Blood oxygenation level-dependent functional magnetic resonance imaging of bilateral but asymmetrical responses to gustatory stimulation in the rat insular cortex
Research highlights
► We established a BOLD fMRI method to investigate the responses to gustatory stimulation in rats. ► BOLD signals were observed in the insular cortex in response to a sucrose solution. ► Intrasubject and intersubject reproducibility of the BOLD signals was confirmed. ► The BOLD signals were observed in the insular cortex of both hemispheres, but they were asymmetrical.
Introduction
Food detection and discrimination are critical for ensuring that animals respond appropriately to their environment, for example, to mediate nutrient ingestion, maintain energy balance, and reject poisons. Neuronal mechanisms of the gustatory system depend on neuronal ensemble codes of the multisensory properties of intraoral taste stimuli under physiological states. Although the molecular basis for peripheral transduction events at the receptor level to detect taste has been reported, the neuronal mechanisms underlying taste discrimination and perception at a higher cortical level are not well understood. In the gustatory system, the insular cortex has been identified as the primary gustatory cortex, which receives taste information from the taste periphery via the gustatory thalamic nucleus (Kosar et al., 1986, Nakashima et al., 2000).
Electrophysiological methods have been used to investigate the gustatory system in vivo (Yamamoto et al., 1980, Yamamoto et al., 1981, Yamamoto et al., 1984, Kosar et al., 1986, Yamamoto and Yuyama, 1987, Ogawa et al., 1990, Ogawa et al., 1992, Hanamori et al., 1998). Although single or several neuronal responses in a defined region (e.g., the insular cortex) can be measured with fine temporal resolution by electrophysiological recording, this method provides lesser spatial information regarding the chemotopic organization of neuronal responses. Optical imaging of intrinsic signals has been used to determine the representation of coding for basal tastants in the rat and pig insular cortices (Yoshimura et al., 2004, Accolla et al., 2007). Although this technique has fine spatial resolution for a local region, it is difficult to apply for identifying intrinsic signals due to stimulation in both insular cortices of the rodent simultaneously.
Functional magnetic resonance imaging (fMRI) is a powerful tool in basic and applied neuroscience to map brain activation noninvasively. It has been applied successfully to investigate the gustatory responses to tastants in the human brain (Faurion et al., 1999, Barry et al., 2001, Cerf-Ducastel et al., 2001). Most human fMRI studies have shown that activation is predominant in one hemisphere of the gustatory cortex, indicating asymmetrical activation. These results suggest that electrophysiological recording and optical imaging in a rodent model, usually applied in one hemisphere of the insular cortex for taste function, provide different conclusions. fMRI can provide an understanding of brain function by enabling the visualization of responses of different brain regions and supplementing the in vitro and invasive data that provide molecular background knowledge on neuronal communication. Thus, it is imperative to utilize an fMRI method to bridge the gap between fMRI, electrophysiological recording, and optical imaging while investigating small animal models. In the present study, we established a blood oxygen level-dependent (BOLD) fMRI method at 7 T to investigate the responses to gustatory stimulation in the insular cortex of a rat model.
Section snippets
Animal preparation
Male Sprague–Dawley rats (220–310 g, n = 15) were initially anesthetized with 4% isoflurane. Then, intraperitoneal catheters (PE-50) were placed for administration of urethane. Their whiskers were cut to avoid signal contamination in the somatosensory cortical region. After these procedures, the use of isoflurane was discontinued and urethane (0.8 g/kg) was administered. Each animal continued spontaneous breathing throughout the experiment. Body temperature was monitored with a rectal thermometer
Reproducibility of functional mapping
Functional mapping to code taste information must be reproducible in repeated stimulations and across animals. Fig. 1 shows forebrain activation in a single animal during sucrose stimulation. After each fMRI run, rinsing with distilled water to remove the tastant and removal of distilled water by airflow on the tongue, and sufficient interval between stimulations, BOLD responses in each run were reproducibly conserved. Sucrose solution (0.5 M) produced a significant BOLD signal increase in the
Discussion
By rinsing and removing the tastant from the animal's tongue and oral cavity in the fMRI setup, reproducible functional maps were successfully obtained across stimulations and animals. To the best of our knowledge, this study is the first to demonstrate functional mapping of insular cortical responses to taste stimulation by using fMRI based on BOLD contrast in the rodent.
BOLD fMRI in small animals has been successfully used for investigating somatosensory (Hyder et al., 1994, Kida and
Acknowledgments
We would like to thank Eiji Yamada (Nuclear Magnetic Resonance Laboratory, Hokkaido University) for technical support. This work was supported by JSPS KAKENHI (no. 21791803 to I.K.).
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