Effects of electrical and chemical stimulation of the amygdala on the spontaneous discharge in the insular cortex in rats

Abstract

Both the amygdala (especially, the basolateral nucleus of the amygdala) and the insular cortex are important for conditioned taste aversion. From the anatomical view point, there are reciprocal connections between the insular cortex and the amygdala. In the present study, we investigated the effect of electrical and chemical stimulation of the amygdala on the spontaneous discharge of the insular cortex neurons in anesthetized rats. In most neurons (10 of 14), spontaneous discharge was decreased after a microinjection of glutamate (Glu). In these neurons, the injection site was within the basolateral nucleus of the amygdala (the basolateral/lateral nuclei). On the other hand, when a γ amino-butyric acid (GABA) was microinjected into the basolateral nucleus of the amygdala, none of the 5 neurons showed any change in spontaneous discharge. Electrical train stimulation of the basolateral nucleus of the amygdala (100 Hz, 2–6 s) depressed the spontaneous discharge of the neurons in the insular cortex, as in the case of a Glu microinjection. These results indicate that activation of the basolateral nucleus of the amygdala could depress the neuronal activity in the insular cortex. Such results may yield data leading to the elucidation of the neuronal mechanisms of conditioned taste aversion.

Introduction

It is known that the anterior and posterior portions of the rat insular cortex are the cortical taste area and the cortical visceral area, respectively, although a distinct zone separating these two sensory cortices has not been clearly shown (Yamamoto et al., 1980, Cechetto and Saper, 1987, Ogawa et al., 1990). It has been reported that there is a chemotopic distribution among taste stimuli (or among the taste nerves) in the gustatory cortex (Yamamoto et al., 1980, Yamamoto et al., 1985, Yoshimura et al., 2004, Sugita and Shiba, 2005, Accolla et al., 2007). Furthermore, it has been reported that the neurons showing multimodal sensitivity (responsive to taste, visceral and nociceptive stimuli) are widely localized in the insular cortex (Hanamori et al., 1997, Hanamori et al., 1998a, Hanamori et al., 1998b, Ogawa and Wang, 2002, Hanamori, 2005). The insular cortex, which receives stimuli from various sensory organs, appears to have complicated functions.

In addition to its role in taste sensation and recognition, the insular cortex has been shown to be important for conditioned taste aversion (c.f., Yamamoto et al., 1995). The insular cortex is believed to be important for keeping the taste memory of a conditioning taste stimulus for a long time in connection with post-ingestional malaise induced by the application of an unconditioned stimulus. Some reports have shown the molecular mechanisms (Bermúdez-Rattoni, 2004) or long-term potentiation (Jones et al., 1999, Escobar and Bermúdez-Rattoni, 2000) in the insular cortex. These data may support the idea that the insular cortex is involved in taste memory (or taste learning). Recently, it has also been reported that the insular cortex is significantly involved in the gustatory neophobia learning (Gutiérrez et al., 2003, Reilly and Bornovalova, 2005).

The amygdala, which is crucial to emotional processing, has been demonstrated to be important for fear conditioning (Ledoux et al., 1990, Paré et al., 2004). Similarly, it has been shown that the amygdala is also an important nucleus for conditioned taste aversion (Yamamoto et al., 1995, Yasoshima et al., 1995). Anatomically, it has been demonstrated that the insular cortex has reciprocal neuronal connections with the amygdala (Saper, 1982, Shi and Cassell, 1998). The neuronal connection between the insular cortex and the amygdala has also been reported electrophysiologically (Yamamoto et al., 1981, Veinante and Freund-Mercier, 1998, Quirk et al., 2003). Many studies have indicated the importance of the neuronal network between the insular cortex and the amygdala for conditioned taste aversion. Recently, it was shown that a Glu microinjection to the amygdala enhances taste aversion through NMDA receptor activation in the insular cortex (Ferreira et al., 2005). Moreover, it has been reported that the acquisition of conditioned taste aversion was disrupted by the injection of blockers of the Glu receptors to the amygdala (Yasoshima et al., 2000). Furthermore, electrical tetanic stimulation to the basolateral amygdala induced long-term potentiation of the insular cortex neurons and enhanced conditioned taste aversion (Escobar and Bermúdez-Rattoni, 2000).

The existence of GABAergic neurons in the amygdala has been reported anatomically (McDonald, 1985, Sun et al., 1994). It has been demonstrated that GABAergic neurons may contribute to the function of the amygdala in fear conditioning (Muller et al., 1997, Paré et al., 2004). Also, GABAergic neurons seem to be involved in conditioned taste aversion. It has been shown that an injection of midazolam, a benzodiazepine agonist, into the basolateral nucleus of the amygdala induced impairment on the expression of conditioned taste aversion (Yasoshima and Yamamoto, 2005).

To investigate the neuronal connection between the insular cortex and the amygdala, the effects of electrical and chemical stimulation of the amygdala on the spontaneous discharge of the neurons in the insular cortex were investigated in anesthetized rats. The results showed that electrical or chemical activation of the basolateral nucleus of the amygdala induced the depression of the spontaneous discharge in the insular cortex neurons (the basolateral nucleus of the amygdala is defined as the basolateral/lateral nuclei in this report).