Major histocompatibility complex peptide ligands as olfactory cues in human body odour assessment

Abstract

In many animal species, social communication and mate choice are influenced by cues encoded by the major histocompatibility complex (MHC). The mechanism by which the MHC influences sexual selection is a matter of intense debate. In mice, peptide ligands of MHC molecules activate subsets of vomeronasal and olfactory sensory neurons and influence social memory formation; in sticklebacks, such peptides predictably modify the outcome of mate choice. Here, we examine whether this evolutionarily conserved mechanism of interindividual communication extends to humans. In psychometric tests, volunteers recognized the supplementation of their body odour by MHC peptides and preferred 'self' to 'non-self' ligands when asked to decide whether the modified odour smelled 'like themselves' or 'like their favourite perfume'. Functional magnetic resonance imaging indicated that 'self'-peptides specifically activated a region in the right middle frontal cortex. Our results suggest that despite the absence of a vomeronasal organ, humans have the ability to detect and evaluate MHC peptides in body odour. This may provide a basis for the sensory evaluation of potential partners during human mate choice.

Figure 1.

Preference for body odour supplemented with ‘self’ stimuli. Participants indicated preference on a scale from +3 to −3. Although participants took part in several trials, only the mean values were used to avoid pseudo-replication. Preference is shown for all sessions of non-smokers without a cold (left), non-smokers with a cold (middle), and smokers without a cold (right). Mean±s.e.m.; *p = 0.0167, two-tailed.

Figure 2.

Activation of the right middle frontal cortex by ‘self’-peptides. Activated areas are visualized in a T1-weighted structural template. (a) Transverse section; this section encompasses parts of the right middle and inferior frontal cortex as ROI (outlined). The t-values for activations induced by ‘self’-peptides relative to solvent are indicated on a blue-to-green scale, those for ‘self’-peptides relative to ‘non-self’-peptides on a red-to-yellow scale. Note the co-localization of the activated regions. (b) Sagittal section with ROIs indicated. (c) Coronal section with ROIs indicated. (d) Spatial activation profile for ‘self’-peptide relative to solvent. The MNI coordinates are indicated as are the colour-coded t-values (P(FWE)corr = 0.074; height threshold was set to p < 0.001 (Bonferroni-corrected) and extend threshold to k = 3 (see (f) for contrast estimates). (e) Spatial activation profile for ‘self’-peptide relative to ‘non-self’-peptide. The MNI coordinates are indicated as are the colour-coded t-values (P(FWE)corr = 0.111); height threshold was set to p < 0.001 (Bonferroni-corrected) and extend threshold to k = 3 (see (f) for contrast estimates). (f) Contrast estimates for selected regions after stimulation with ‘self’-peptides. *,p < 0.001, Bonferroni-corrected. Activated areas are visualized in a T1-weighted structural template.