The effects of nembutal anesthesia on the auditory steady-state response (ASSR) from the inferior colliculus and auditory cortex of the chinchilla

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Abstract

We examined the effects of nembutal anesthesia on the amplitude of the auditory steady-state response (ASSR) in the inferior colliculus (IC) and auditory cortex (AC) of the chinchilla. Tungsten electrodes were chronically implanted following anesthesia with ketamine/acepromazine. After a recovery period, the chinchillas were placed in a passive restraining device and put in a sound-attenuating booth. Recordings were made from the right IC and AC simultaneously, while a two-tone stimulus was presented to the left ear. The stimuli consisted of two equal-level tones (F1 and F2) that were mixed acoustically; F1 remained constant at 2000 Hz, while F2 varied between 2029 and 2249 Hz, in steps of ∼20 Hz. The stimuli decreased in 10 dB steps from 80 to 30 dB pSPL. Animals were evaluated when unanesthetized, as well as when anesthetized with nembutal (on separate days).

In the IC, the administration of nembutal resulted in either no change in ASSR amplitude or an amplitude increase for difference tone (DT) frequencies below 90 Hz, while an amplitude decrease was typically seen for DT frequencies at or above 90 Hz. In the AC, a decrease in amplitude was seen across DT frequencies and stimulus levels after the administration of nembutal anesthesia. Our results suggest that both the AC and IC may contribute to the scalp-recorded ASSR in the awake state. However, in the nembutal-anesthetized state, it seems unlikely that the AC contributes substantially to the surface-recorded ASSR, as the AC response was greatly attenuated under nembutal anesthesia. In contrast, the IC ASSR responses remained robust, which makes it a likely contributor to the surface-recorded responses under nembutal anesthesia.

Introduction

The auditory steady-state response (ASSR) is a physiological response that follows the envelope of the stimulus (Kuwada et al., 1986, Kuwada et al., 2002, Arnold and Burkard, 2002). It can be obtained by presenting the ear with periodic stimuli such as clicks or tonebursts, with continuous stimuli that are amplitude-modulated (AM), or with two-tone stimuli (F1, F2) (Dolphin et al., 1994, Galambos and Makeig, 1992). While the DT or MF is not seen in the acoustic signal, they can be observed in the evoked response due to nonlinearities of the auditory system (Arnold and Burkard, 2002).

The ASSR has been studied in humans (Dimitrijevic et al., 2002, Reyes et al., 2003, Pantev et al., 1996, Dobie and Wilson, 1998) as well as a variety of non-human animals (Kiren et al., 1994, Kuwada et al., 2002, Makela et al., 1990). One of the advantages of using an animal model is in the ability to use near-field electrodes, which allows recordings to be dominated by a known brain region. In chinchillas, using DTs of 20, 40, 80, 160 and 320 Hz, Arnold and Burkard (2002) found that the dominant frequency in the inferior colliculus (IC) was either 80 or 160 Hz, depending on stimulus level, while the dominant frequency from the auditory cortex (AC) was 80 Hz. Arnold and Burkard (2002) used broad frequency steps, and hence details about the chinchilla modulation rate transfer function (MRTF) from the IC and AC are not known.

The ASSR can be used clinically for the estimation of threshold in infants and young children (Cone-Wesson et al., 2002, Rance et al., 1995, Aoyagi et al., 1994a). There are effects of state of arousal/anesthesia on these responses (Gilron et al., 1998, Tiitinen et al., 1993; Jerger et al., 1986; Linden et al., 1985; Plourde and Picton, 1990), and these effects are dependent on the modulation frequency that is used. Studies have shown that the ASSR to lower modulation frequencies (∼40 Hz) are more affected by level of arousal or anesthesia than higher modulation frequencies (>∼70 Hz) (Cohen et al., 1991, Aoyagi et al., 1993, Levi et al., 1993). Although this technique shows promise for hearing screening and threshold estimation, one of the limitations in the clinical application of the ASSR is that its generators are not known.

The purpose of the present experiment is to define with greater resolution the MRTFs for both the IC and AC of the chinchilla. Defining these functions will aid in determining the contributions of the IC and AC to scalp-recorded responses, as well as optimal stimulation parameters. In addition, we would like to determine the effects of anesthesia on the ASSR, which will also provide insight into where the response is being generated. One theory is that high-frequency modulators arise primarily from the brainstem, while low-frequency modulators come primarily from cortex (Kuwada et al., 1986). As nembutal anesthesia depresses cortical function (i.e., the animal is rendered unconscious), we hypothesize that the ASSR to low frequency DTs from the cortex will be affected by the anesthesia, while responses from the IC will be relatively unaffected, regardless of DT.

Section snippets

Surgical procedures

Eleven adult chinchillas were used to examine the effects of nembutal on the ASSR. Two of the 11 chinchillas lost their electrode cap before data collection could be completed, and as a result were excluded from the study. One chinchilla, which received the anesthesia intraperitoneally, died during data collection and was also excluded from the study. Data was collected and analyzed on a total of eight chinchillas, 7 female and 1 male, with weight ranging from 476 to 578 g. All eight of the

IC and AC responses

Fig. 1, Fig. 2 are examples of the recordings obtained from the IC (DT = 70 Hz) and AC (DT = 51 Hz) in both the time and frequency domains. In the time domain (left panels of each figure), both the IC and AC responses follow the envelope of the stimulus presented to the ear. The ASSR in the frequency domain is shown on the right side of Fig. 1, Fig. 2. Note that there is typically a response at the DT frequency, as well as several of the harmonics.

Inferior colliculus

Fig. 3 shows the mean MRTF from the IC in the

Peaks in the modulation rate transfer function

In this investigation, small frequency steps were used to try and provide a greater resolution of the MRTFs from the IC and AC of the chinchilla. Previous studies, such as Arnold and Burkard (2002), used broad frequency steps to measure the MRTFs from the chinchilla IC and AC. In the IC, they found that the peak in the MRTF was dependent on stimulus level. At high stimulus levels (such as 80 dB pSPL) they found that the peak occurred at 160 Hz, while at moderate stimulus levels (such as 60 dB

Conclusions

In the IC, nembutal caused a significant decrease in ASSR amplitude for most modulation frequencies at and above 90 Hz. This was true for several stimulus levels. Interestingly, nembutal produced an increase in IC ASSR amplitude for several modulation frequencies below 90 Hz. Again, this was seen for multiple stimulus levels. In the AC, nembutal produced a decrease in ASSR amplitude, which was seen across modulation frequency and stimulus level. The magnitude of this decrease was greater in the

Acknowledgments

Yuqing Guo is thanked for his help with surgically implanting the electrodes for this study. Work supported by NIH NIDCD DC03600.

References (27)

  • B. Cone-Wesson et al.

    The auditory steady-state response: comparisons with the auditory brainstem response

    Journal of the American Academy of Audiology

    (2002)
  • A. Dimitrijevic et al.

    Estimating the audiogram using multiple auditory steady-state responses

    Journal of the American Academy of Audiology

    (2002)
  • R. Dobie et al.

    Low-level steady-state auditory evoked potentials: effects of rate and sedation on detectability

    Journal of the Acoustical Society of America

    (1998)
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