The locus ceruleus is involved in the successful retrieval of emotional memories in humans

Abstract

Emotional memories are better remembered than neutral ones. The amygdala is involved in this enhancement not only by modulating the hippocampal activity, but possibly also by modulating central arousal. Using functional magnetic resonance imaging, we analyzed the retrieval of neutral faces encoded in emotional or neutral contexts. The pupillary size measured during encoding was used as a modulator of brain responses during retrieval. The interaction between emotion and memory showed significant responses in a set of areas, including the amygdala and parahippocampal gyrus. These areas responded significantly more for correctly remembered faces encoded in an emotional, compared with neutral, context. The same interaction conducted on responses modulated by the pupillary size revealed an area of the dorsal tegmentum of the ponto-mesencephalic region, consistent with the locus ceruleus. Moreover, a psychophysiological interaction showed that amygdalar responses were more tightly related to those of the locus ceruleus when remembering faces that had been encoded in an emotional, rather than neutral, context. These findings suggest that the restoration of a central arousal similar to encoding takes part in the successful retrieval of neutral events learned in an emotional context.

Figure 1.

Experimental design.

Figure 2.

Mean pupillary changes for different trial types in a typical subject. A, Encoding session. The pupillary size is stable during baseline (fixation cross). During context presentation, the arousal induced by the context images influences the pupillary size. Face presentation induces a decrease in pupillary size because of both accommodation and light reflex (related to the white background of face images). Pupil dilatation then stabilizes, allowing a reliable measure. The average pupillary size recorded in the analysis window was introduced in the fMRI data analysis. B, Retrieval session. The pupillary measure is stable during the presentation of the face and the questions.

Figure 3.

fMRI data. Significant responses during successful recognition of faces encoded in emotional context are shown. Top panels, Functional results are displayed on the mean structural MR image, normalized to the same stereotactic space (display at p < 0.001, uncorrected). Bottom panels, Corresponding parameter estimates (arbitrary units ± SD). neu, Neutral; neg, emotional; Rec, recognized faces; Forg, forgotten faces. A, B, Right amygdala. C, D, Parahippocampus gyrus (display at p = 0.005, uncorrected). E, F, Middle temporal sulcus. G, H, Inferior frontal cortex.

Figure 4.

fMRI data. Significant responses during successful recognition of faces encoded in emotional context, modulated by the pupillary size recorded at encoding. A, Locus ceruleus, displayed on the mean structural MR image, normalized to the same stereotactic space. B, Parameter estimates of the responses in the LC, modulated by the pupillary size observed at encoding (arbitrary units ± SD).

Figure 5.

Psychophysiological interaction. PPI results (in red) overlap with the LC detected in the interaction contrast reported in Figure 4 (in yellow).