Blood oxygenation level-dependent functional magnetic resonance imaging of bilateral but asymmetrical responses to gustatory stimulation in the rat insular cortex

Abstract

Evidence has suggested asymmetrical processing of taste in the human insular cortex, but this phenomenon has not been demonstrated in the rodent brain. Functional magnetic resonance imaging (fMRI) is a powerful tool for studying the functional organization of the brain. In this study, we established a blood oxygenation level-dependent (BOLD) fMRI method at 7 T to investigate the responses to gustatory stimulation in the insular cortex of anesthetized rats (220–310 g, n = 15). BOLD signals were observed in the insular cortex in response to 0.5 M sucrose solution as the tastant but not observed in response to distilled water as the control. The reproducibility of the BOLD signals in response to the tastant was confirmed between fMRI runs in the same animal and across animals. The signals were mainly located between 2.3 mm and 0.0 mm anterior to the bregma in the insular cortex. Interestingly, the signals were observed in the insular cortex of both hemispheres, but they were asymmetrical: the anterior and posterior regions to the intersection of the middle cerebral artery and the rhinal fissure as the landmark of the gustatory cortex were dominant in the left and right hemispheres of the insular cortex, respectively. These results suggest that activity in both hemispheres of the insular cortex should be considered to analyze taste processing. We think that BOLD fMRI of taste function in rodents will improve our understanding of taste information processing.

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.