Sex differences in brain activation elicited by humor

Abstract

With recent investigation beginning to reveal the cortical and subcortical neuroanatomical correlates of humor appreciation, the present event-related functional MRI (fMRI) study was designed to elucidate sex-specific recruitment of these humor related networks. Twenty healthy subjects (10 females) underwent fMRI scanning while subjectively rating 70 verbal and nonverbal achromatic cartoons as funny or unfunny. Data were analyzed by comparing blood oxygenation-level-dependent signal activation during funny and unfunny stimuli. Males and females share an extensive humor-response strategy as indicated by recruitment of similar brain regions: both activate the temporal-occipital junction and temporal pole, structures implicated in semantic knowledge and juxtaposition, and the inferior frontal gyrus, likely to be involved in language processing. Females, however, activate the left prefrontal cortex more than males, suggesting a greater degree of executive processing and language-based decoding. Females also exhibit greater activation of mesolimbic regions, including the nucleus accumbens, implying greater reward network response and possibly less reward expectation. These results indicate sex-specific differences in neural response to humor with implications for sex-based disparities in the integration of cognition and emotion.

Fig. 1.

Event-related cartoon presentation and behavioral results. (a) Task design. Funny (I) and unfunny (II) stimuli were presented in an event-related paradigm with each cartoon presented in random order for 6,000 ms. A jittered inter-stimulus interval (ISI) of 2,000, 4,000, and 6,000 ms was varied randomly and counterbalanced across events (see Materials and Methods for more details). (b) Behavioral results. We found no between-sex differences in the number of stimuli found funny [t(17.531) = -0.029, P < 0.977], the subjective degree of funniness [t(17) = 0.895, P < 0.383], or the response time (RT) to funny [t(17.99) = 0.20, P < 0.944] or unfunny [t(16.22) = -0.769, P < 0.453] stimuli. Males show no within-sex RT differences to funny and unfunny cartoons [t(9) = -0.20, P < 0.984], whereas female RT is significantly shorter for unfunny stimuli [t(9) = 2.949, P < 0.016]. Error bars indicate SD.

Fig. 2.

BOLD signal activation for funny - unfunny cartoons. Clusters of activation were superimposed on a Talairach-normalized brain by using mricro software. Significance of activation was determined by using the joint expected probability distribution (36) with height (P < 0.05) and extent (P < 0.05) corrected for the whole brain. Males demonstrate cortical activation of the temporal-occipital junction (FG/ITG) (BA 37), the temporal pole, and STG (BA 38), as well as the IFG (BA 44). Females show activation of the temporal-occipital junction (FG/ITG) (BA 37), the temporal pole, and STG (BA 38), extending into the DLPFC, IFG, and MFG (BA 44/45/46), as well as subcortical dopaminergic reward regions, including the NAcc.

Fig. 3.

Female - male activation: time-series analysis of NAcc and DLPFC. Female - male comparison shows greater female activation in the DLPFC, IFG, and MFG (BA 45, 46, and 47), as well as the NAcc. Averaged time-series analysis for funny vs. unfunny activity in a 10-voxel subcluster of the NAcc (stereotaxic coordinates, 6, 2, -4; P < 0.0001) reveals strong female activation during funny stimuli and little activity during unfunny events. Males show low activation during funny stimuli and deactivation during unfunny events. A 477-voxel cluster extending through the DLPFC (peak stereotaxic coordinates, -44, 10, 28; P < 0.05) shows similar male and female response to unfunny stimuli and a noticeably more robust female response when they find the cartoon funny. Sex differences were significant for the NAcc-Funny, NAcc-Unfunny, DLPFC-Funny time-series curves (P ≤ 0.001), but not for the DLPFC-Unfunny curves (P = 0.95).

Fig. 4.

Female NAcc activation covarying with degree of humor intensity. Parametric analysis (see Materials and Methods) reveals NAcc activity (stereotaxic coordinates, 6, 2, -4; P < 0.0001) covarying with subjective rankings of humor intensity in females but not in males. Female - male comparison of NAcc activity shows significant increase in disparity as humor intensity increases [t(18) = 4.702, P < 0.0005].