Jiří Popelář

Enhancement of the auditory cortex evoked responses in awake guinea pigs after noise exposure

In a previous paper [Popelár et al., Hear. Res. 26, 239-247 (1987)] we have shown that amplitudes of the auditory cortex evoked responses (AC-ER) in awake guinea pigs were enhanced for several hours after 1 h of noise exposure whereas amplitudes of the compound potential of the auditory nerve (CAP) and of the inferior colliculus evoked responses (IC-ER) declined. The present study demonstrates that the duration of the AC-ER amplitude increase is related to the intensity of the noise exposure (white noise, for 30 min or 1 h, intensity range 105-125 dB). The AC-ER amplitude as well as the threshold shift increased linearly with increasing intensity of the noise. The maximum AC-ER increase occurred when clicks served as stimuli; amplitude enhancement was smaller for 1 kHz tone pips and was absent when 20 kHz tone pips were used. The amplitude enhancement was specific for the auditory cortex since the amplitude of visually evoked responses, recorded in the occipital cortex, was unchanged after noise exposure. It is suggested that the postexposure amplitude enhancement of the AC-ER is produced by temporary exhaustion of inhibitory processes in the auditory cortex.

Comparison of Response Properties of Neurons in the Inferior Colliculus of Guinea Pigs Under Different Anesthetics

Responses of the inferior colliculus (IC) neurons to acoustical stimulation were recorded in anesthetized guinea pigs. Three kinds of anesthesia were used: (1) urethane (8 ml/kg b.w. of 20 per cent solution i.p.); (2) ketamine-xylazine combination (1 ml/kg b.w. of mixture 2:1); and (3) pentobarbital (25 mg/kg i.p.) combined with intramuscular injection of fentanyl (0.5 ml) and droperidol (1 ml). The frequency tuning of neurons evaluated on the basis of Q10 values and the composite neural audiogram represented by points of lowest thresholds of individual IC neurons were similar for guinea pigs treated with any of the anesthetics. The number of spontaneously active IC neurons was significantly larger with ketamine than with urethane or pentobarbital. The response latencies to tone bursts at characteristic frequency (CF) were shortest in animals anesthetized with pentobarbital. Whereas with ketamine and urethane many neurons were recorded in which response latencies were longer than 40 ms, in pentobarbital-anesthetized animals the latencies usually did not exceed 25 ms. The occurrence of neurons with an onset type of response was significantly larger with pentobarbital than with the other two anesthetics. In ketamine and urethane anesthesia, thresholds of units with sustained response were significantly lower than thresholds of units with onset response. Our results suggest that in experiments where the level of spontaneous activity, latency and type of responses were important parameters, the kind of anesthesia should be taken into account.

Brief exposure of juvenile rats to noise impairs the development of the response properties of inferior colliculus neurons

Temporary impairment of the auditory periphery during the sensitive period of postnatal development of rats may result in a deterioration of neuronal responsiveness in the central auditory nuclei of adult animals. In this study, juvenile rats (postnatal day 14) were exposed for 8 min to intense broad‐band noise; at the age of 3–6 months, the excitatory and inhibitory response areas of neurons in the central nucleus of the inferior colliculus were recorded under ketamine–xylazine anaesthesia in these animals and compared with those of age‐matched controls. The response thresholds were similar in the exposed and control animals. The frequency selectivity of low‐frequency neurons was comparable in both groups; however, high‐frequency neurons had significantly wider excitatory response areas in the exposed rats, indicating disrupted development of high‐frequency hearing. Forty‐one per cent and 25% of neurons in exposed animals and in controls, respectively, lacked a distinct inhibitory area; these neurons had similar frequency selectivity in the exposed and control rats. As the presence of an inhibitory sideband was associated with sharper frequency tuning in both groups, it appears that lateral inhibition substantially influences neuronal frequency selectivity. If present, the inhibitory areas had comparable bandwidths in both groups; however, they were shifted to the side in the exposed animals, allowing the expansion of the excitatory areas. The results indicate that a brief exposure of juvenile rats to noise leads to a significant worsening of the frequency selectivity of inferior colliculus neurons in adult animals; the poorer frequency selectivity may be due to missing or displaced inhibitory sidebands.

Noise exposure during early development impairs the processing of sound intensity in adult rats

During the early postnatal development of rats, the structural and functional maturation of the central auditory nuclei strongly relies on the natural character of the incoming neural activity. Even a temporary deprivation in the critical period results in a deterioration of neuronal responsiveness in adult animals. We demonstrate that besides the poorer frequency selectivity of neurons in the impaired animals reported previously [ Grecova et al. (2009)Eur. J. Neurosci. 29, 1921–1930], the neuronal representation of sound intensity is significantly affected. Rate–intensity functions of inferior colliculus neurons were recorded in anaesthetized adult rats that were exposed to intense noise at postnatal day 14, and compared with those obtained in age‐matched controls. Although the response thresholds were similar in the exposed and control rats, the neurons in the exposed animals had a longer first‐spike latency, a narrower dynamic range, lower maximum response magnitudes and a steeper slope of the rate–intensity functions. The percentage of monotonic neurons was significantly lower in the exposed animals. The observed anomalies were confined to the mid‐ and high‐frequency regions, whereas no significant changes were found in the low‐frequency neurons. The altered parameters of the individual rate–intensity functions led also to differences in the cumulative responses. We conclude that a brief noise exposure during the critical period leads to a frequency‐dependent alteration of the sound intensity representation in the inferior colliculus of adult rats. The results suggest that such impairments may appear in individuals with normal hearing thresholds, but with a history of noise exposure very early in childhood.

Inactivation of the left auditory cortex impairs temporal discrimination in the rat

The left auditory cortex (AC) in humans is involved in the processing of the temporal parameters of acoustical signals, specifically in speech perception, whereas the right AC plays the dominant role in pitch and melody perception. The hemispheric lateralization of acoustical signal processing in non-human mammals is less explored. The present study examined the ability of rats to detect or discriminate a series of gaps in continuous noise under conditions of unilateral or bilateral reversible inactivation of the AC. The results showed that muscimol-induced reversible inactivation of the left AC suppresses the ability of rats to discriminate between acoustical stimuli of different temporal parameters (duration or repetition rate), whereas inactivation of the right AC results in no change or only a mild decrease in discrimination ability. Hemispheric asymmetry was observed only in the case of gap discrimination tasks, but not in a gap detection task. Our findings demonstrate that, similarly as in humans, the left AC in the rat plays the dominant role in temporal discrimination. These data provide further evidence for the functional asymmetry of the mammalian brain, which appears in a relatively early phase of evolution.

Noise exposure during early development influences the acoustic startle reflex in adult rats

Noise exposure during the critical period of postnatal development in rats results in anomalous processing of acoustic stimuli in the adult auditory system. In the present study, the behavioral consequences of an acute acoustic trauma in the critical period are assessed in adult rats using the acoustic startle reflex (ASR) and prepulse inhibition (PPI) of ASR. Rat pups (strain Long-Evans) were exposed to broad-band noise of 125 dB SPL for 8 min on postnatal day 14; at the age of 3-5 months, ASR and PPI of ASR were examined and compared with those obtained in age-matched controls. In addition, hearing thresholds were measured in all animals by means of auditory brainstem responses. The results show that although the hearing thresholds in both groups of animals were not different, a reduced strength of the startle reflex was observed in exposed rats compared with controls. The efficacy of PPI in exposed and control rats was also markedly different. In contrast to control rats, in which an increase in prepulse intensity was accompanied by a consistent increase in the efficacy of PPI, the PPI function in the exposed animals was characterized by a steep increase in inhibitory efficacy at low prepulse intensities of 20-30 dB SPL. A further increase of prepulse intensity up to 60-70 dB SPL caused only a small and insignificant change of PPI. Our findings demonstrate that brief noise exposure in rat pups results in altered behavioral responses to sounds in adulthood, indicating anomalies in intensity coding and loudness perception.

Representation of species-specific vocalizations in the medial geniculate body of the guinea pig

Individual nuclei of the auditory pathway contribute in a specific way to the processing of complex acoustical signals. We investigated the responses of single neurons to typical guinea pig vocalizations (purr, chutter, chirp and whistle) in the ventral part of the medial geniculate body (MGB) of anesthetized guinea pigs. The neuronal and population peristimulus time histograms (PSTHs) reflected the repetition frequency of individual phrases in the calls. The patterns of PSTHs correlated well with the sound temporal envelope in calls with short phrases (purr, chirp). The dominant onset character of the neuronal responses resulted in a lower correlation between the sound envelope and the PSTH pattern in the case of longer calls (chutter and whistle). A time-reversed version of whistle elicited on average a 13% weaker response than did the natural whistle. The rate-characteristic frequency (CF) profile provided only a coarse representation of the sound frequency spectrum without detailed information about the individual spectral peaks and their relative magnitudes. In comparison with the inferior colliculus (Šuta et al. in J Neurophysiol 90:3794-3808, 2003), the processing of species-specific vocalizations in the MGB differs in: (1) a less precise representation of the temporal envelope in the case of longer calls, but not in the case of calls consisting of one or more short phrases; (2) a less precise rate-CF representation of the spectral envelope in the case of low-frequency calls, but not in the case of broad-band calls; (3) a smaller difference between the responses to natural and time-reversed whistle.

Modulation of thresholds to acoustical and electrical stimulation of the intact ear in guinea pig by furosemide and noise

Middle latency responses (MLR) to acoustical stimulation (AS) and to electrical stimulation (ES) of the intact inner ear were recorded in guinea pigs. ES threshold curve decreased in the frequency range 2-16 kHz with a slope 5.4 dB/octave. Immediately after 50 mg/kg intravenous injection of the furosemide, which resulted in a temporary suppression of the cochlear function, the ES thresholds increased and resembled thresholds found in gentamicin-treated animals. Whereas temporary threshold shift (TTS) at 1 kHz ES was negligible at this time, maximum TTS at 8 kHz and 20 kHz ES was limited to 27 dB and 37 dB resp. TTS to acoustical stimulation was larger than TTS to ES (in some cases exceeded 50 dB) and it was similar at all frequencies. Amplitude-intensity functions (AIF) to high-frequency ES stimuli (20 kHz) consisted of two parts--a flat part at low intensities and a steep part at high intensities of the ES. High-frequency noise exposure (third-octave band noise, centered at 16 kHz, intensity 105 dB for 1 h) reduced or abolished only the flat part of the AIF, the steep part, as well as the responses to low-frequency ES, were not substantially changed. TTS at high frequencies, elicited by the noise exposure, were similar for ES and AS. However, amplitudes of acoustically evoked MLR significantly increased after the noise exposure while MLR amplitudes to ES did not change. The results characterize the frequency-intensity domain of the electrophonic effect in the guinea pig and its changes after influencing the inner ear function by furosemide and noise.

First-spike latency in the presence of spontaneous activity

A new statistical method for the estimation of the response latency is proposed. When spontaneous discharge is present, the first spike after the stimulus application may be caused by either the stimulus itself, or it may appear due to the prevailing spontaneous activity. Therefore, an appropriate method to deduce the response latency from the time to the first spike after the stimulus is needed. We develop a nonparametric estimator of the response latency based on repeated stimulations. A simulation study is provided to show how the estimator behaves with an increasing number of observations and for different rates of spontaneous and evoked spikes. Our nonparametric approach requires very few assumptions. For comparison, we also consider a parametric model. The proposed probabilistic model can be used for both single and parallel neuronal spike trains. In the case of simultaneously recorded spike trains in several neurons, the estimators of joint distribution and correlations of response latencies are also introduced. Real data from inferior colliculus auditory neurons obtained from a multielectrode probe are studied to demonstrate the statistical estimators of response latencies and their correlations in space.

Development of the acoustic startle response in rats and its change after early acoustic trauma.

Even brief acoustic trauma during the critical period of development that results in no permanent hearing threshold shift may lead to altered auditory processing in adulthood. By monitoring the acoustic startle response (ASR), we examined the development of auditory function in control rats and in rats exposed to intense noise at the 14th postnatal day (P14). First ASRs appeared on P10-P11 to intense low-frequency tones. By P14, the range of sound intensities and frequencies eliciting ASRs extended considerably, the ASR reactivity being similar at all frequencies (4-32 kHz). During the subsequent two weeks, ASR amplitudes to low-frequency stimuli (4-8 kHz) increased, whereas the ASRs to high-frequency tones were maintained (16 kHz) or even decreased (32 kHz). Compared to controls, noise exposure on P14 (125 dB SPL for 8, 12, or 25 min) produced transient hyper-reactivity to startle stimuli, manifested by a decrease of ASR thresholds and an increase of ASR amplitudes. ASR enhancement occurred regardless of permanent hearing loss and was more pronounced at high frequencies. The hyper-reactivity of ASRs declined by P30; the ASR amplitudes in adult exposed rats were lower than in controls. The histological control did not reveal loss of hair cells in adult exposed rats, however, the number of inner hair cell ribbon synapses was significantly decreased, especially in the high-frequency part of the cochlea. The results indicate that early acoustic trauma may result in complex changes of ASRs during development.