producing large amounts of informational masking. Slope was affected more for some listeners and conditions while asymptote was affected more for others; consequently, neither parameter alone was highly predictive of individual thresholds or the amount of informational masking. Mean slopes and asymptotes varied nonmonotonically with the number of masker components in a manner similar to mean thresholds, particularly when the estimated effect of energetic masking on thresholds was subtracted out. As in past studies, the threshold data were well described by a model in which trial-by-trial judgments are based on a weighted sum of levels in dB at the output of independent auditory filters. The psychometric data, however, complicated the model’s interpretation in two ways: First, they suggested that, depending on the listener and condition, the weights can either reflect a fixed influence of masker components on each trial or the effect of occasionally mistaking a masker component for the signal from trial to trial. Second, they indicated that in either case the variance of the underlying decision variable as estimated from PF slope is not by itself great enough to account for the observed changes in informational masking.

The strength of the acoustic startle reflex (ASR) as a function of age was studied in adult C57BL/6J and CBA/CaJ mice, because altered ASR levels are a potential behavioral consequence of the neural reorganization that accompanies the early-onset hearing loss of the C57BL, in contrast to the normal-hearing CBA. For C57BL mice at 14-36 weeks of age, compared with 7-week-old mice, high-frequency thresholds measured with the auditory brainstem response (ABR) were less sensitive by about 25-30 dB while the hearing loss at low frequencies was 10-15 dB, but by 60 weeks losses of 45-50 dB were present across the entire spectrum. Their ASR amplitudes for 16 kHz tone pips were highest at 7 weeks and then declined with age, but, for 4 kHz tones the ASR increased in strength at 18 weeks and beyond to levels above that of the younger mice. This hyperreactivity persisted even in 60-week-old mice. The ASR for 16 kHz stimuli was positively correlated with hearing sensitivity, but the ASR for 4 kHz stimuli was positively correlated with hearing loss for mice that were 18-36 weeks of age. Furthermore, ASR amplitudes for 4 kHz stimuli were positively correlated with the 16 kHz ASR in young C57BL mice but negatively correlated in older mice. There were no similar ASR or ABR changes in adult CBA mice through 19 weeks of age. Correlations between ASR and ABR scores were always weakly positive, and correlations between 4 kHz and 16 kHz ASR amplitudes were always strongly positive. The ASR data in older C57BL mice with hearing loss are consistent with reports describing their increased neural representation of low-frequency sounds and reinforce the value of this strain for studying the functional consequences that accompany age-related cochlear degeneration.

The present study aimed to examine the effect of noise on vowel-like suprathreshold discrimination in cochlear-implant listeners. The task was to detect an increment in level at the middle harmonic (400 Hz) in the background of a seven-harmonic complex from 100 to 700 Hz in 100-Hz steps. The task was performed in the absence (control) and presence of a white noise presented over a 20-35-dB range from inaudible to loud. The present result shows that discrimination of suprathreshold harmonic stimuli was significantly enhanced, particularly at the soft signal level, with suprathreshold noise. This result suggests that tuning of the noise level is required to optimize performance of different tasks in cochlear implants.

The hedgehog tenrec, Echinops telfairi, has certain basal mammalian features, like a cloaca and a sparsely differentiated brain with smooth cerebral hemispheres. The peripheral auditory capabilities of this species were investigated by means of distortion product otoacoustic emissions (DPOAE). For comparison, we determined auditory evoked potentials (AEP) in the inferior colliculus and the auditory cortex. Both methods show that the auditory range of E. telfairi extends well into ultrasonic frequencies, with a region of highest sensitivity at around 16 kHz. The total auditory range spans about 4 octaves at 40 dB SPL. The low-frequency limit of auditory processing is found at frequencies of about 2-3 kHz. The DPOAE and the AEP thresholds of E. telfairi do not run fully parallel in the high-frequency range. For a threshold value of 40 dB SPL, cochlear mechanical thresholds as measured with DPOAE extend up to 50 kHz, whereas neuronal thresholds reach the high-frequency limit at about 30 kHz. Frequency tuning, as assessed from DPOAE suppression tuning curves, was low to moderate with Q(10 dB) values ranging from 1.7 to 8. The lack of discontinuity in the group delay (derived from DPOAE measurements) reveals that cochlear frequency representation is tonotopic without any region of specialized mechanical tuning.

The voltage-gated potassium (Kv) channel subunit Kv1.1, encoded by the Kcna1 gene, is expressed strongly in the ventral cochlear nucleus (VCN) and the medial nucleus of the trapezoid body (MNTB) of the auditory pathway. To examine the contribution of the Kv1.1 subunit to the processing of auditory information, in vivo single-unit recordings were made from VCN neurons (bushy cells), axonal endings of bushy cells at MNTB cells (calyces of Held), and MNTB neurons of Kcna1 -null (-/-) mice and littermate control (+/+) mice. Thresholds and spontaneous firing rates of VCN and MNTB neurons were not different between genotypes. At higher sound intensities, however, evoked firing rates of VCN and MNTB neurons were significantly lower in -/- mice than +/+ mice. The SD of the first-spike latency (jitter) was increased in VCN neurons, calyces, and MNTB neurons of -/- mice compared with +/+ controls. Comparison along the ascending pathway suggests that the increased jitter found in -/- MNTB responses arises mostly in the axons of VCN bushy cells and/or their calyceal terminals rather than in the MNTB neurons themselves. At high rates of sinusoidal amplitude modulations, -/- MNTB neurons maintained high vector strength values but discharged on significantly fewer cycles of the amplitude-modulated stimulus than +/+ MNTB neurons. These results indicate that in Kcna1 -null mice the absence of the Kv1.1 subunit results in a loss of temporal fidelity (increased jitter) and the failure to follow high-frequency amplitude-modulated sound stimulation in vivo .

Bilateral amygdala (AM) lesions prevent the acquisition of fear-related conditional responses (CRs) in rats, a result that is most commonly concluded to reflect a learning or memory deficit. An alternative hypothesis is that AM-lesioned animals fail to acquire certain fear CRs simply because they cannot perform these behaviors. This performance-deficit hypothesis is usually invoked in regard to studies in which the CR is freezing, the most commonly measured behavior. Here we explore this interpretation by measuring two different behaviors [freezing and 22 kHz ultrasonic vocalization (USV)] elicited under three conditions (during context conditioning, during subsequent retention testing, and after ejaculation) in experimental rats [that received electrolytic lesions of the central nucleus of the amygdala (ACe)] and control animals (that received a sham operation). If ACe damage produces a discrete motor deficit that specifically renders the animal unable to remain immobile, then freezing should be blocked or impaired when elicited under all three conditions, whereas USV should be spared. Alternatively, if ACe damage selectively interferes with CR formation, maintenance, or expression, then both freezing and USV should be blocked or impaired when elicited as CRs during acquisition and retention testing but spared when evoked as unconditional responses (URs) to ejaculation. ACe damage blocked or severely impaired both freezing and USV elicited as CRs but had no effect on either behavior elicited as URs. We reject the motor-deficit hypothesis and discuss some viable alternatives.

We evaluated the spatial selectivity of auditory cortical neurons in awake cats. Single- and multiunit activity was recorded in primary auditory cortex as the animals performed a nonspatial auditory discrimination or sat idly. Their heads were unrestrained, and head position was tracked. Broadband sounds were delivered from locations throughout 360° on the horizontal plane, and source locations were expressed in head-centered coordinates. As in anesthetized animals, the firing rates of most units were modulated by sound location, and most units responded best to sounds in the contralateral hemifield. Tuning was sharper than in anesthetized cats, in part because of suppression at nonoptimal locations. Nonetheless, spatial receptive fields typically spanned 150-180°. Units exhibited diverse temporal response patterns that often depended on sound location. An information-theoretic analysis showed that information transmission was reduced by ∼10% when the precision of spike timing was disrupted by 16-32 msec, and by ∼50% when all location-related variation of spike timing was removed. Spikes occurring within 60 msec of stimulus onset transmitted the most location-related information, but later spikes also carried information. The amount of information transmitted by ensembles of units increased with the number of units, indicating some degree of mutual independence in the spatial information transmitted by various units. Spatial tuning and information transmission were changed little by an increase in sound level of 20-30 dB. For the vast majority of units, receptive fields showed no significant change with the cat's head position or level of participation in the auditory task.

The Zwicker tone (ZT) is defined as an auditory negative afterimage, perceived after the presentation of an appropriate inducer. Typically, a notched noise (NN) with a notch width of 1/2 octave induces a ZT with a pitch falling in the frequency range of the notch. The aim of the present study was to find potential neural correlates of the ZT in the primary auditory cortex of ketamine-anesthetized cats. Responses of multiunits were recorded simultaneously with two 8-electrode arrays during 1 s and over 2 s after the presentation of a white noise (WN) and three NNs differing by the width of the notch, namely, 1/3 octave (NN1), 1/2 octave (NN2), and 2/3 octave (NN3). Both firing rate (FR) and peak cross-correlation coefficient (p) were evaluated for time windows of 500 ms. The cortical units were grouped according to whether their characteristic frequency (CF) was inside ("In" neurons) or outside ("Out" neurons) a 1-octave-wide frequency band centered on the notch center frequency. The ratios between the FRs and the rhos for each NN and the WN condition and for each group of neurons were then statistically evaluated. The ratios of FRs were significantly increased during and after the presentation of the NN for the "In" neurons. In contrast, the changes for the t" neurons were small and most often insignificant. The ratios of the p values differed significantly from 1 in the "In-In" and "In-Out" groups during stimulation as well as after it. We also found that the ps of "Out" neurons were dependent on the type of NN. Potentially, a combination of increased p and increased FR might be a neurophysiological correlate of the ZT.

Neurons are often assumed to operate in a highly unreliable manner: a neuron can signal the same stimulus with a variable number of action potentials. However, much of the experimental evidence supporting this view was obtained in the visual cortex. We have, therefore, assessed trial-to-trial variability in the auditory cortex of the rat. To ensure single-unit isolation, we used cell-attached recording. Tone-evoked responses were usually transient, often consisting of, on average, only a single spike per stimulus. Surprisingly, the majority of responses were not just transient, but were also binary, consisting of 0 or 1 action potentials, but not more, in response to each stimulus; several dramatic examples consisted of exactly one spike on 100% of trials, with no trial-to-trial variability in spike count. The variability of such binary responses differs from comparably transient responses recorded in visual cortical areas such as area MT, and represent the lowest trial-to-trial variability mathematically possible for responses of a given firing rate. Our study thus establishes for the first time that transient responses in auditory cortex can be described as a binary process, rather than as a highly variable Poisson process. These results demonstrate that cortical architecture can support a more precise control of spike number than was previously recognized, and they suggest a re-evaluation of models of cortical processing that assume noisiness to be an inevitable feature of cortical codes.

The prevailing hierarchical model of cortical sensory processing holds that early processing is specific to individual modalities and that combination of information from different modalities is deferred until higher-order stages of processing. In this paper, we present physiological evidence of multisensory convergence at an early stage of cortical auditory processing. We used multi-neuron cluster recordings, along with a limited sample of single-unit recordings, to determine whether neurons in the macaque auditory cortex respond to cutaneous stimulation. We found coextensive cutaneous and auditory responses in caudomedial auditory cortex, an area lying adjacent to A1, and at the second stage of the auditory cortical hierarchy. Somatosensory-auditory convergence in auditory cortex may underlie effects observed in human studies. Convergence of inputs from different sensory modalities at very early stages of cortical sensory processing has important implications for both our developing understanding of multisensory processing and established views of unisensory processing.

Thyroid hormone action is mediated by thyroid hormone receptors (TRs), which are members of the nuclear hormone receptor superfamily. DNA-binding is presumed to be essential for all nuclear actions of thyroid hormone. To test this hypothesis in vivo, the DNA-binding domain of TR-beta was mutated within its P-box (GS mutant) using gene targeting techniques. This mutation in vitro completely abolishes TR-beta DNA-binding, while preserving ligand (T3) and cofactor interactions with the receptor. Homozygous mutant (TR-betaGS/GS) mice displayed abnormal T3 regulation of the hypothalamic-pituitary-thyroid axis and retina identical to abnormalities previously observed in TR-beta KO (TR-beta-/-) mice. However, TR-betaGS/GS mutant mice maintained normal hearing at certain frequencies and did not display significant outer hair cell loss, in contrast to TR-beta-/- mice. DNA-binding, therefore, is essential for many functions of the TR, including retinal development and negative feedback regulation by thyroid hormone of the hypothalamic-pituitary-thyroid axis. Inner ear development, although not completely normal, can occur in the absence of TR DNA-binding, suggesting that an alternative and perhaps novel thyroid hormone-signaling pathway may mediate these effects.

Neurons in the medial superior olive encode interaural temporal disparity, and their receptive fields indicate the location of a sound source in the azimuthal plane. It is often assumed that the projections of these neurons transmit the receptive field information about azimuth from point to point, much like the projections of the retina to the brain transmit the position of a visual stimulus. Yet this assumption has never been verified. Here, we use physiological and anatomical methods to examine the projections of the medial superior olive to the inferior colliculus for evidence of a spatial topography that would support transmission of azimuthal receptive fields. The results show that this projection does not follow a simple point-to-point topographical map of receptive field location. Thus, the representation of sound location along the azimuth in the inferior colliculus most likely relies on a complex, nonlinear map.

Contrary to findings in subcortical auditory nuclei, auditory cortex neurons have traditionally been described as spiking only at the onsets of simple sounds such as pure tones or bandpass noise and to acoustic transients in complex sounds. Furthermore, primary auditory cortex (A1) has traditionally been described as mostly tone responsive and the lateral belt area of primates as mostly noise responsive. The present study was designed to unify the study of these two cortical areas using random spectrum stimuli (RSS), a new class of parametric, wideband, stationary acoustic stimuli. We found that 60% of all neurons encountered in A1 and the lateral belt of awake marmoset monkeys (Callithrix jacchus) showed significant changes in firing rates in response to RSS. Of these, 89% showed sustained spiking in response to one or more individual RSS, a substantially greater percentage than would be expected from traditional studies, indicating that RSS are well suited for studying these two cortical areas. When firing rates elicited by RSS were used to construct linear estimates of frequency tuning for these sustained responders, the shape of the estimate function remained relatively constant throughout the stimulus interval and across the stimulus properties of mean sound level, spectral density, and spectral contrast. This finding indicates that frequency tuning computed from RSS reflects a robust estimate of the actual tuning of a neuron. Use of this estimate to predict rate responses to other RSS, however, yielded poor results, implying that auditory cortex neurons integrate information across frequency nonlinearly. No systematic difference in prediction quality between A1 and the lateral belt could be detected.