Elsevier

Hearing Research

Volume 206, Issues 1–2, August 2005, Pages 177-184
Hearing Research

Responses to species-specific vocalizations in the auditory cortex of awake and anesthetized guinea pigs

https://doi.org/10.1016/j.heares.2005.01.013Get rights and content

Abstract

Species-specific vocalizations represent an important acoustical signal that must be decoded in the auditory system of the listener. We were interested in examining to what extent anesthesia may change the process of signal decoding in neurons of the auditory cortex in the guinea pig. With this aim, the multiple-unit activity, either spontaneous or acoustically evoked, was recorded in the auditory cortex of guinea pigs, at first in the awake state and then after the injection of anesthetics (33 mg/kg ketamine with 6.6 mg/kg xylazine). Acoustical stimuli, presented in free-field conditions, consisted of four typical guinea pig calls (purr, chutter, chirp and whistle), a time-reversed version of the whistle and a broad-band noise burst. The administration of anesthesia typically resulted in a decrease in the level of spontaneous activity and in changes in the strength of the neuronal response to acoustical stimuli. The effect of anesthesia was mostly, but not exclusively, suppressive. Diversity in the effects of anesthesia led in some recordings to an enhanced response to one call accompanied by a suppressed response to another call. The temporal pattern of the response to vocalizations was changed in some cases under anesthesia, which may indicate a change in the synaptic input of the recorded neurons. In summary, our results suggest that anesthesia must be considered as an important factor when investigating the processing of complex sounds such as species-specific vocalizations in the auditory cortex.

Introduction

Most information about the function of the mammalian sensory systems (including the auditory system) has been accumulated in electrophysiological studies performed on anesthetized animals. Anesthesia, similarly as a state of vigilance (Edeline et al., 2001), can affect sensory processing, therefore the investigator must be aware of the influences of anesthetics on neural processing and the relevancy of the obtained data when interpreting results in a non-anesthetized animal. The first studies of unit activity in the auditory cortex already demonstrated strong effects of anesthesia. Anesthesia was found to reduce the number of units encountered by a micro-electrode (Katsuki et al., 1959) and to reduce the capacity of units to respond to auditory stimuli (Thomas, 1952; Erulkar et al., 1956). Several studies reported a mainly suppressive effect of various anesthetics on spontaneous activity in different subcortical nuclei (e.g., pentobarbital, chloralose, and halothane, Evans and Nelson, 1973; pentobarbital, Kuwada et al., 1989; ketamine and pentobarbital, Zurita et al., 1994), but less is known about the impact of anesthetics on sound-evoked activity in the auditory system and signal processing in neuronal circuits. Kisley and Gerstein (1999) reported that the variability of stimulus-evoked responses in the cortex is modulated by the depth of ketamine anesthesia. The authors showed that trial-to-trial variability was usually lowest under light anesthesia and highest under moderate anesthesia. Gaese and Ostwald (2001) found a loss of tuning in some neurons and a sharpening of the frequency response areas in other neurons in the auditory cortex (AC) of the rat after pentobarbital/chloral hydrate anesthesia.

The effect of anesthesia on the processing of acoustical information has been studied not only at the cortical level, but also at subcortical levels of the auditory system such as the cochlear nucleus (Anderson and Young, 2004), the inferior colliculus (Astl et al., 1996; Torterolo et al., 2002) and the medial geniculate body (Massaux et al., 2004).

The effects of anesthesia seem to be even more important when we attempt to understand the processing of sounds such as species-specific vocalizations. These calls are typically complex sounds characterized by time-varying amplitudes and spectral features (Syka et al., 1997; Šuta et al., 2003). It is possible that the processing of such sounds in the auditory cortex depends on the level of vigilance of the animal, especially in the case of calls with a high behavioral impact. The aim of this study was therefore to investigate the effects of ketamine–xylazine anesthesia on the responses of neurons in the auditory cortex of the guinea pig to a set of spectrally and temporally different complex sounds – guinea pig calls. The responses of multiple units in the auditory cortex of the guinea pig were recorded first in an awake and weakly restrained animal and then after the injection of the anesthetic.

Section snippets

Animal preparation

Experiments were performed on 12 adult, healthy, pigmented male guinea pigs, 3–9 months old (mean age 6 ± 1.7 months), weighing 300–500 g. The care and use of animals reported in this study were approved by the Ethics Committee of the Institute of Experimental Medicine and followed the guidelines of the Declaration of Helsinki.

Recording of neuronal activity in the AC

Neuronal activity in the AC was recorded by either of two procedures. In the first procedure, four platinum–iridium electrodes (Bionic Technologies, impedance 0.5–2 MΩ)

Results

The results are based on 20 multiple-unit (MU) recordings in 12 guinea pigs for which reliable records were obtained in both states, i.e., awake as well as anesthetized.

The spontaneous activity under anesthesia was positively correlated with the level of spontaneous activity in awake animals (R2 = 0.64). Ketamine–xylazine anesthesia reduced spontaneous neural activity on average to 79% of the activity level present in an awake animal (means of 16.4 spikes/s in awake animals vs. 13.0 spikes/s in

Discussion

The results of our experiments demonstrate a significant influence of ketamine–xylazine anesthesia on the responses of neurons in the auditory cortex of the guinea pig to complex acoustical stimuli such as species-specific vocalizations. The strength of the response and the temporal pattern of the response are modified in many AC neurons. The effect is, however, not uniform since the administration of anesthesia may increase the response to some types of stimuli and suppress the response to

Acknowledgments

The study was supported by the Grant Agency of the Czech Republic (GA CR No. 309/04/1074) and the Grant Agency of the Ministry of Health of the Czech Republic (NR 8113-4).

References (29)

  • M. Elhilali et al.

    Comparison of response characteristics in auditory cortex of the awake and anesthetized ferret

    Assoc. Res. Otolaryngol. Abst.

    (2002)
  • S.D. Erulkar et al.

    Single unit activity in the auditory cortex of the cat

    Johns. Hopk. Hosp. Bull.

    (1956)
  • E.F. Evans et al.

    The responses of single neurons in the cochlear nucleus of the cat as a function of their location and anaesthetic state

    Exp. Brain Res.

    (1973)
  • E.F. Evans et al.

    Classification of unit responses in the auditory cortex of the unanaesthetized and unrestrained cat

    J. Physiol.

    (1964)
  • Cited by (54)

    • Degraded cortical temporal processing in the valproic acid-induced rat model of autism

      2022, Neuropharmacology
      Citation Excerpt :

      One limitation of the present study is that we recorded cortical responses in the animals anesthetized with pentobarbital. It has been shown that anesthesia significantly affects the spontaneous rate, the spectral and temporal responses, and the spatial tuning properties of auditory cortical neurons (Lu et al., 2001; Liang et al., 2002; Mickey and Middlebrooks, 2003; Syka et al., 2005; Scott et al., 2007; Zhou and Wang, 2012). However, anesthesia probably would not create a bias in measuring changes in cortical responses induced by VPA exposure because identical anesthetic conditions were applied for both animal cohorts during recording.

    • Stream segregation in the anesthetized auditory cortex

      2015, Hearing Research
      Citation Excerpt :

      It is likely that anesthesia accentuates the effects of forward suppression in our data compared with responses in an awake animal. While urethane lowers average cortical firing rates (Albrecht and Davidowa, 1989; Capsius and Leppelsack, 1996; Syka et al., 2005), we are unaware of any studies directly comparing adaptation under urethane with awake responses. Ketamine significantly increases the duration of suppression by preceding stimuli in auditory cortex (Rennaker et al., 2007).

    • Response properties underlying selectivity for the rate of frequency modulated sweeps in the auditory cortex of the mouse

      2013, Hearing Research
      Citation Excerpt :

      The first is that mechanisms were assessed under ketamine/xylazine/isoflurane anesthesia. In the auditory cortex, ketamine reduces spontaneous and sound-evoked activity (Syka et al., 2005; Zurita et al., 1994). Thus it is likely that response magnitudes reported in this study are under-estimates relative to responses from awake animals.

    View all citing articles on Scopus
    View full text