The effects of intragastric infusion of umami solutions on amygdalar and lateral hypothalamic neurons in rats

Abstract

Previous behavioral studies have suggested that l-glutamate, an umami substance, is detected in the gut, and that this information regarding glutamate is conveyed from the gut to the amygdala and the lateral hypothalamus (LH) through the vagus nerve to establish glutamate preference. In this study, we investigated the roles of the amygdala and LH in the information processing of gut glutamate. We recorded the activity of amygdalar and LH neurons during the intragastric administration of five test solutions (monosodium l-glutamate [MSG, 60 mmol/L]; inosine monophosphate [IMP, 60 mmol/L]; a mixture of MSG and IMP; NaCl [60 mmol/L]; or physiological saline) in intact and subdiaphragmatic vagotomized awake rats. In intact rats, 349 and 189 neurons were recorded from the amygdala and LH, respectively, while in vagotomized rats, 104 and 90 neurons were recorded from the amygdala and LH, respectively. In intact rats, similar percentages of neurons (30–60%) in the amygdala and LH responded to the intragastric infusion of the solutions. Vagotomy significantly altered responses to the MSG and NaCl solutions. In particular, vagotomy suppressed the inhibitory responses to the NaCl solution. Furthermore, vagotomy increased the response similarity between the MSG and NaCl solutions, suggesting that vagotomy impaired the coding of the postingestive consequences of the MSG solution in the amygdala and LH, which are unique for glutamate. The present results provide the first neurophysiological evidence that amygdalar and LH neurons process glutamate signals from the gut.

Flavor Preferences Conditioned by Dietary Glutamate

“…Uematsu et al (27) showed that rats that had a total abdominal vagotomy did not learn to prefer a flavor paired with intragastric MSG. Consistent with this observation, vagotomy also altered the neural response to intragastric MSG in the amygdala and lateral hypothalamus, which was taken as evidence that it blocked the coding of positive postingestive actions of glutamate (34). This contrasts with our findings that vagal surgical or chemical denervation does not block postoral carbohydrate or fat conditioning (35), which, in turn, is consistent with the lack of change in forebrain response to glucose after vagotomy (36).…”

Rewarding Effects of Operant Dry-Licking Behavior on Neuronal Firing in the Nucleus Accumbens Core

“…Surgical procedures have been described previously ( Matsumoto et al, 2012 ; Davaasuren et al, 2015 ). Briefly, rats were anesthetized with sodium pentobarbital (40 mg/kg; intraperitoneal, i.p.).…”

“…Food exerts its reinforcing effects on the brain reward system via both gustatory (oral-sensory) and post-ingestive pathways ( Li et al, 2002 ; Jang et al, 2007 ; Margolskee et al, 2007 ; Dotson et al, 2010 ; Fernstrom et al, 2012 ). A previous neurophysiological study reported that intragastric (IG) infusion of amino acids changed neuronal activity in the lateral hypothalamus and amygdala ( Davaasuren et al, 2015 ). Furthermore, studies have suggested that hepato-portal glucose sensors, which act as an unconditioned stimulus for the acquisition of a learned-food-preference ( Delaere et al, 2013 ) and regulates several physiological functions such as glucose utilization ( Burcelin et al, 2000 ), may directly influence dopaminergic activity.…”

Insights into the role of neuronal glucokinase

“…LHA glucokinase may also mediate glucoprivic feeding through direct connections between the LHA and the gut, as diet restriction induced neuronal activation of the LHA in mice ( 143 ). This brain-gut connection appears to occur via the vagus nerve and may be bidirectional, as vagotomy impaired LHA neuronal activation induced by intragastric infusions of various glutamate-containing solutions ( 38 , 171 ).…”