Differences between cerebral activation of analgesia by sucrose and an artificial sweetener in humans

Abstract

Intraoral infusion of sweet taste produces analgesia in adult humans (sweet taste-induced analgesia; SIA) (Kakeda 2010). However, few studies have investigated brain activation associated with SIA (Kakeda et al. 2010). To our knowledge, there is no information on how artificial sweeteners induce SIA in human brain. The aim of this study was to examine the differences between cerebral activation of SIA by sucrose and that by an artificial sweetener, using 3-T functional magnetic resonance imaging (fMRI). The Human Experimentation Committee of Kyushu University approved all experimental procedures. Seven males and seven females (aged 22-33 years) participated in this study. Sucrose solution [24% (w/v)] and the solution of an artificial sweetener (PalsweetTM) [8% (w/v)] were used for generating the sweet condition, while artificial saliva (25 mM KCl with 2.5 mM NaHCO3) was used as the control solution. Sweet and control solutions were alternately applied to the participant’s mouth for 20 sec. The participants were subjected to the cold pressure test which involved applying an ice pack onto the participant’s dorsum manus for 20 sec. During fMRI scanning, participants underwent 5 events: “Sucrose”, “Sucrose + Pain”, “Palsweet”, “Palsweet + Pain” and “Pain + control.” Each event was repeated 12 times randomly. The ice pack was applied to alternate hands in each pain event. Participants pressed a button with their non-stimulated hand when they began to feel the pain. Cerebral activation of SIA by sucrose and Palsweet was compared in four contrasts: “Sucrose + Pain” - “Pain + control”, “Palsweet + Pain” - “Pain + control”, “Sucrose + Pain” - “Palsweet + Pain” and “Palsweet + Pain” - “Sucrose + Pain”. An anatomical mask was applied on the statistical maps involving the taste and pain pathways. Cerebral activation of SIA by sucrose was observed in the right putamen [P < 0.05 FWE-corrected with small volume correction (SVC)]. Cerebral activation of SIA by Palsweet was observed in the left postcentral gyrus, the left ACC, and the right rolandic operculum (P < 0.05 FWE-corrected with SVC). No significant neural activation was observed in “Sucrose + Pain” - “Palsweet + Pain” contrast, whereas neural activation in the right rolandic operculum was detected in “Palsweet + Pain” - “Sucrose + Pain” contrast (P < 0.05 FWE-corrected with SVC). Cerebral activation of SIA by sucrose was observed in the putamen, which is a dopaminergic area related to the behavioral pleasantness response, whereas in “Palsweet + Pain” - “Sucrose + Pain” contrast, neural activation was observed in the pain pathways, possibly suggesting that the effect of SIA by sucrose is more significant than that by Palsweet.