Abstract
There is growing evidence that the amygdala serves as the base for dealing with complex human social communication and emotion. Although amygdalar networks plays a central role in these functions, causality connectivity during the human lifespan between amygdalar subregions and their corresponding perception network (PerN), affiliation network (AffN) and aversion network (AveN) remain largely unclear. Granger causal analysis (GCA), an approach to assess directed functional interactions from time series data, was utilized to investigated effective connectivity between amygdalar subregions and their related networks as a function of age to reveal the maturation and degradation of neural circuits during development and ageing in the present study. For each human resting functional magnetic resonance imaging (fMRI) dataset, the amygdala was divided into three subareas, namely ventrolateral amygdala (VLA), medial amygdala (MedA) and dorsal amygdala (DorA), by using resting-state functional connectivity, from which the corresponding networks (PerN, AffN and AveN) were extracted. Subsequently, the GC interaction of the three amygdalar subregions and their associated networks during life were explored with a generalised linear model (GLM). We found that three causality flows significantly varied with age: the GC of VLA → PerN showed an inverted U-shaped trend with ageing; the GC of MedA→ AffN had a U-shaped trend with ageing; and the GC of DorA→ AveN decreased with ageing. Moreover, during ageing, the above GCs were significantly correlated with Social Responsiveness Scale (SRS) and State-Trait Anxiety Inventory (STAI) scores. In short, PerN, AffN and AveN associated with the amygdalar subregions separately presented different causality connectivity changes with ageing. These findings provide a strong constituent framework for normal and neurological diseases associated with social disorders to analyse the neural basis of social behaviour during life.
Highlights
Emotional characteristics differ greatly over the human lifespan
The perception network (PerN) is involved with the lateral orbitofrontal cortex, fusiform gyrus (FFA), rostral superior temporal sulcus, ventromedial temporal cortex, temporal pole and subgenual anterior cingulate cortex (ACC); the affiliation network (AffN) is associated with the ventromedial prefrontal cortex, ventral medial striatum of the nucleus accumbens, ventromedial hypothalamus, adjoining subgenual and rACC, dorsomedial temporal pole and medial temporal lobe; and the aversion network (AveN) refers to caudal ACC, ventrolateral striatum, anterior insula, somatosensory operculum, caudolateral hypothalamus, thalamus and brainstem[7,18,19,20,21,22,23,24,25,26,27]
In this study we proposed a novel approach to examine the flows of Granger causality (GC) between the amygdalar subregions (VLA, medial amygdala (MedA) or dorsal amygdala (DorA)) and their corresponding networks (PerN, AffN or AveN) during the entire human lifespan based on an age-related generalised linear model (GLM)
Summary
Emotional characteristics differ greatly over the human lifespan (from development to ageing). Other studies have suggested that the amygdala is a key hub in social cognitive and emotional systems, and it is involved in face perception together with fusiform gyrus[8,9]. Www.nature.com/scientificreports the amygdala could contribute to the integrative processing of social information that underlies the awareness of other individual’s affective experiences in complex social perception. Previous research about lifespan emotional changes focused on the amygdala as a whole[13], but some studies suggested that the amygdalar role in cognition, disapproval and sympathy might be separable. The perception network (PerN) is responsible for social perceptual abilities, the affiliation network (AffN) is related to prosocial behaviours and the aversion network (AveN) contributes to antipathetic processes. The connectivity within/between functional networks separately presented inverted/upright U-shaped trends[29,30]. The lateral frontal and parietal lobe exhibit an inverted and upright U-shaped trend, respectively[31]
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