Human cerebellum and corticocerebellar connections involved in emotional memory enhancement

Matthias Fastenrath, Klara Spalek, David Coynel https://orcid.org/0000-0001-5028-5807, +7 , Eva Loos, Annette Milnik https://orcid.org/0000-0002-3933-3289, Tobias Egli, Nathalie Schicktanz https://orcid.org/0000-0002-6049-6306, Léonie Geissmann https://orcid.org/0000-0002-1175-652X, Benno Roozendaal, Andreas Papassotiropoulos https://orcid.org/0000-0002-2210-9651, and Dominique J.-F. de Quervain https://orcid.org/0000-0001-7131-2464 dominique.dequervain@unibas.ch-7Authors Info & Affiliations
Edited by James McGaugh, University of California Irvine, Irvine, CA; received March 21, 2022; accepted August 9, 2022
October 3, 2022
119 (41) e2204900119
https://doi.org/10.1073/pnas.2204900119
 

Significance

Enhanced memory for emotional stimuli is crucial for survival, but it may also contribute to the development and maintenance of fear-related disorders in case of highly aversive experiences. This large-scale functional brain imaging study identifies the cerebellum and cerebellar–cerebral connections involved in the phenomenon of superior memory for emotionally arousing visual information. These findings expand knowledge on the role of the cerebellum in complex cognitive and emotional processes and may be relevant for the understanding of psychiatric disorders with aberrant emotional circuitry, such as posttraumatic stress disorder or autism spectrum disorder.

Abstract

Emotional information is better remembered than neutral information. Extensive evidence indicates that the amygdala and its interactions with other cerebral regions play an important role in the memory-enhancing effect of emotional arousal. While the cerebellum has been found to be involved in fear conditioning, its role in emotional enhancement of episodic memory is less clear. To address this issue, we used a whole-brain functional MRI approach in 1,418 healthy participants. First, we identified clusters significantly activated during enhanced memory encoding of negative and positive emotional pictures. In addition to the well-known emotional memory–related cerebral regions, we identified a cluster in the cerebellum. We then used dynamic causal modeling and identified several cerebellar connections with increased connection strength corresponding to enhanced emotional memory, including one to a cluster covering the amygdala and hippocampus, and bidirectional connections with a cluster covering the anterior cingulate cortex. The present findings indicate that the cerebellum is an integral part of a network involved in emotional enhancement of episodic memory.

https://www.pnas.org/doi/full/10.1073/pnas.2204900119