Limbic areas are functionally decoupled and visual cortex takes a more central role during fear conditioning in humans.

Chrysa Lithari,Stephan Moratti,Nathan Weisz

doi:10.1038/srep29220

Abstract

Going beyond the focus on isolated brain regions (e.g. amygdala), recent neuroimaging studies on fear conditioning point to the relevance of a network of mutually interacting brain regions. In the present MEG study we used Graph Theory to uncover changes in the architecture of the brain functional network shaped by fear conditioning. Firstly, induced power analysis revealed differences in local cortical excitability (lower alpha and beta power) between CS+ and CS− localized to somatosensory cortex and insula. What is more striking however is that the graph theoretical measures unveiled a re-organization of brain functional connections, not evident using conventional power analysis. Subcortical fear-related structures exhibited reduced connectivity with temporal and frontal areas rendering the overall brain functional network more sparse during fear conditioning. At the same time, the calcarine took on a more central role in the network. Interestingly, the more the connectivity of limbic areas is reduced, the more central the role of the occipital cortex becomes. We speculated that both, the reduced coupling in some regions and the emerging centrality of others, contribute to the efficient processing of fear-relevant information during fear learning.

Highlights

Going beyond the focus on isolated brain regions, recent neuroimaging studies on fear conditioning point to the relevance of a network of mutually interacting brain regions
The startle responses during the ITIs were significantly higher than both CS+and CS−during habituation and extinction (p < 0.001; leading to the overall negative values), whereas during the conditioning phase they were at the same level with CS+.The differentiated startle response at CS+validates the effectiveness of classical fear conditioning as it indicates a conditioning-specific activation of the defense system[12]
In considering the brain functional network as a complex graph that is dynamically modified in response to, and in anticipation of, environmental changes, we intended to examine how fear conditioning alters the graph structure and properties

Summary

Introduction

Going beyond the focus on isolated brain regions (e.g. amygdala), recent neuroimaging studies on fear conditioning point to the relevance of a network of mutually interacting brain regions. Another fMRI study reported increased connectivity of right amygdala and visual cortex and decreased connectivity of left amygdala and occipito-temporal regions when participants were asked to identify fear faces[6] These studies demonstrate that some regions exhibit fear-related coupling and others decoupling suggesting a re-routing of the functional pathways, which we intend to investigate in the present study. The current study expands the scope of the previous work, on induced responses with a main focus on characterizing connectivity patterns using graph theoretical tools in source space The latter allows the investigation of fear-related differences in the organization of the brain functional network that are not evident with other analysis methods. Since prominent limbic-frontal connectivity is related to emotion regulation[10,11], in a situation like fear conditioning, we expected decoupling phenomena in fear-relevant regions

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