Genetic and neuronal basis for facial emotion perception in humans and macaques

Li Wang; Bo Zhang; Xiqian Lu; Ruidi Wang; Jian Ma; Yujie Chen; Yuan Zhou; Ji Dai; Yi Jiang

doi:10.1093/nsr/nwae381

Genetic and neuronal basis for facial emotion perception in humans and macaques

Natl Sci Rev. 2024 Nov 8;11(11):nwae381. doi: 10.1093/nsr/nwae381. eCollection 2024 Nov.

Authors

Li Wang^{1

2}, Bo Zhang^{3

4}, Xiqian Lu^{1

2}, Ruidi Wang^{1

2}, Jian Ma^{3

5}, Yujie Chen^{1

2}, Yuan Zhou^{1

2}, Ji Dai^{3

5

6

2}, Yi Jiang^{1

2}

Affiliations

¹ State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, Beijing 100101, China.
² Department of Psychology, University of Chinese Academy of Sciences, Beijing 100049, China.
³ Shenzhen Technological Research Center for Primate Translational Medicine, Shenzhen-Hong Kong Institute of Brain Science, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China.
⁴ Key Laboratory of Brain Science, Zunyi Medical University, Zunyi 563000, China.
⁵ CAS Key Laboratory of Brain Connectome and Manipulation, Brain Cognition and Brain Disease Institute, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China.
⁶ Guangdong Provincial Key Laboratory of Brain Connectome and Behavior, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China.

Abstract

The ability to rapidly recognize basic facial emotions (e.g. fear) is crucial for social interactions and adaptive functioning. To date, the origin of facial-emotion-recognition ability remains equivocal. Using a classical twin design in humans, we found a clear dissection of low and high spatial frequencies (LSF and HSF) in facial emotion perception: whereas genetic factors contributed to individual variation in LSF processing, HSF processing is largely shaped by environmental effects. Furthermore, the ability to recognize facial emotions of LSF content genetically correlated with the function of the amygdala. Crucially, single-unit recording of the amygdala in macaques further revealed the dissociation between LSF and HSF processing in facial emotion perception, indicating the existence of an evolutionarily conserved mechanism. This cross-species study enhances insights into the neurobiological dual-route model (subcortical vs. cortical) of emotion perception and illuminates the origin and the functional development of the emotional brain in primates.

Keywords: amygdala; behavioral genetics; facial emotion recognition; spatial frequency; twin study.