Approche empirique pour déterminer les générateurs neurophysiologiques sous-jacents des potentiels évoqués auditifs engendrés par des sons de parole (Speech ABR)

Auditory evoked potentials to speech (Speech auditory brainstem response [Speech ABR]) are a non-invasive way to investigate neurophysiological activity, at the level of the brainstem. The Speech ABR precise neurophyiological generators remain poorly defined. However, latencies and low-pass spectrum both suggest that these generators might lie in the upper brainstem (roughly between the cochlear nucleus and the inferior colliculus). Having considered the particular functional pattern of cells along the auditory pathway, specific stimuli have been synthesized to make out the acoustic sensitivity of Speech ABR components. Accordingly, hypotheses have been made on the probable neurophysiological generators, most likely to have elicited both Speech ABR components: onset response and frequency following response. Speech ABR have been recorded to pure tones, harmonic complex tones, /ba/ and /pa/ syllables, and their analogues (calculated as a sum of five weighted sine waves at the formant frequencies and amplitudes, and modulated by the syllables temporal envelopes). In addition, the Auditory Image Model (Patterson et al., 1995 [17]), simulating the neural activity at the auditory periphery, i.e. inferior colliculus input, suggests that both analogues and syllables elicit the same amount of energy, in contrast to the recorded FFR. This contradiction means that the neurophysiological signal processing leading to FFR is made beyond auditory periphery. Indeed, FFR synchronisation on F0 seems to be the result of an overall processing of the whole stimulus spectrum. This behaviour reminds the functional characteristics of disc-shape cells in the inferior colliculus, as described in a previous study of physiological periodicity coding (Periodicity analysis network, Voutsas et al., 2005 [42]).     

Ontogenesis of the echolocation system in the rufous horseshoe bat,Rhinolophus rouxi (Audition and vocalization in early postnatal development)

1. The development of vocalization and hearing was studied in Sri Lankan horseshoe bats (Rhinolophus rouxi) during the first postnatal month. The young bats were caught in a nursing colony of rhinolophids in which birth took place within a two week period. 2. The new-born bats emitted isolation calls through the mouth. At the beginning these calls consisted of pure tones with frequencies below 10 kHz (Fig. 1). During the first postnatal week the call frequency increased to about 15 kHz, and the fundamental was augmented by two to four harmonics. No evoked potentials to pure tone stimuli could be elicited in the inferior colliculus of this age group, i.e., auditory processing at the midbrain level was not demonstrable. 3. Evoked potentials were first recorded in the second week, broadly tuned to 15-45 kHz, with a maximum sensitivity between 15-25 kHz. In the course of the second week, however, higher frequencies up to 60 kHz became progressively incorporated into the audiogram (Fig. 3). The fundamental frequency of the multiharmonic isolation calls, emitted strictly through the mouth, increased to about 20 kHz. 4. In the bats' third postnatal week an increased hearing sensitivity (auditory filter) emerged, sharply tuned at frequencies between 57 and 60 kHz (Fig. 4e). The same individuals were also the first to emit long constant frequency echolocation calls through the nostrils (Fig. 4c). The energy of the calls was arranged in harmonic frequency bands with the second harmonic exactly tuned to the auditory filter. These young bats continued to emit isolation calls through the mouth, which were, however, not harmonically related to the echolocation calls (Fig. 4b, d). 5. During the fourth week, both the auditory filter and the matched echolocation pulses (the second harmonic) shifted towards higher frequencies (Fig. 5). During the fifth week the fundamental frequency of the calls was progressively attenuated, and both the second harmonic of the pulses and the auditory filter reached the frequency range typical for adult bats of 73-78 kHz (Fig. 6). 6. The development of audition and vocalization is discussed with regard to possible interactions of both subsystems, and their incorporation into the active orientation system of echolocation.     

Serotonin modulates responses to species-specific vocalizations in the inferior colliculus

Neuromodulators such as serotonin are capable of altering the neural processing of stimuli across many sensory modalities. In the inferior colliculus, a major midbrain auditory gateway, serotonin alters the way that individual neurons respond to simple tone bursts and linear frequency modulated sweeps. The effects of serotonin are complex, and vary among neurons. How serotonin transforms the responses to spectrotemporally complex sounds of the type normally heard in natural settings has been poorly examined. To explore this issue further, the effects of iontophoretically applied serotonin on the responses of individual inferior colliculus neurons to a variety of recorded species-specific vocalizations were examined. These experiments were performed in the Mexican free-tailed bat, a species that uses a rich repertoire of vocalizations for the purposes of communication as well as echolocation. Serotonin frequently changed the number of recorded calls that were capable of evoking a response from individual neurons, sometimes increasing (15% of serotonin-responsive neurons), but usually decreasing (62% of serotonin-responsive neurons), this number. A functional consequence of these serotonin-evoked changes would be to change the population response to species-specific vocalizations.     

Discrimination of Ultrasonic Vocalizations by CBA/CaJ Mice (Mus musculus) Is Related to Spectrotemporal Dissimilarity of Vocalizations

The function of ultrasonic vocalizations (USVs) produced by mice (Mus musculus) is a topic of broad interest to many researchers. These USVs differ widely in spectrotemporal characteristics, suggesting different categories of vocalizations, although this has never been behaviorally demonstrated. Although electrophysiological studies indicate that neurons can discriminate among vocalizations at the level of the auditory midbrain, perceptual acuity for vocalizations has yet to be determined. Here, we trained CBA/CaJ mice using operant conditioning to discriminate between different vocalizations and between a spectrotemporally modified vocalization and its original version. Mice were able to discriminate between vocalization types and between manipulated vocalizations, with performance negatively correlating with spectrotemporal similarity. That is, discrimination performance was higher for dissimilar vocalizations and much lower for similar vocalizations. The behavioral data match previous neurophysiological results in the inferior colliculus (IC), using the same stimuli. These findings suggest that the different vocalizations could carry different meanings for the mice. Furthermore, the finding that behavioral discrimination matched neural discrimination in the IC suggests that the IC plays an important role in the perceptual discrimination of vocalizations.     

Frequency sensitivity in the auditory periphery of male and female black-capped chickadees (Poecile atricapillus)

The black-capped chickadee is a songbird that has been used extensively as a model of animal communication in field and laboratory settings. Although many studies have focused on the complex call and song systems of the black-capped chickadee, relatively fewer studies have focused on chickadee audition. However, we do know from behavioral and molecular work that chickadees (and auditory processing areas in their brains) discriminate between artificially generated tones, between conspecific and heterospecific vocalizations, and among different types of conspecific vocalizations. In this paper we investigate peripheral auditory processing of frequency in the black-capped chickadee and the potential influence of sex on frequency sensitivity using a technique called auditory evoked potentials. We found that male and female black-capped chickadees did not differ in any measure of frequency sensitivity. Both sexes had the greatest sensitivity to frequencies between 2 and 4 kHz. This range of frequencies is well represented in black-capped chickadee song, partially supporting the idea that sender and receiver coevolve. Finally, we suggest that the call and song system of North American parids make them an ideal taxonomic group for comparative work exploring the relationship between call systems and the evolution of auditory processing.     

Evidence of neuronal plasticity within the inferior colliculus after noise exposure: a study of evoked potentials in the rat

Recent investigations have implicated that the central nervous system has a role in the changes that occur in auditory function following acoustic trauma caused by noise exposure. These investigations indicate that the inferior colliculus may be the primary anatomical location in the ascending auditory pathway where noise-induced neuronal plasticity occurs, thereby resulting in changes in the neuronal processing of auditory information. In the present investigation, we show that the amplitudes of all peaks in the click-evoked response from the external nucleus of the inferior colliculus decrease during a 30 min exposure to a tone (104 dB sound pressure level (SPL) at 4 kHz and 8 kHz). After tone exposure, the amplitudes of two of the peaks of the response from the external nucleus of the inferior colliculus that reflect the input from more caudal structures slowly returned to baseline levels, whereas the amplitudes of the two peaks reflecting neuronal activity in the inferior colliculus increased above baseline levels and remained at the increased levels for at least 90 min following exposure to the tone.We also show that exposure to a 4 kHz tone at 104 dB SPL causes changes in the neuronal processing of tonebursts in the form of changes in the temporal integration function for one of the peaks of the response from the external nucleus of the inferior colliculus that originates in the inferior colliculus. Before tone exposure the amplitude of this peak decreased with increasing stimulus duration, but after tone exposure the amplitude of this peak was independent of the duration of the toneburst stimulus.We interpret these changes as evidence that noise exposure (tone exposure) causes changes in the excitability of the inferior colliculus that are not seen in more caudal structures, and these changes are probably a result of a change in the balance between inhibition and excitation in the inferior colliculus.     

Adult Plasticity in the Subcortical Auditory Pathway of the Maternal Mouse

Subcortical auditory nuclei were traditionally viewed as non-plastic in adulthood so that acoustic information could be stably conveyed to higher auditory areas. Studies in a variety of species, including humans, now suggest that prolonged acoustic training can drive long-lasting brainstem plasticity. The neurobiological mechanisms for such changes are not well understood in natural behavioral contexts due to a relative dearth of in vivo animal models in which to study this. Here, we demonstrate in a mouse model that a natural life experience with increased demands on the auditory system – motherhood – is associated with improved temporal processing in the subcortical auditory pathway. We measured the auditory brainstem response to test whether mothers and pup-naïve virgin mice differed in temporal responses to both broadband and tone stimuli, including ultrasonic frequencies found in mouse pup vocalizations. Mothers had shorter latencies for early ABR peaks, indicating plasticity in the auditory nerve and the cochlear nucleus. Shorter interpeak latency between waves IV and V also suggest plasticity in the inferior colliculus. Hormone manipulations revealed that these cannot be explained solely by estrogen levels experienced during pregnancy and parturition in mothers. In contrast, we found that pup-care experience, independent of pregnancy and parturition, contributes to shortening auditory brainstem response latencies. These results suggest that acoustic experience in the maternal context imparts plasticity on early auditory processing that lasts beyond pup weaning. In addition to establishing an animal model for exploring adult auditory brainstem plasticity in a neuroethological context, our results have broader implications for models of perceptual, behavioral and neural changes that arise during maternity, where subcortical sensorineural plasticity has not previously been considered.     

Psychophysical and neurophysiological hearing thresholds in the bat <Emphasis Type="Italic">Phyllostomus </Emphasis><Emphasis Type="Italic">discolor</Emphasis>

Absolute hearing thresholds in the spear-nosed bat Phyllostomus discolor have been determined both with psychophysical and neurophysiological methods. Neurophysiological data have been obtained from two different structures of the ascending auditory pathway, the inferior colliculus and the auditory cortex. Minimum auditory thresholds of neurons are very similar in both structures. Lowest absolute thresholds of 0 dB SPL are reached at frequencies from about 35 to 55 kHz in both cases. Overall behavioural sensitivity is roughly 20 dB better than neural sensitivity. The behavioural audiogram shows a first threshold dip around 23 kHz but threshold was lowest at 80 kHz (−10 dB SPL). This high sensitivity at 80 kHz is not reflected in the neural data. The data suggest that P. discolor has considerably better absolute auditory thresholds than estimated previously. The psychophysical and neurophysiological data are compared to other phyllostomid bats and differences are discussed. S. Hoffmann, L. Baier, F. Borina contributed equally to this work.     

Adaptations in the Mouse Auditory System for Perception of Ultrasonic Communication Calls

Ultrasonic calls in the frequency range of 40–80 kHz play an important role in sound communication of house mice. The processing of ultrasounds is enhanced by overrepresentation of the corresponding frequency range in the inferior colliculus and auditory cortex. The latter has an ultrasonic field that is distinct from the tonotopy of the primary auditory cortex and has connections with brain areas of multi-sensory, motivational, and motor control. Mechanisms, such as critical band filtering and categorical perception, ensure that ultrasounds can easily be discriminated from other sounds of the mouse acoustic repertoire.     

Corticofugal regulation of auditory sensitivity in the bat inferior colliculus

Under free-field stimulation conditions, corticofugal regulation of auditory sensitivity of neurons in the central nucleus of the inferior colliculus of the big brown bat, Eptesicus fuscus, was studied by blocking activities of auditory cortical neurons with Lidocaine or by electrical stimulation in auditory cortical neuron recording sites. The corticocollicular pathway regulated the number of impulses, the auditory spatial response areas and the frequency-tuning curves of inferior colliculus neurons through facilitation or inhibition. Corticofugal regulation was most effective at low sound intensity and was dependent upon the time interval between acoustic and electrical stimuli. At optimal interstimulus intervals, inferior colliculus neurons had the smallest number of impulses and the longest response latency during corticofugal inhibition. The opposite effects were observed during corticofugal facilitation. Corticofugal inhibitory latency was longer than corticofugal facilitatory latency. Iontophoretic application of γ-aminobutyric acid and bicuculline to inferior colliculus recording sites produced effects similar to what were observed during corticofugal inhibition and facilitation. We suggest that corticofugal regulation of central auditory sensitivity can provide an animal with a mechanism to regulate acoustic signal processing in the ascending auditory pathway. Accepted: 15 July 1998     

Mouse auditory sensitivity as measured by averaged evoked potentials]

The audition of four strains of mice was determined with summated auditory evoked potentials at the inferior colliculus level. One of these strains was completely deaf. For the 3 others a specific auditory sensitivity was found with statistically different thresholds. But, for these, the best sensitivity is around 16 kHz. Two of them show a flattening of the curve between 32 and 64 kHz. This range corresponds to the ultrasounds emitted by the pups.     

Responses of midbrain auditory neurons in rats to FM and AM tones presented simultaneously

Speech and other communication signals contain components of frequency and amplitude modulations (FM, AM) that often occur together. Auditory midbrain (or inferior colliculus, IC) is an important center for coding time-varying features of sounds. It remains unclear how IC neurons respond when FM and AM stimuli are both presented. Here we studied IC neurons in the urethane-anesthetized rats when animals were simultaneously stimulated with FM and AM tones. Of 122 units that were sensitive to the dual stimuli, the responses could be grossly divided into two types: one that resembled the respective responses to FM or AM stimuli presented separately ("simple" sensitivity, 45% of units), and another that appeared markedly different from their respective responses to FM or AM tones ("complex" sensitivity, 55%). These types of combinational sensitivities were further correlated with individual cell's frequency tuning pattern (response area) and with their common response pattern to FM and AM sounds. Results suggested that such combinational sensitivity could reflect local synaptic interactions on IC neurons and that the neural mechanisms could underlie more developed sensitivities to acoustic combinations found at the auditory cortex.     

Hearing conspecific vocal signals alters peripheral auditory sensitivity

We investigated whether hearing advertisement calls over several nights, as happens in natural frog choruses, modified the responses of the peripheral auditory system in the green treefrog, Hyla cinerea. Using auditory evoked potentials (AEP), we found that exposure to 10 nights of a simulated male chorus lowered auditory thresholds in males and females, while exposure to random tones had no effect in males, but did result in lower thresholds in females. The threshold change was larger at the lower frequencies stimulating the amphibian papilla than at higher frequencies stimulating the basilar papilla. Suprathreshold responses to tonal stimuli were assessed for two peaks in the AEP recordings. For the peak P1 (assessed for 0.8–1.25 kHz), peak amplitude increased following chorus exposure. For peak P2 (assessed for 2–4 kHz), peak amplitude decreased at frequencies between 2.5 and 4.0 kHz, but remained unaltered at 2.0 kHz. Our results show for the first time, to our knowledge, that hearing dynamic social stimuli, like frog choruses, can alter the responses of the auditory periphery in a way that could enhance the detection of and response to conspecific acoustic communication signals.     

Regularly firing neurons in the inferior colliculus have a weak interaural intensity difference sensitivity

The spike discharge regularity may be important in the processing of information in the auditory pathway. It has already been shown that many cells in the central nucleus of the inferior colliculus fire regularly in response to monaural stimulation by the best frequency tones. The aim of this study was to find how the regularity of units was affected by adding ipsilateral tone, and how interaural intensity difference sensitivity is related to regularity. Single unit recordings were performed from 66 units in the inferior colliculus of the anaesthetized guinea pig in response to the best frequency tone. Regularity of firing was measured by calculating the coefficient of variation as a function of time of a unit’s response. There was a positive correlation between coefficient of variation and interaural intensity difference sensitivity, indicating that highly regular units had very weak and irregular units had strong interaural intensity difference sensitivity responses. Three effects of binaural interaction on the sustained regularity were observed: constant coefficient of variation despite change in rate (66% of the units), negative (20%) and positive (13%) rate–CV relationships. A negative rate-coefficient of variation relationship was the dominant pattern of binaural interaction on the onset regularity.     

Tonotopical organization and pure tone response characteristics of single units in the auditory cortex of the Greater Horseshoe Bat

Summary Tonotopical organization and frequency representation in the auditory cortex of Greater Horseshoe Bats was studied using multi-unit recordings.The auditory responsive cortical area can be divided into a primary and a secondary region on the basis of response characteristics forming a core/belt structure.In the primary area units with best frequencies in the range of echolocation signals are strongly overrepresented (Figs. 6–8). There are two separate large areas concerned with the processing of the two components of the echolocation signals. In one area frequencies between the individual resting frequency and about 2 kHz above are represented, which normally occur in the constant frequency (CF) part of the echoes (CF-area), in a second one best frequencies between resting frequency and about 8 kHz below are found (FM-area).In the CF-area tonotopical organization differs from the usual mammalian scheme of dorso-ventral isofrequency slabs. Here isofrequency contours are arranged in a semicircular pattern.The representation of the cochlear partition (cochleotopic organization) was calculated. In the inferior colliculus and auditory cortex there is a disproportionate representation of the basilar membrane. This finding is in contradiction to the current opinion that frequency representation in the auditory system of Horseshoe Bats is only determined by the mechanical tuning properties of the basilar membrane.Response characteristics for single units were studied using pure tone stimuli. Most units showed transient responses. In 25% of units response characteristics depended on the combination of frequency and sound pressure level used.Frequency selectivity of units with best frequencies in the range of echolocation sounds is very high. Q-10dB values of up to 400 were found in a small frequency band just above resting frequency.Abbreviations BF best frequency - CF constant frequency - FM frequency modulated - MT minimal threshold     

Response properties of auditory activated cells in the occipital cortex of the blind mole rat: an electrophysiological study

Previous studies have demonstrated that despite its blindness, the subterranean blind mole rat (Spalax ehrenbergi) possesses a noticeable lateral geniculate nucleus and a typical cyto-architectural occipital cortex that are reciprocally connected. These two areas, as revealed by the metabolic tracer 2-deoxyglucose, are activated by auditory stimuli. Using single unit recordings, we show that about 57% of 325 cells located within the occipital cortex of anesthetized mole rats responded to at least one of the following auditory stimuli — white noise, pure tones, clicks, and amplitude modulated tones — with the latter two being the most effective. About 85% of cells driven by either contralateral or ipsilateral stimulation also responded to binaural stimulation; about 13% responded only to binaural stimulation; and 2% were driven exclusively by contralateral stimulation. Comparing responsiveness and response strength to these three modes of stimulation revealed a contralateral predominance. Mean latency (±SD) of ipsilateral and contralateral responses were 48.5±32.6 ms and 33.5±9.4 ms, respectively. Characteristic frequencies could be divided into two distinct subgroups ranging between 80 and 125 Hz and between 2,500 and 4,400 Hz, corresponding to the most intensive spectral components of the vibratory intraspecific communication signals and airborne vocalizations.Abbreviations BMF best modulation frequency - CF characteristic frequency - 2-DG 2-deoxyglucose - dLGN dorsal lateral geniculate nucleus - IC inferior colliculus - LGN lateral geniculate nucleus - OC occipital cortex - MTF modulation transfer function - SAM sinusoidally amplitude modulation - SC superior colliculus     

Role of a species-specific acoustic environment in the development of hearing in nestlings

Main parameters were studied of the acoustic evoked potentials (EPs) from L field of the caudal neostriatum of altricial nestlings of 2-8 days to pure tones in the range of species-specific signals. It has been established that auditory EPs to the tones of different frequencies differ by the terms of appearance and the degree of maturity. At every of the revealed stages of the auditory ontogenesis, including the stage of completely formed auditory sensitivity, such parameters of auditory EPs, as latencies of different phases, amplitude-temporal pattern and the course of recovery curve are different for the tones of different frequencies. The earliest to appear are the responses to the tones 0.2-4.0 kHz, corresponding to the energy of alimentary signals. Responses to tones of higher frequencies corresponding to the spectrum of other species-specific signals appear later, but the speed of their formation is higher than in the responses to the tones of low frequencies. It is suggested that the higher speed of sensitivity maturation in the high-frequency region is determined by ecologically conditioned afferentation, the function of which is fulfilled by nestlings own vocalization.     

Efficient temporal processing of naturalistic sounds

In this study, we investigate the ability of the mammalian auditory pathway to adapt its strategy for temporal processing under natural stimulus conditions. We derive temporal receptive fields from the responses of neurons in the inferior colliculus to vocalization stimuli with and without additional ambient noise. We find that the onset of ambient noise evokes a change in receptive field dynamics that corresponds to a change from bandpass to lowpass temporal filtering. We show that these changes occur within a few hundred milliseconds of the onset of the noise and are evident across a range of overall stimulus intensities. Using a simple model, we illustrate how these changes in temporal processing exploit differences in the statistical properties of vocalizations and ambient noises to increase the information in the neural response in a manner consistent with the principles of efficient coding.     

Constructing Noise-Invariant Representations of Sound in the Auditory Pathway

Identifying behaviorally relevant sounds in the presence of background noise is one of the most important and poorly understood challenges faced by the auditory system. An elegant solution to this problem would be for the auditory system to represent sounds in a noise-invariant fashion. Since a major effect of background noise is to alter the statistics of the sounds reaching the ear, noise-invariant representations could be promoted by neurons adapting to stimulus statistics. Here we investigated the extent of neuronal adaptation to the mean and contrast of auditory stimulation as one ascends the auditory pathway. We measured these forms of adaptation by presenting complex synthetic and natural sounds, recording neuronal responses in the inferior colliculus and primary fields of the auditory cortex of anaesthetized ferrets, and comparing these responses with a sophisticated model of the auditory nerve. We find that the strength of both forms of adaptation increases as one ascends the auditory pathway. To investigate whether this adaptation to stimulus statistics contributes to the construction of noise-invariant sound representations, we also presented complex, natural sounds embedded in stationary noise, and used a decoding approach to assess the noise tolerance of the neuronal population code. We find that the code for complex sounds in the periphery is affected more by the addition of noise than the cortical code. We also find that noise tolerance is correlated with adaptation to stimulus statistics, so that populations that show the strongest adaptation to stimulus statistics are also the most noise-tolerant. This suggests that the increase in adaptation to sound statistics from auditory nerve to midbrain to cortex is an important stage in the construction of noise-invariant sound representations in the higher auditory brain.     

Distribution of auditory motion-direction sensitive neurons in the barn owl's midbrain

Barn owls have neurons sensitive to acoustic motion-direction in the midbrain. We report here that acoustic motion-direction sensitive neurons with receptive-field centres in frontal auditory space are not randomly distributed. In the inferior colliculus and optic tectum in the left (right) brain, the responses of about two-thirds of the motion-direction sensitive neurons were sensitive to clockwise (counter-clockwise) motion. The midbrain contains maps of auditory space that represent about 15 degrees of ipsilateral and all of contralateral space. Since a similar bias in motion-direction sensitivity was observed for neurons with receptive-field centres in ipsilateral as well as for neurons with receptive fields centres in contralateral auditory space, the brain side at which a motion-direction sensitive neuron was recorded was a more important predictor for the preferred direction of a cell than the spatial direction of the centre of the receptive field. Within one dorso-ventral electrode pass motion-direction sensitivity typically stayed constant suggesting a clustered or even a columnar-like organization. We hypothesize from these distributions that the right brain is important for orientating movements to the left hemisphere and vice versa.