Effective connectivity of the amygdala during the consumption of erotic, sexual humor, and monetary rewards with a DCM-PEB approach

PLoS One. 2022 Dec 29;17(12):e0279281. doi: 10.1371/journal.pone.0279281. eCollection 2022.

Abstract

While a large body of research exists on the processing of monetary rewards, less is known about sexual reward processing. This study aimed to identify effective connectivity for the consumption of sexual (erotic and sexual humor) and non-sexual (monetary) rewards, using dynamic causal modeling and parametric empirical Bayes with subjective hedonic ratings included. Our results support the importance of the amygdala for sexual humor amusement, the nucleus accumbens (NAc) for monetary rewards, and the lateral orbitofrontal cortex (lOFC) for erotic pleasure. The amygdala, NAc, and lOFC are major dopaminergic targets with known roles in the reward circuitry. Appreciating sexual humor was associated with ventral tegmental area (VTA) to amygdala connectivity. Enjoying monetary gains was associated with VTA-to-NAc and amygdala-to-NAc connectivity. The mesolimbic dopamine system originates in the VTA and sends major projections to the amygdala and NAc. Specifically, sexual humor appreciation was associated with effective connectivity from the ventromedial prefrontal cortex (vmPFC) to the amygdala, suggesting that subjective pleasure triggers activation of the vmPFC which exerts an excitatory influence on the amygdala. Unexpectedly, processing pleasure from monetary gains was linked to VTA-to-vmPFC connectivity, rather than the expected vmPFC-to-NAc connectivity. Importantly, we identified core roles for the amygdala. Sexual humor appreciation was associated with VTA-to-amygdala and vmPFC-to-amygdala effective connectivity, while we found amygdala-to-lOFC connectivity for erotic pleasure and amygdala-to-NAc connectivity for pleasure from monetary gains. Our findings represent an important step in understanding how effective connectivity in the mesocorticolimbic-amygdala circuitry differs for processing the consumption of sexual and monetary rewards.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amygdala* / physiology
  • Bayes Theorem
  • Magnetic Resonance Imaging
  • Nucleus Accumbens* / diagnostic imaging
  • Nucleus Accumbens* / physiology
  • Prefrontal Cortex / diagnostic imaging
  • Prefrontal Cortex / physiology
  • Reward

Grants and funding

This study was supported by a grant from the Ministry of Science and Technology of Taiwan (MOST 105-2410-H-007-027-MY2) and the Yin Shu-Tien Educational Foundation (NTHU-YS-B-2018003).