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