Normal variations in the morphology of auditory brainstem response (ABR) waveforms: a study in wistar rats
Highlights
► We characterize the patterns of ABR waves in Wistar rats. ► We establish criteria that could be used to identify ABR abnormalities in Wistar rats. ► Wave II of the rat ABR is the most prominent wave. ► Wave III of the rat ABR is the smallest and, in many cases, is not apparent. ► We suggest that criteria used to evaluate ABRs in humans are not suitable for rats.
Introduction
The auditory brainstem response (ABR) is an evoked potential recording technique commonly used to study auditory function in either normal or pathological conditions. This technique is easy to use and is non-invasive, making it ideal for use in both clinical and experimental studies. ABRs are recorded far-field from the scalp and are typically comprised of five to seven vertex positive waves that appear within the first 10 ms after an auditory stimulus (Chiappa et al., 1979, Chen and Chen, 1991, Reichmuth et al., 2007, Parkkonen et al., 2009). The localization of the sources or generator of each wave is still unclear (Simpson et al., 1985, Kuwada et al., 1986, Chen and Chen, 1991, Newton et al., 1992, Church et al., 2004, Church et al., 2007, Church et al., 2010, Church et al., 2012, Reichmuth et al., 2007, Parkkonen et al., 2009); however, for most mammalian species, it is generally accepted that the responses of the neuronal activity in the auditory nerve, cochlear nucleus (CN), superior olivary complex (SOC), lateral lemniscus (LL) and inferior colliculus (IC) correspond to waves I, II, III, IV and V, respectively (Simpson et al., 1985, Chen and Chen, 1991, Reichmuth et al., 2007). Nevertheless, several studies have reported noticeable differences between rodent ABRs and the ABRs of other mammals. In the mouse, it has been suggested that wave II is generated by the posterior ventral CN, wave III by the anterior ventral CN and the trapezoid body, wave IV by the SOC and wave V by the LL and the IC (Parham et al., 2001). It has been proposed that in rats, wave IV is generated by the LL and IC and wave V by the medial geniculate body and/or thalamo-cortical radiations (Henry, 1979). Another study in rats using radiofrequency lesions in auditory brainstem nuclei has shown that lesions in the LL are associated with changes in waves IV and V, while lesions in the IC did not significantly affect any ABR waves (Chen and Chen, 1991).
Thus, it is possible that differences in the sources of the ABR waves in different species could lead to functional modifications in the pattern and morphology of the waves. For instance, in humans, waves I, III, and V are the most common and are frequently used to measure ABR parameters, such as inter-peak latencies (see Chiappa, 2007, Burkard and Don, 2007 for review). Waves III and V are also the largest, and therefore, they are often used to determine hearing thresholds and to identify the remaining waves (see Chiappa, 2007, Burkard and Don, 2007 for review). Conversely, wave II is the largest in rats, and wave III is the smallest; wave V is not commonly used for the evaluation of ABR parameters (Overbeck and Church, 1992, Church et al., 2010, Church et al., 2012). Due to these obvious differences, caution should be taken in using ABR measures that are standardized in humans for the evaluation of rat ABRs.
In human ABRs, waves IV and V forming up to six different patterns that include five different complexes, which were observed in 86% of the 52 patients included in an study by Chiappa et al. (1979). According to Chiappa et al. (1979), knowing the normal variations of the waves is a fundamental factor in the interpretation of ABRs. Surprisingly, even though there is a wealth of studies that have evaluated rat ABR parameters, such as threshold, latency and amplitude (Borg, 1982, Chen and Chen, 1991, Newton et al., 1992, Overbeck and Church, 1992, Pukkila et al., 1997, Fujioka et al., 2006, Kujawa and Liberman, 2006, Church et al., 2007, Church et al., 2010, Church et al., 2012, Hougaard et al., 2007, Bielefeld et al., 2008, Hu and Cai, 2010), to date, a detailed characterization of the normal variations found in the morphology and patterns of the ABR waves has not yet been performed. The goal of the current study was to determine and evaluate the patterns of normal ABR waves in Wistar rats, which are one of the most widely used animal models for the study of the auditory function and thus, to establish criteria for the adequate evaluation and diagnosis of the normal ABR and to detect possible abnormalities that may occur after experimental or pathological conditions that induce hearing impairment.
Section snippets
Animals
Data were obtained from 30 adult male Wistar rats. Animals were purchased from Charles River (Barcelona, Spain) and housed at the Universidad de Castilla-La Mancha (Albacete, Spain). Upon arrival, animals were maintained on a 12/12 h light/dark cycle with free access to water and food. All procedures were approved by institutional ethics committees and conformed to Spanish (Royal Decree 1201/2005; Law 32/2007) and European Union (Directive 2010/63/EU) regulations for the use and care of animals
ABR thresholds
Auditory thresholds were calculated for all frequencies used in the present study. Background activity was low and stable at all sound intensity levels and frequencies (Fig. 2). ABR wave amplitudes increased as the sound level increased, although the beginning of this increase seemed to be dependent on the stimulus frequency (Fig. 2). When the mean auditory thresholds of Wistar rats were plotted as a function of frequency, there was an inverse relationship between these factors (Fig. 3). The
Discussion
In the present study, using pure tone sounds at 7 frequencies from 0.5 to 32 kHz, a complete evaluation of the normal variations in the ABR waveform pattern of the Wistar rat was performed. The results demonstrate that in rats there are frequency-dependent variations in the patterns of ABR waveforms, including complexes primarily formed between wave III and either waves IV or II, and less commonly, between waves IV and V. The relationship between complexes and stimulus frequency was demonstrated
Acknowledgments
The authors would like to thank José Julio Cabanes and Mari Cruz Gabaldón for excellent technical assistance. Research was supported by Programa I3 del Ministerio de Ciencia e Innovación (I320101590 to V.F.S and I320101589 to J.C.A.), Gobierno de Castilla-La Mancha (PE110901526233) and Ministerio de Ciencia e Innovación (BFU2009-13754-C02-01).
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