Significant differences were observed in the cerebral processing of taste information between OB and NW in response to a sucrose solution, regardless the time (morning or afternoon) or the session (eating a standard lunch or fasting). The main difference was reflected by an increase in P1 GEP latencies (recorded in Cz, Pz and Fz) in OB compared with NW. This increased in GEP latencies might correspond to a slowing of the neural signals from peripheral receptors to primary cortical areas (24). Furthermore, the significant increase in latencies observed in NW after intake compared to the pre-prandial period was not observed in OB. In addition, correlations between GEP latencies and acylated ghrelin or insulin, observed in NW, were not encountered in OB, whose hormonal levels were markedly different from those of NW.
This study is the first to investigate the specificities of GEP before and after lunch in a population of OB. It has been reported that cortical activities of OB process taste information differently than NW. These differences have been observed in GEP (26), in fMRI studies during gustatory stimulations or food presentation (13, 19, 35, 36). In that way, several authors noted that OB have an increase of their primary gustatory cortex reactivity compared to NW (21, 37–39), although others showed that after ingesting glucose, OB display a decreased response in the orbito-frontal cortex compared with NW (21, 40, 41). A longitudinal study in OB also noted hyperactivation of the insula and prefrontal cortex in subjects who have lost weight (42). Our study provides novel information concerning the differences of taste cortical activity between OB and NW. Despite a generally accepted higher activation in the primary taste cortex in OB according to the fMRI studies, present GEP (Cz, Pz, Fz) results highlight a slower activation in these areas which does not exclude a sustained activation. Our results reinforce the conclusions of the study by Hardikar et al which concludes with a difference in cerebral response to salty and sweet stimulations recorded by GEP in OB and NW (26).
Results obtained in NW confirm the findings of our previous study (24) with a significant increase in P1 latency of GEPs after food intake. Change in brain response could be explained by habituation (43, 44) or negative alliesthesia originating from the gut (45, 46). Food intake modifies internal homeostasis, which would modify the gustatory cortex activity, especially the insula, and as a result the pleasure induced by food (24, 43, 44). As OB did not display the changes in P1 latency, this would indicate a lack of response to food intake or to changes in the internal milieu reflecting a genuine maladaptation of the brain's response to gustatory stimuli after intake.
The slower GEP responses in OB and the lack of their delays after food intake in OB could be related to higher plasmatic levels of leptin and insulin associated with lower plasmatic levels of acylated ghrelin compared with NW. P1 latency correlates positively with leptin and insulin, and negatively with acylated ghrelin when analyses were performed considering all subjects. In NW, negative correlation between P1 latency and acylated ghrelin on the one hand, and a trend to positive correlation between P1 latency and insulin on the other hand are noted. However, these correlations disappear in OB. These results are concordant with fMRI studies since leptin supplements for leptin-deficient adults have been shown to reduce fMRI activation in several gustatory areas in response to pictures (47), in leptin-deficient adolescents whether fed or fasted (48) and OB (49), especially following weight loss (49). For insulin, fMRI studies suggest that insulin mainly reduces the rewarding effects of food (50, 51) but also parts of the secondary gustatory cortex (50, 52). Concerning the ghrelin effect, it has been observed in fMRI studies, attenuation of response in brain regions regulating reward and feeding after food intake which has been attributed to a decrease in circulating ghrelin (52, 53) and in contrast, the primary gustatory cortex and amygdala were activated by ghrelin injections (54). Elevated ghrelin levels is also accompanied by greater postprandial activation to food pictures in the primary and the secondary gustatory cortices in Prader–Willi patients when compared with healthy controls (55). Taken together, these results suggest that alterations in cortical processing of taste stimuli could be related to the hormonal changes observed in obesity (brain resistance to leptin and insulin and the defect in ghrelin secretion) bringing the subjects into a vicious circle of overeating.
Some limitation of this GEP study compared to the fMRI studies is link to its poor special resolution in spite of its best temporal discrimination. As the insula is an integral part of the primary gustatory cortex (56), its activity cannot be recorded by GEP because it is located too deep within the brain. Therefore, additional studies combining the 2 techniques could provide new insights into the functioning of taste and food-related brain activities in OB. Another limitation is that the sex ratio does not correspond to what is observed in epidemiological studies. The recruitment of voluntary subjects did not allow us to respect this one. Nevertheless, we respected the sex ratio in the groups, which are therefore completely comparable. Difference in GEPs between men and women cannot be statistically valid from the results of this experiment. Indeed, we compared GEPs parameters in men and women in another previous study (32) and no significant difference was observed between genders. Another limitation is the lack of blood sampling for evaluation of glycaemia. This blood analysis was not performed because the subjects were not fasting at the beginning of the sessions (they had to breakfast at home). However, before inclusion, we checked that they had no diabetes mellitus. In addition, our study was only interested in the evoked gustative potentials of sweet tastes. It would also be interesting to test other tastes (acid, sour, bitter, umami) and especially the fat taste (27), a palatable taste seemed to be altered in obesity (7, 13). Food, with its discriminative and hedonic qualities, is a key element of reward-based energy intake. An alteration in the brain reward system for highly palatable energy-rich foods could be one of the main factors involved in the development of obesity by increasing the consumption of fat-rich foods which in turn, could induce a decrease in the taste of fat (by a negative feedback mechanism) as frequently reported (13). Finally, one of the main limitations of the study is that energy intake during lunch should have been measured. However, we made the choice to place ourselves in real life conditions to study the cerebral activity by GEPs and not the eating behavior or the ingesta. Likewise, we made the choice to place the subjects in real life alimentary conditions for breakfast. Breakfast respected dietary habits and was identical in the two sessions. This procedure seemed to be more relevant than imposing a standard breakfast that did not conform to the usual. It was difficult to interpret the difference in the feeling of hunger between NW and OB. The differences could result from a higher leptin level in OB and even more, from a well-known cognitive control that OB manifest when placed in experimental conditions.
In conclusion, this GEPs study showed that there are changes in brain response following the delivery of a sweet taste stimulus in OB compared to NW. In addition, GEP P1 latencies lengthened after a lunch in NW and remained unchanged in OB. These changes in GEPs correlated negatively with plasmatic concentrations of acylated ghrelin and positively with those of leptin and insulin. These results suggest that cortical processing of taste stimuli could be modified in OB. Further studies are needed to determine whether these changes are the cause or the consequence and to better understand how hormones influence brain activity in response to taste stimuli. It would also be interesting to test other tastes and especially the fat taste, a palatable taste seemed to be altered in obesity.