Human cerebellum and corticocerebellar connections involved in emotional memory enhancement

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.

Keywords: cerebellum; dynamic causal modeling; emotional memory enhancement; episodic memory; fMRI.

Fig. 1.

Clusters showing an increased activation for enhanced emotional memory encoding within the discovery sample. Clusters span voxels significantly activated during enhanced emotional memory encoding (P_{whole-brain-FWE-corrected} < 0.05, n = 944). These clusters were used as ROIs to explore the connectivity of the cerebellar cluster (ROI 12). Different colors denote different clusters. (A) Three-dimensional images of the 29 clusters. (B) Sagittal, coronal, and horizontal views, focusing on the cluster located in the cerebellum (ROI 12). L, left; R, right. See SI Appendix, Figs. S3–S7 for additional illustrations.

Fig. 2.

Increase in the strength of cerebellar connections during enhanced emotional memory encoding. Green edges indicate an increased connection from the cerebellum to a target ROI, while the other colors represent an increased connection from the ROI to the cerebellum. The width of the edges denotes the strength of the increase in connectivity in the replication sample. Only replicating connections are depicted (discovery sample n_max = 902, n_mean = 887, n_min = 798; replication sample n_max = 433, n_mean = 426, n_min = 378; posterior probability > 0.99; SI Appendix, Table S1). For a detailed breakdown of anatomical localization per ROI, see SI Appendix, Table S5. For connection strength values, see SI Appendix, Tables S6–S9. For additional illustrations, see SI Appendix, Figs. S8–S10.