Event-related nociceptive arousal enhances memory consolidation for neutral scenes

Abstract

The superior memory for emotional events has been attributed to the beneficial effects of noradrenaline released into the amygdala attributable to arousal. Noradrenaline mediates the effects of different hormones and neurotransmitters, including adrenal stress hormones on consolidation (McGaugh, 2004; Roozendaal et al., 2009). The majority of human fMRI studies of the enhancement of emotional memories contrasted successful encoding of emotionally arousing and neutral stimuli (LaBar and Cabeza, 2006; Murty et al., 2010). Recently, it was highlighted that emotional stimuli elicit not only arousal but also intensify cognitive processes that contribute to the enhanced memory. In particular, the enhanced use of selective attention as well as the greater distinctiveness and semantic relatedness of emotional stimuli influence memory formation (Talmi et al., 2007a). The present study aimed to explore the effects of arousal on memory formation independent of these cognitive factors in an event-related manner. Arousal was induced by the application of a nociceptive stimulus briefly after the presentation of neutral scenes. The results show a purely arousal-driven memory enhancement for the neutral scenes that differs in critical aspects from the superior memory for emotional stimuli. In particular, the enhancement was only evident after consolidation and exclusively based on an increase in item familiarity but not recollection. Moreover, successful memory formation for stimuli followed by arousal was correlated with activity in the parahippocampal cortex but not the amygdala, as is the case for emotional stimuli.

Figure 1.

Top, Percentage of hits. Bottom, Estimates for recollection (R) and familiarity (d′). A, Day 1 group. B, Day 2 group. C, Day 2-fMRI group. In the day 2 group, familiarity is enhanced for scenes^+shock (light gray) compared with scenes^{no shock} (dark gray) (*p < 0.01). Whiskers reflect the SEM.

Figure 2.

Amygdala activity associated with nociceptive stimulation. Parameter estimates (mean ± SEM) in the peak voxel for the right amygdala are depicted for hits (H) and misses (M) in both conditions (scenes^{no shock} compared with scenes^+shock). For visualization purposes, a threshold of p < 0.001 uncorrected was applied.

Figure 3.

Arousal-induced subsequent memory effect. Activation of the right parahippocampal gyrus is associated with a subsequent memory effect for scenes followed by shock (scenes^+shock) compared with scenes not followed by shock (scenes^{no shock}). Parameter estimates (mean ± SEM) in the peak voxel are depicted for hits (H) and misses (M) in both conditions. For visualization purposes, a threshold of p < 0.001 uncorrected was applied.